Background This report details the case
histories of two women who suffer from chronic
and debilitating episodes of excessive yawning
in the absence of sleep problems.
Methods Each woman independently provided
information and answered questions about their
excessive yawning symptoms and medical
histories.
Results Both women show signs of
thermoregulatory dysfunction, and each reports
symptom relief and/or the postponement of
yawning attacks through means of behavioral
cooling. One woman recorded her body temperature
before and after bouts of yawning, revealing a
significant drop in temperature following each
episode (p<O.O5).
Conclusions The trigger for yawning in these
patients appears to be related to increases in
body/brain temperature. These cases are
consistent with growing evidence showing that
recurrent episodes of excessive yawning are not
necessarily associated with a sleep disorder,
but rather may be indicative of thermoregulatory
dysfunction.
Introduction
For most people, yawning occurs in a
consistent fashion throughout life, with
frequent instances of yawning occurring during
the first hour after waking and the last hour
before sleeping [1-3]. Excessive yawning
is generally viewed as a symptom reflecting a
sleep disorder and/or sleep deprivation.
Contrary to popular belief, however, the
frequency of yawning is not correlated with
sleep duration [3].
There is little consensus as to the
functional significance of yawning [4].
One commonly held view is that yawning functions
to equilibrate oxygen levels in the blood;
however, yawning is unaffected in subjects that
breathe increased levels of oxygen or carbon
dioxide [5]. Recent evidence suggests
that yawning is involved in thermoregulation and
may act as a brain cooling mechanism [6,
7]. According to this model, increases in
facial blood flow resulting from a yawn operate
like a radiator removing hyperthermic blood from
the face and head, while introducing cooler
blood from the lungs and extremities. The
respiratory and arterial actions triggered by a
yawn are similar to those that promote cerebral
cooling [6, 7]. In addition, excessive
yawning has been linked to certain medical
conditions involving abnormal thermoregulation
(e.g., multiple sclerosis and epilepsy), and
research reveals that yawning occurs before,
after, and during instances of heat stress or
hyperthermia [7].
The brain cooling hypothesis is consistent
with the fact - that the incidence of yawning
follows a circadian pattern [1-3].
Thermoregulation and sleep are interconnected,
and the temperature changes before and after
sleep act in a positive feedback loop as core
body temperature and sleep vary inversely
[8]. For instance, body temperature
begins to peak in the evening and the onset of
sleep initiates a decline in the core body
temperature curve, and likewise, the tendency to
wake-up occurs in tandem with a rise in core
body temperature in the morning. Therefore, the
highest frequency of yawning occurs when body
temperature is highest in the evening, and when
it rises in the morning.
Here, we report two women who suffer from
recurring episodes of excessive and debilitating
yawning that include symptoms of
thermoregulatory dysfunction. Neither woman
reports sleep problems, nor have they been
accurately diagnosed.
Materials and methods
Two women independently contacted us about
their experience with chronic bouts of
debilitating yawning. One patient is a
39-year-old woman from South Africa and the
other is a 61-year-old woman from the USA. Both
are Caucasian, college educated, married,
reasonably healthy, and have children. Each
patient was asked to describe their symptoms and
to provide their medical histories regarding
their condition. The local university
institutional review board approved this
research and both individuals gave consent to
participate in this study.
Case 1
The first person to contact us was a
39-year-old woman from South Africa. She is 1.72
m tall and weighs 62 kg. Her previous medical
history included chicken pox and whooping cough
as a child and malaria once as an adult. She was
diagnosed with polycystic ovulatory syndrome and
insulin resistance while flying to conceive, and
was treated with metformin, which resolved the
problem. Her blood pressure is normal and her
cholesterol is slightly high, but she does not
take medication for it.
Her pathological yawning attacks began 8
years ago and due to the extreme debilitating
nature of these episodes (i.e., inability to
walk, feeling ill, or extreme discomfort), she
immediately sought medical assistance. She has
seen 13 doctors about this problem, including
two general practitioners; four neurologists; a
dentist; an endocrinologist; an ear, nose, and
throat specialist; two physicians; a
maxillofacial surgeon from a headache clinic;
and a neuropsychologist. She has received
diagnoses of narcolepsy, pathological yawning,
seizure, migraine activity, excessive daytime
sleepiness, and insulin resistance. Blood tests
have shown nothing other than high fasting
insulin levels, confirming insulin resistance.
Magnetic resonance imaging (MRI) has revealed no
problems, MSLT and polysomnograms are negative
for narcolepsy and hypersomnolence, and EEG is
normal. Diagnoses which have been ruled out are
narcolepsy and excessive daytime sleepiness. She
has been prescribed a number of drugs including
reactivan, metformin, sodium valproate,
modafinil, folie acid supplementation, and
5-hydroxytryptophan. All have either provided
only temporary relief or worsened the
problem.
She typically gets 8 h of sleep at night.
She never experiences these attacks while
sleeping; however, they are often the last thing
she experiences at night. She notes that on some
days, relief only comes when she falls asleep,
and she may retire early in an attempt to end
the attacks.
Case 2
The second person to contact us was a
61-year-old woman from the USA. She is 1.65 m
tall and weighs 96.5 kg. Her medical history
includes the removal of one ovary, she has had
her veins stripped twice in her left leg, a
herniated disc, alpha 1 -antitrypsin deficiency,
and has had carpal tunnel surgery on her right
hand. Her blood pressure is normal and she takes
Lipitor for high cholesterol.
Her chronic yawning bouts began 3 years ago,
and she sought medical assistance 6 months after
the onset. She has been to two general
practitioners and two neurologists, but has not
been offered a diagnosis for her condition, with
multiple sclerosis, Parkinson's disease, and Lou
Gehrig's disease all being ruled out. She has
had two MRIs with no evidence of abnormality.
She has not been prescribed any medication for
her condition.
She gets 7-8 h of sleep at night and does
not report feeling tired during the day. She
sometimes experiences the onset of negative
symptoms prior to sleeping and reports having
woken up in deep sleep to a yawn attack. She
took part in a sleep study and was diagnosed
with sleep apnea but not narcolepsy. She was
given a continuous positive airflow pressure
machine (CPAP) for treatment of apnea. She
reports an improvement in sleep following the
use of the device, but her yawning attacks have
not changed.
Results
Both of their symptoms are very similar.
Each complains of unpredictable and uncontrolled
yawning attacks lasting from 5 to 45 min. During
these excessive yawning episodes, they
experience deep, recurrent, overwhehning yawns
that cause their eyes to water and nose to run.
Occurring one to 15 times a day, these attacks
are very aversive and debilitating, and both
patients report feeling ill and exhausted
following an attack. The most common diagnosis
is a sleep disorder, although neither patient
reports sleep problems.
These cases include features consistent with
a diagnosis of thermoregulatory dysfunction.
Both patients report that nasal breathing and/or
applying cool cloths to the forehead can provide
temporary relief and/or postpone the onset of an
attack. These effects are consistent with
evidence that nasal breathing and facial cooling
reduce brain temperature (9,10), and research
has shown that nasal breathing and forehead
cooling diminish the incidence of yawning
[6). Taking a cold shower or swimming in
cold water after the onset of an attack produces
complete remission of symptoms for the South
African woman. Both patients report feeling cold
during or after an attack and experience goose
bumps and shivering which may be a consequence
of overcompensation by cooling mechanisms
activated during thermoregulatory dysfunction.
Each patient has also noticed that eating a
large meal increases the likelihood of an
attack. One obvious effect of food ingestion is
to divert blood to the stomach and small
intestine, which may occur at the expense of
sending cooler blood from the periphery to the
brain and compromise brain cooling as a
result.
The woman from the USA can anticipate the
onset of these yawning episodes and has taken
oral measurements of her temperature using a
digital thennometer (nearest 0.1°C) at the
beginning and after a number of attacks. Her
average temperature at the start of an attack
was 37.5'C, compared with 37.1°C after an
attack (Wilcoxon signed-ranks test,
Z=-2.194,p=0.03), and her body temperature went
down in nine out of ten instances (sign test,
p=O.O2). The other woman has taken a variety of
different medications, but none have provided
consistent long-term relief. At one point, she
was given modafinil (Provigil), prescribed for
patients with narcolepsy, but it made her
attacks more severe. This is particularly
interesting because modafinil has been shown to
elevate core temperature and impair cooling
responses [11].
Discussion
Contrary to popular opinion, yawning is not
related to blood levels of oxygen or carbon
dioxide [s1. Instead, growing evidence
suggests that yawning acts as a thermoregulatory
mechanism [6, 7). According to this model,
increases in facial and cerebral blood flow
following a yawn operate like a radiator,
removing hyperthermic blood from the face and
head, while introducing cooler blood from the
lungs and extremities.
These cases suggest that excessive yawning
is not indicative of a sleep disorder, and
instead include features consistent with a
diagnosis of thermoregulatory dysfunction.
The woman from the USA was diagnosed with
sleep apnea, yet this was corrected with a CPAP,
and her yawning persists. The same woman reports
a significant reduction in body temperature
following a bout of yawning, and the other
reports that her symptoms were exacerbated while
taking drugs shown to elevate core body
temperature. In addition, both women report that
nasal breathing and forehead coohng provide
symptom relief and/or postpone the onset of an
attack.
These findings suggest that the trigger for
excessive yawning may be due to increases in
brain and/or body temperature. That excessive
yawning may be symptomatic of abnormal
thermoregulation is also supported by bouts of
excessive yawning in patients with
thennoregulatory disorders (e.g., multiple
sclerosis, epilepsy, or migraine headache) (7).
Likewise, drugs that increase brain temperature
frequently produce excessive yawning (e.g.,
SSRIs), while drugs that lead to hypothermia
inhibit yawning (e.g., opioids) (7).
In summary, patients with symptoms of
excessive yawning may experience debilitating
side effects and should not be belittled nor
should theft symptoms be trivialized. The
applications of this research range from basic
physiological understanding to using symptoms of
excessive yawning as a diagnostic tool for
identifying instances of thermoregulatory
dysfunction. This evidence has the potential to
provide important insight to sleep medicine and
may clear up misconceptions regarding excessive
yawning and sleep disorders. Further research
needs to investigate the relationship between
excessive yawning, body temperature, and the
ability to effectively deal with heat stress. To
this point, neither woman has been accurately
diagnosed or effectively treated for theft
condition; however, both have been notified of
the possible connection to temperature
regulation.
6. Gallup AC,
Gallup GG Jr Yawning as a brain cooling
mechanism: nasal breathing and forehead cooling
diminish the incidence of contagious yawning.
Evol Psychol 2007;5:92-101
8. Gilbert 55, van den Heuvel CJ, Ferguson
SA, Dawson D Thermoregulation as a sleep
signally system. Sleep Med Rev
2004;8:81-93.
9. Hanis BA, Andrews PJD, Murray GD Enhanced
upper respiratory tract airflow and head fanning
reduce brain temperature in brain-injured,
mechanically ventilated patients: a randomized,
crossover, factorial trial. Br J Anaesth
2007;98:93-99.
10. Zenker W, Kubik S Brain cooling in
humans--anatomical considerations. Anat Embryol
(Berl) 1996;193:1-13
11. Launay JC, Besnard Y, GuinetA, Bessard
G, RapheiC, Savourey G Effects of modafinil on
heat thermoregulatory responses in humans at
rest Can J Physiol Pharmacol
2002;80:796-803
Faculty of Pharmacy, University of
Helsinki, Finland
Letter to the editirs
Dear Editors,
The paper "Excessive yawning and
thermoregulation: two case histories of chronic,
debilitating bouts of yawning" by Gallup and
Gallup [1] deals with an interesting and
potentially important topic. Yet, there are
problems concerning it.
The patients never met the investigators,
only providing subjective reports. On the basis
of the two cases of pathological yawning that
may be etiologically unrelated, conclusions are
drawn concerning yawning in general.
The medical histories contain
contradictions, and no details are given
concerning blood tests and MRI investigations.
Both patients are reported to suffer from
excessive yawning in the absence of sleep
problems. Yet, both had received sleep-related
diagnoses (patient 1 received diagnoses of
narcolepsy and excessive daytime sleepiness-and
the same diagnoses were ruled out, and patient 2
was diagnosed with sleep apnoea).
A high fasting insulin level (patient 1)
does not confirm insulin resistance and could
result from insulinoma that causes
life-threatening hypoglycaemias and would
explain the symptoms (inability to walk, feeling
ill, and extreme discomfort) and diagnoses
(seizure, migraine, and excessive daytime
sleepiness) [2-4]. It is not revealed
which drug(s) worsened the problem. Metformin
worsens hypoglycaemias [5].
The alpha-1-antitrypsin deficiency of
patient 2 is important (often related to
emphysema/COPD) [6], but this goes
unnoticed, and the focus is solely on the
putative thermoregulatory role of her yawning.
No attention is paid to her obesity and its
consequences. It is not always possible to
exclude multiple sclerosis at an early
stage.
Both patients should be encouraged to seek
medical assistance. It is not sufficient that
they have been "notified of the possible
connection to temperature regulation".
The only measurements were performed by one
patient under uncontrolled conditions and using
uncontrolled methodology (no details given).
Oral temperatures do not necessarily reflect
core or brain temperature. What exactly is meant
by saying "at the beginning and after a number
of attacks" is not told, or how attacks were
chosen for measurement. Subjectivity may have
played a marked role, especially as the patient
"can anticipate" the episodes. How she
anticipates them is not reported. No conclusions
should be based on these sporadic
measurements.
A 0.4°C decrease of body temperature of
a 96.5-kg patient requires the loss of 137 kJ of
heat (specific heat capacity of the body 3.56 kJ
kg-1 K-1 [7]). During a 5-min bout, the
body would thus act as a 460-W heater capable of
heating 430 ml of water from 25°C to the
boiling point in 5 min (specific heat capacity
of water 4.19 kJ kg' K' [7, 8]). With 15
daily bouts, the extra loss of heat is over
2,000 kJ, and if not compensated for by
increased heat production, severe hypothermia
will result (6°C decrease daily). If
compensated (without extra eating), the
increased metabolism will lead to a loss of more
than 2 kg of body fat in a month. The obesity of
the patient is not in accord with this.
Compensation by drinking hot liquids (50°C)
would require a daily consumption of ca. 38l
.
There are few mechanisms by which the body
can lose heat so that its temperature
decreases:
1. Direct heat exchange with the environment
(conduction to air, cloths, etc.)
2. Evaporation of water (lungs/airways,
skin, and mucous membranes)
3. Thermal radiation
Yawning hardly directly affects thermal
radiation (that depends only on the temperature
and surface properties) or conduction of heat
from the skin to the environment. It may
increase air flow to the lungs, but even with
maximal conductive loss (thermal equilibrium
with the inhaled air), the amount lost is
minimal, since the specific heat capacity and
density of air are low [9]. Assuming
ambient air of 25°C, the 0.4°C
decrease requires inhalation of over 9,000 l of
air. Thus, this mechanism cannot account for the
temperature decreases.
Evaporation of water from the airways/lungs
causes a maximal heat loss when the inhaled air
is water-free. At 37°C, a loss of 137 kJ
requires the extra evaporation of 57 g of water
(heat of vaporisation 2,410 kJ
kg-1[10]). Since the vapour pressure of
water at 37°C is 47.1 mmHg [11,
12], the loss of 137 kJ requires inhalation
and saturation of 1,380 l of dry air. With air
that is already saturated with water at
25°C, 2,797 l must be inhaled. In the
dry-air case, assuming exhalation of the maximum
possible amount (3.6 l for a female) on every
expiration, 383 inspirations are needed. With 15
expirations per minute, this takes 25 min. In
the more realistic humid-air case, the process
takes 52 min. (We have, for simplicity,
neglected the fact that also normal breathing
removes water vapour, and thus the extra removal
of 137 kJ requires still far larger
volumes.)
Furthermore, breathing with the maximal
vital capacity for a long time causes severe
respiratory alkalosis, unconsciousness, and
death. So, this mechanism cannot explain the
results. Water vapour can be lost also through
sweating. This is the only explanation, if
yawning indeed markedly decreases body
temperature, and requires the extra evaporation
(in addition to normal perspiration) of 57 g of
sweat on each bout of yawning (850 ml with 15
bouts) and must lead to increased thirst and
water intake that were not reported.
Deceleration of the body's heat production
(decrease of metabolic rate) may indirectly
decrease body temperature. With a consumption of
food equivalent with 2,100 kcal per day, a
complete stop of metabolism (which would kill
the patient) would have to continue for 23 min
for each 0.4°C decrease of body
temperature, assuming normal perspiration
(impossible without metabolism!). If metabolism
decreases by 25%, ca. 1.5 h will be needed for
each bout of yawning. Even with a 3,000-kcal
diet, each deceleration (100% or 25%) of
metabolism would have to continue for 15 min or
1 h, respectively.
Thus, the reported decreases of body
temperature during yawning are physically
possible only if yawning effectively increases
perspiration. The thermoregulatory hypothesis is
interesting, and hypotheses are
needed&emdash;but they should be called
hypotheses or theories, not conclusions or
results, as long as convincing evidence is
missing.
References
1. Gallup GG, Gallup AC. Excessive yawning
and thermoregulation: two case histories of
chronic, debilitating bouts of yawning. Sleep
Breath. 2010;14:157-159
2. Graves TD, Gandhi S, Smith SJM, Sisodiya
SM, Conway GS Misdiagnosis of seizures:
insulinoma presenting as adultonset seizure
disorder. J Neurol Neurosurg Psychiatry
2004;75:1091&endash;1092.
3. Chin S, Popat V, Boyne MS, Cochran C,
Tulloch-Reid M Insulinoma induced hypoglycaemia
in a Jamaican patient. West Indian Med J.
2007;56:182&endash;186
4. Ebady S, Arami M, Kucheki E. A case of
insulinoma with neuropsychiatric symptoms and
cerebral infarction.
Internet J Neurol 2005;4(2).
5. Omari A, Yue DK, Twigg SM Exercise,
metformin and hypoglycaemia: a neglected entity.
Brit J Diabetes Vascular Dis
2005;5:106&endash;108.
6. Fregonese L, Stolk J Hereditary
alpha-1-antitrypsin deficiency and its clinical
consequences. Orphanet J Rare Dis
2008;3:16.
7. Koehler KR
8. Nordling C, Österman J (2004)
Physics handbook for science and engineering,
(10th printing, 2007), 7th edn.
Studentlitteratur, Lund, p 39
9. McQuillan FJ, Culham JR, Yovanovich MM
(1984) Properties of dry air at one atmosphere,
Report "UW/MHTL 8406, G-01", Microelectronics
Heat Transfer Lab, University of Waterloo,
Waterloo, Ontario, Canada.
10. Bray JJ, Cragg PA, Macknight ADC, Mills
RG (2003) Lecture notes on human physiology, 4th
edn. Blackwell Publishing, Oxford
11. Wagner W, Pruss A International
equations for the saturation properties of
ordinary water substance. Revised
according to the international temperature
scale of 1990. J Phys Chem Reference Data 1993;
22:783&endash;787
12. Oklahoma State University, Department of
Chemistry (2010) Vapor Pressure of Water
mise à jour
du
12 septembre
2010
Sleep
Med
2011;12(1):102
Yawning
cannot cause
significant
temperature
decreases in humans
Hannu Elo
University of
Helsinki, Faculty of
Pharmacy
To the Editor,
In their paper on yawning in multiple
sclerosis (MS), Gallup et al. [1]
advocate their theory [2-4], according
to which the physiological function of yawning
is cooling of the brain and/or body. Without a
trace of convincing evidence, the authors state
that yawning is ''involved in thermoregulation.
" A main piece of ''evidence" for the Gallup
theory is constituted by a few measurements
carried out (without controlled conditions or
methods) by one patient who ''anticipates" her
yawning attacks [2].
I have shown by calculations [5]
that the temperature decreases claimed to occur
during those attacks are physically impossible.
In fact, any significant decrease of body
temperature as a result of a few yawns is
physically impossible except if yawning causes
massive sweating. The same is true of any
significant cooling of the brain, taking into
account the following potential cooling
mechanisms: evaporation of water
(lungs/airways), conductive heat losses, thermal
radiation, and deceleration of metabolism.
Gallup et al. state that ''increases in
facial blood flow resulting from a yawn" remove
''hyperthermic blood from the face and head,
while introducing cooler blood from the lungs
and extremities. " There is no evidence for such
''hyperthermic blood" or such temperature
differences. A ''sense of gratification" caused
by yawning by no means constitutes evidence for
the claimed homeostatic function of
yawning.
Gallup et al. summarize: ''Growing evidence
suggests that yawning may be a useful diagnostic
tool for identifying thermoregulatory problems.
" However, there is no evidence (not to mention
growing evidence) for this claim. Unscientific
claims in a clinically oriented journal may have
potentially dangerous consequences.
The authors should pay attention to
scientific reasoning and distinguish hypotheses
from results, conclusions, and facts. If yawning
relieves MS symptoms, the mechanism might be
constituted by effects on the autonomic nervous
system and/or release of hormones.
References
[1] Gallup AC, Gallup Jr GG, Feo C.
Yawning, sleep, and symptom relief in patients
with multiple sclerosis. Sleep Med 2010;
11:329&endash;30.
[2] Gallup GG, Gallup AC. Excessive
yawning and thermoregulation: two case histories
of chronic, debilitating bouts of yawning. Sleep
Breath 2010; 14:157&endash;9.
[3] Gallup AC, Gallup Jr GG. Yawning
and thermoregulation. Physiol Behav 2008;
95:10&endash;6.
[4] Gallup AC, Gallup Jr GG. Yawning
as a brain cooling mechanism: nasal breathing
and forehead cooling diminish the incidence of
contagious yawning. Evol Psychol 2007;
5:92&endash;101.
[5] Elo H. Yawning and
thermoregulation. Sleep Breath
mise à jour
du
26 décembre
2010
Sleep
Med
2011;12(1):102-103
The
thermoregulatory hypothesis of yawning: Time to
reconsider terms such as "impossible" and
"cannot" and evaluate theories based on
evidence
Andrew C. Gallup
Response from the author:
Without significant evaluation of the
original paper describing yawning and symptom
relief in patients with multiple sclerosis, Elo
attempts to undermine growing convergent support
for the thermoregulatory hypothesis of yawning
by simply reiterating comments made from a
previous critique. In each case, Elo is
uninformed, unscientific, misleading, and
inaccurate when describing past research in this
area.
His main contention is that by his
'calculations", yawning "cannot" produce
significant changes in temperature, and that
such changes are "impossible" without "massive
sweating." However, his conclusions are
untenable since the "calculations" refer solely
to changes in overall body temperature, and not
to localized changes in specific areas relevant
to yawning (i.e., neck, face, and head). In
fact, Elo's position is completely contrary to
recent research where we directly investigated
the relationship between yawning and brain
temperature changes in rats.
Using implanted thermocoupled temperature
probes in the prelimbic cortex, continuous
measures of brain temperature were coupled with
video-recorded sessions to track yawns and other
behaviors. Results show yawning was preceded in
all instances by rapid increases in brain
temperature, accompanied by correspondingly
consistent decreases in brain temperature and a
return to baseline following each yawn.
Furthermore, analyses show that similar
decreases in brain temperature did not occur
outside yawning and stretching events.
Therefore, it is time to reconsider the use of
blanket terms such as "impossible" and 'cannot"
and begin evaluating theories based on
evidence.
As for the paper on yawning and symptom
relief in patients with multiple sclerosis, the
results remain entirely consistent with the view
that yawning may provide temporary mitigation of
symptoms through a cerebral cooling effect. An
appended table summarizes current evidence
supporting the thermoregulatory hypothesis of
yawning.
