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VIEWS AND REVIEWS • Arq. Neuro-Psiquiatr. 76 (7) • July 2018 • https://doi.org/10.1590/0004-282X20180057 copy
Yawning in neurology: a review
Bocejo em neurologia: uma revisão
Hélio A. G. Teive
Universidade Federal do Paraná, Hospital de Clínicas, Departamento de Medicina Interna, Unidade de Distúrbios do Movimento, Serviço de Neurologia, Curitiba PR, Brasil;
Renato P. Munhoz
University Health Network, Toronto Western Hospital, Gloria and Morton Shulman Movement Disorders, Toronto, ON, Canada;
Carlos Henrique F. Camargo
Universidade Estadual de Ponta Grossa, Hospital Universitário, Serviço de Neurologia, Ponta Grossa PR, Brasil;
Olivier Walusinski
General Practice, Brou, France.
Yawning is a stereotyped physiological behavior that can represent a sign or symptom of several conditions, such as stroke, parakinesia brachialis oscitans, parkinsonism, Parkinson's disease and epilepsy. More rarely, it can occur in patients with intracranial hypertension, brain tumor, multiple sclerosis, migraine, Chiari malformation type I, and amyotrophic lateral sclerosis. Drug-induced yawning is an uncommon clinical condition and yawning in patients with autism or schizophrenia is very rare. The aim of this review is to describe in detail the occurrence of the phenomenon in such conditions, and its' phenomenology and pathophysiology.
yawning; parakinesia, stroke
Bocejo é um comportamento estereotipado fisiológico, o qual, contudo, pode representar um sinal ou sintoma de várias condições neurológicas, tais como, acidente vascular encefálico, incluindo a parakinesia brachial oscitans, parkinsonismo, doença de Parkinson, e epilepsia. Mais raramente, o bocejo pode ocorrer em pacientes com hipertensão intra-craniana, tumor cerebral, esclerose múltipla, migrânea, malformação de Chiari tipo I, e esclerose lateral amiotrófica. Bocejo-induzido por drogas representa outra condição clínica pouco comum. De outro modo, bocejo é muito raro em pacientes com autismo e esquizofrenia. O objetivo desta revisão foi descrever em detalhes a ocorrência deste fenômeno em tais condições, sua fenomenologia e fisiopatologia.
bocejo; paracinesia; acidente vascular cerebral
Yawning is considered an intriguing and fascinating phenomenon with an obscure etiopathogenesis. It involves opening the mouth wide and closing the eyelids while inhaling deeply and then exhaling more briefly. A yawn typically lasts 5-10 seconds (Figure 1)11. Walusinski O. Yawning in diseases. Eur Neurol. 2009;62(3):180-7. https://doi.org/10.1159/000228262
https://doi.org/10.1159/000228262... ,22. Guggisberg AG, Mathis J, Schnider A, Hess CW. Why do we yawn? Neurosci Biobehav Rev. 2010 Jul;34(8):1267-76. https://doi.org/10.1016/j.neubiorev.2010.03.008
https://doi.org/10.1016/j.neubiorev.2010... ,33. Gallup AC. Why do we yawn? Primitive versus derived features. Neurosci Biobehav Rev. 2011 Jan;35(3):765-9. https://doi.org/10.1016/j.neubiorev.2010.09.009
https://doi.org/10.1016/j.neubiorev.2010... ,44. Guggisberg AG, Mathis J, Schnider A, Hess CW. Why do we yawn? The importance of evidence for specific yawn-induced effects. Neurosci Biobehav Rev. 2011 Apr;35(5):1302-4. https://doi.org/10.1016/j.neubiorev.2010.12.004
https://doi.org/10.1016/j.neubiorev.2010... ,55. Gallup AC, Gallup GG Jr. Yawning and thermoregulation. Physiol Behav. 2008 Sep;95(1-2):10-6. https://doi.org/10.1016/j.physbeh.2008.05.003
https://doi.org/10.1016/j.physbeh.2008.0... ,66. Gallup AC. A thermoregulatory behavior. Front Neurol Neurosci. 2010;28:84-9. https://doi.org/10.1159/000307084
https://doi.org/10.1159/000307084... ,77. Giganti F, Salzarulo P. Yawning throughout life. Front Neurol Neurosci. 2010;28:26-31. https://doi.org/10.1159/000307072
https://doi.org/10.1159/000307072... and is usually accompanied by retroflexion of the head and sometimes by elevation of the arms (known as pandiculation when occurring together). Human beings yawn with a frequency of up to 28 times a day11. Walusinski O. Yawning in diseases. Eur Neurol. 2009;62(3):180-7. https://doi.org/10.1159/000228262
https://doi.org/10.1159/000307072... , often after waking up and before falling asleep. Yawning is frequently contagious and is considered a sign of boredom or even disrespectful behavior in the presence of others88. Walusinski O. Historical perspectives. Front Neurol Neurosci. 2010;28:1-21. https://doi.org/10.1159/000307069
https://doi.org/10.1159/000307069... ,99. Schiller F. Yawning? J Hist Neurosci. 2002;11(4):392-401. https://doi.org/10.1076/jhin.11.4.392.8540
https://doi.org/10.1076/jhin.11.4.392.85... ,1010. Walusinski O. Popular knowledge and beliefs. Front Neurol Neurosci. 2010;28:22-5. https://doi.org/10.1159/000307071
https://doi.org/10.1159/000307071... . In the 19th century, Charcot considered yawning an important clinical neurological sign, but for many years neurologists attached little importance to it88. Walusinski O. Historical perspectives. Front Neurol Neurosci. 2010;28:1-21. https://doi.org/10.1159/000307069
https://doi.org/10.1159/000307069... ,1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... . Nowadays, however, although yawning continues to be a largely under-appreciated behavior, chasmology, the study of yawning, has become the focus of considerable interest1212. Walusinski O, Deputte BL. [The phylogeny, ethology and nosology of yawning]. Rev Neurol (Paris). 2004 Nov;160(11):1011-21. French. https://doi.org/10.1016/S0035-3787(04)71138-8
https://doi.org/10.1016/S0035-3787(04)71... . The aim of this article is to review yawning in neurology.
The Yawner. Pieter Bruegel. The Elder.
A literature search was performed in Pubmed, for English-language articles over the time period from 1992 to 2018, using the terms "yawning" and "CNS", "neurology", "neurologic disorders". The initial references were selected using the following main exclusion criteria: 1) duplicate articles; 2) articles unrelated to the purpose of the study; 3) articles unrelated to yawning; 4) articles not including sufficient relevant data.
HISTORICAL ASPECTS OF YAWNING
Phylogenetically, yawning is a very old behavior that can be detected in most vertebrates from the fetal stages to old age33. Gallup AC. Why do we yawn? Primitive versus derived features. Neurosci Biobehav Rev. 2011 Jan;35(3):765-9. https://doi.org/10.1016/j.neubiorev.2010.09.009
https://doi.org/10.1016/j.physbeh.2008.0... ,88. Walusinski O. Historical perspectives. Front Neurol Neurosci. 2010;28:1-21. https://doi.org/10.1159/000307069
https://doi.org/10.1159/000307069... . Its meaning has been the subject of speculation since antiquity. In some cultures, it has been associated with Satan (Arab countries) and spirits (India), while Hippocrates associated it with apoplexy88. Walusinski O. Historical perspectives. Front Neurol Neurosci. 2010;28:1-21. https://doi.org/10.1159/000307069
https://doi.org/10.1159/000307069... . In the Hindu world, yawning in public is a religious offense. Since the 17th century, various explanations for its meaning have been put forward88. Walusinski O. Historical perspectives. Front Neurol Neurosci. 2010;28:1-21. https://doi.org/10.1159/000307069
https://doi.org/10.1159/000307069... . Boerhaave, the founder of clinical medicine, stated in 1680, that yawns promote "the equitable distribution of spiritus in all muscles and unblock the vessels". In the 18th century, yawning was believed to be associated with the "improvement of brain oxygenation"88. Walusinski O. Historical perspectives. Front Neurol Neurosci. 2010;28:1-21. https://doi.org/10.1159/000307069
https://doi.org/10.1159/000307069... and, in the 19th century, it was associated with different etiologies, including hysteria, and considered a reflex. Curiously, in 1888, in his famous Leçons du Mardi à la Salpêtrière, Charcot discussed the case of a 17-year-old patient who yawned eight times a minute, or 480 times an hour, and only stopped when she went to sleep. Her condition was believed at the time to be associated with hysteria and oxygenation of the nervous centers88. Walusinski O. Historical perspectives. Front Neurol Neurosci. 2010;28:1-21. https://doi.org/10.1159/000307069
https://doi.org/10.1159/000307098... . She had generalized epileptic seizures, complete anosmia and binasal hemianopsia. She had been amenorrheic for a year. Charcot's young patient was most likely suffering from a prolactinoma compression of her optic chiasma and her hypothalamus88. Walusinski O. Historical perspectives. Front Neurol Neurosci. 2010;28:1-21. https://doi.org/10.1159/000307069
https://doi.org/10.1159/000307098... .
During the 20th century, substantial progress was made in understanding yawning, and several studies on this behavior and neurophysiology, hormones, dopamine receptors and social behavior were carried out11. Walusinski O. Yawning in diseases. Eur Neurol. 2009;62(3):180-7. https://doi.org/10.1159/000228262
https://doi.org/10.1159/000307072... ,88. Walusinski O. Historical perspectives. Front Neurol Neurosci. 2010;28:1-21. https://doi.org/10.1159/000307069
https://doi.org/10.1159/000307069... ,11. Walusinski O. Yawning in diseases. Eur Neurol. 2009;62(3):180-7. https://doi.org/10.1159/000228262
https://doi.org/10.1159/000228262... 22. Guggisberg AG, Mathis J, Schnider A, Hess CW. Why do we yawn? Neurosci Biobehav Rev. 2010 Jul;34(8):1267-76. https://doi.org/10.1016/j.neubiorev.2010.03.008
https://doi.org/10.1016/j.neubiorev.2010... ,1313. Collins GT, Eguibar JR. Neurophamacology of yawning. Front Neurol Neurosci. 2010;28:90-106. https://doi.org/10.1159/000307085
https://doi.org/10.1159/000307085... . Despite this progress, yawning remains a mysterious and fascinating physiological, or even pathological, phenomenon.
THE NEUROPHYSIOLOGY OF YAWNING – A SUMMARY
There are several hypotheses to explain yawning: physiological hypotheses (such as the respiratory and circulatory system, arousal, sleepiness, thermoregulatory, ear-pressure and state-change hypotheses) and the social/communication hypothesis44. Guggisberg AG, Mathis J, Schnider A, Hess CW. Why do we yawn? The importance of evidence for specific yawn-induced effects. Neurosci Biobehav Rev. 2011 Apr;35(5):1302-4. https://doi.org/10.1016/j.neubiorev.2010.12.004
https://doi.org/10.1016/j.physbeh.2008.0... . In a study published in 2011, Guggisberg et al.44. Guggisberg AG, Mathis J, Schnider A, Hess CW. Why do we yawn? The importance of evidence for specific yawn-induced effects. Neurosci Biobehav Rev. 2011 Apr;35(5):1302-4. https://doi.org/10.1016/j.neubiorev.2010.12.004
https://doi.org/10.1016/j.neubiorev.2010... concluded that the hypothesis best supported by experimental evidence is the social/communication hypothesis. In contrast, Gallup33. Gallup AC. Why do we yawn? Primitive versus derived features. Neurosci Biobehav Rev. 2011 Jan;35(3):765-9. https://doi.org/10.1016/j.neubiorev.2010.09.009
https://doi.org/10.1016/j.neubiorev.2010... argued, in 2011, that the social/communication hypothesis is unattractive and suggested that yawning is probably multifunctional across species. In their view, the most acceptable hypothesis in humans is the thermoregulatory one, according to which yawning is a brain-cooling mechanism. In 2014, Walusinski1414. Walusinski O. How yawning switches the default-mode network to the attentional network by activating the cerebrospinal fluid flow. Clin Anat. 2014 Mar;27(2):201-9. https://doi.org/10.1002/ca.22280
https://doi.org/10.1002/ca.22280... proposed a new hypothesis, according to which yawning switches the default-mode network to the attentional network by activating cerebrospinal fluid flow. The default-mode network is a set of interconnected brain areas identified in functional neuroimaging (fMRI) that exhibit spontaneous physiological activity during the normal resting state. There is a high level of activity in the default-mode network when the mind is not involved in specific behavioral tasks, and a low level of activity during focused attention1414. Walusinski O. How yawning switches the default-mode network to the attentional network by activating the cerebrospinal fluid flow. Clin Anat. 2014 Mar;27(2):201-9. https://doi.org/10.1002/ca.22280
https://doi.org/10.1002/ca.22280... . According to Walusinski's hypothesis, yawning is a homeostatic process that appears when the default-mode network is active and sleepiness increases; yawning then disengages the default-mode network to promote the attentional network, which accelerates the circulation of cerebrospinal fluid, increasing clearance of somnogens such as adenosine, prostaglandin D2, VIP, prolactin and anandamide, and reducing sleepiness1414. Walusinski O. How yawning switches the default-mode network to the attentional network by activating the cerebrospinal fluid flow. Clin Anat. 2014 Mar;27(2):201-9. https://doi.org/10.1002/ca.22280
https://doi.org/10.1002/ca.22280... . The anatomic structures involved in yawning have yet to be elucidated and, more recently, fMRI has demonstrated that different levels of the neuroaxis, including the brainstem, prefrontal cortex and subcortical regions, may be involved1515. Nahab FB, Hattori N, Saad ZS, Hallett M. Contagious yawning and the frontal lobe: an fMRI study. Hum Brain Mapp. 2009 May;30(5):1744-51. https://doi.org/10.1002/hbm.20638
https://doi.org/10.1002/hbm.20638... ,1616. Nahab FB. Exploring yawning with neuroimaging. Front Neurol Neurosci. 2010;28:128-33. https://doi.org/10.1159/000307093
https://doi.org/10.1159/000307093... . In 2010, Collins and Eguibar1313. Collins GT, Eguibar JR. Neurophamacology of yawning. Front Neurol Neurosci. 2010;28:90-106. https://doi.org/10.1159/000307085
https://doi.org/10.1159/000307085... hypothesized that there are three main neural pathways involved in the regulation of yawning (Figure 2). Two of these are formed by groups of oxytocinergic neurons projecting from the paraventricular nucleus (one of the hypothalamic nuclei) to the hippocampus, pons, medulla and spinal cord; the other is formed by ACTH (adrenocorticotrophic hormone) and melanocyte-stimulating hormone-activated neurons projecting from the paraventricular nucleus to the hippocampus via activation of cholinergic neurons. There is also direct activation of hippocampal cholinergic neurons and a serotonergic-cholinergic pathway1313. Collins GT, Eguibar JR. Neurophamacology of yawning. Front Neurol Neurosci. 2010;28:90-106. https://doi.org/10.1159/000307085
https://doi.org/10.1159/000307085... . In summary, several neurotransmitters and neuropeptides, such as dopamine, acetylcholine, serotonin, glutamate, GABA, adrenergics, excitatory amino acids, nitric acid, ACTH-related peptides, α-melanocyte-stimulating hormones and oxytocin, seem to be involved biochemically in the mechanism of yawning1313. Collins GT, Eguibar JR. Neurophamacology of yawning. Front Neurol Neurosci. 2010;28:90-106. https://doi.org/10.1159/000307085
https://doi.org/10.1159/000307085... . Dopamine activates oxytocin production in the paraventricular nucleus of the hypothalamus, and oxytocin in turn activates cholinergic transmission in the hippocampus and the reticular formation of the brainstem, resulting in acetylcholine induction of yawning via muscle muscarinic receptors.1313. Collins GT, Eguibar JR. Neurophamacology of yawning. Front Neurol Neurosci. 2010;28:90-106. https://doi.org/10.1159/000307085
https://doi.org/10.1159/000307085... In general, dopamine and its agonists trigger yawning, while opioid peptides and GABA reduce its frequency1313. Collins GT, Eguibar JR. Neurophamacology of yawning. Front Neurol Neurosci. 2010;28:90-106. https://doi.org/10.1159/000307085
https://doi.org/10.1159/000307085... . Yawning is used as an indicator of dopaminergic and oxytocinergic transmission and, in Parkinson's disease it is an expression of therapeutic dopaminergic activity, particularly as a marker of D3 dopamine receptor activity1313. Collins GT, Eguibar JR. Neurophamacology of yawning. Front Neurol Neurosci. 2010;28:90-106. https://doi.org/10.1159/000307085
https://doi.org/10.1159/000307085... ,1717. Goren JL, Friedman JH. Yawning as an aura for an L-dopa-induced "on" in Parkinson's disease. Neurology. 1998 Mar;50(3):823. https://doi.org/10.1212/WNL.50.3.823
https://doi.org/10.1212/WNL.50.3.823... .
Yawning – Neurotransmitters.
YAWNING – A CONTAGIOUS BEHAVIOR
It is a popular belief that yawning is contagious1010. Walusinski O. Popular knowledge and beliefs. Front Neurol Neurosci. 2010;28:22-5. https://doi.org/10.1159/000307071
https://doi.org/10.1159/000307071... , and it is well known that watching another person yawn may induce the person watching to yawn too1010. Walusinski O. Popular knowledge and beliefs. Front Neurol Neurosci. 2010;28:22-5. https://doi.org/10.1159/000307071
https://doi.org/10.1159/000307071... ,1818. Perriol MP, Monaca C. "One person yawning sets off everyone else". J Neurol Neurosurg Psychiatry. 2006 Jan;77(1):3. https://doi.org/10.1136/jnnp.2005.078337
https://doi.org/10.1136/jnnp.2005.078337... . According to Guggisberg et al.22. Guggisberg AG, Mathis J, Schnider A, Hess CW. Why do we yawn? Neurosci Biobehav Rev. 2010 Jul;34(8):1267-76. https://doi.org/10.1016/j.neubiorev.2010.03.008
https://doi.org/10.1016/j.neubiorev.2010... , who support the social/communication hypothesis, contagious yawning is due to activation of a complex network of brain areas associated with imitation, empathy and social behavior22. Guggisberg AG, Mathis J, Schnider A, Hess CW. Why do we yawn? Neurosci Biobehav Rev. 2010 Jul;34(8):1267-76. https://doi.org/10.1016/j.neubiorev.2010.03.008
https://doi.org/10.1016/j.neubiorev.2010... . In 2005, Schürman et al.1919. Schürmann M, Hesse MD, Stephan KE, Saarela M, Zilles K, Hari R et al. Yearning to yawn: the neural basis of contagious yawning. Neuroimage. 2005 Feb;24(4):1260-4. studied this intriguing phenomenon using fMRI. They observed activation of the left periamygdalar region, suggesting a connection between yawn contagiousness and amygdala activation. In contrast, Platek et al.2020. Platek SM, Mohamed FB, Gallup GG Jr. Contagious yawning and the brain. Brain Res Cogn Brain Res. 2005 May;23(2-3):448-52. https://doi.org/10.1016/j.cogbrainres.2004.11.011
https://doi.org/10.1016/j.cogbrainres.20... , using fMRI in 2005 to study contagious yawning, showed activation of the posterior cingulate and precuneus and, in 2009, Nahab et al.1515. Nahab FB, Hattori N, Saad ZS, Hallett M. Contagious yawning and the frontal lobe: an fMRI study. Hum Brain Mapp. 2009 May;30(5):1744-51. https://doi.org/10.1002/hbm.20638
https://doi.org/10.1002/hbm.20638... , also using fMRI, demonstrated activation in the ventromedial prefrontal cortex, suggesting that mirror neuron networks play a role in yawning. Since the latter study, various papers on the relationship between contagious behavior, such as yawning and itching/scratching, and the activation of mirror neurons and the neurological mechanism of social behavior have been published1919. Schürmann M, Hesse MD, Stephan KE, Saarela M, Zilles K, Hari R et al. Yearning to yawn: the neural basis of contagious yawning. Neuroimage. 2005 Feb;24(4):1260-4.,2020. Platek SM, Mohamed FB, Gallup GG Jr. Contagious yawning and the brain. Brain Res Cogn Brain Res. 2005 May;23(2-3):448-52. https://doi.org/10.1016/j.cogbrainres.2004.11.011
https://doi.org/10.1016/j.cogbrainres.20... ,2121. Gupta S, Mittal S. Yawning and its physiological significance. Int J Appl Basic Med Res. 2013 Jan;3(1):11-5. https://doi.org/10.4103/2229-516X.112230
https://doi.org/10.4103/2229-516X.112230... . In 2014, Provine2222. Provine RR. Contagious behavior: an alternative approach to mirror-like phenomena. Behav Brain Sci. 2014 Apr;37(2):216-7. https://doi.org/10.1017/S0140525X13002458
https://doi.org/10.1017/S0140525X1300245... stated that contagious behaviors such as yawning have mirror-like properties.
PHYSIOLOGICAL YAWNING
Physiological yawning can occur during the transition between wakefulness and sleep or vice versa, or in response to fatigue, tiredness, stress, overwork, lack of stimulation, hunger or satiety11. Walusinski O. Yawning in diseases. Eur Neurol. 2009;62(3):180-7. https://doi.org/10.1159/000228262
https://doi.org/10.1016/j.neubiorev.2010... . In general, it is associated with sleep deprivation during the night and drowsiness during the day and often occurs when people are bored22. Guggisberg AG, Mathis J, Schnider A, Hess CW. Why do we yawn? Neurosci Biobehav Rev. 2010 Jul;34(8):1267-76. https://doi.org/10.1016/j.neubiorev.2010.03.008
https://doi.org/10.1016/j.neubiorev.2010... ,1010. Walusinski O. Popular knowledge and beliefs. Front Neurol Neurosci. 2010;28:22-5. https://doi.org/10.1159/000307071
https://doi.org/10.1159/000307098... ,2121. Gupta S, Mittal S. Yawning and its physiological significance. Int J Appl Basic Med Res. 2013 Jan;3(1):11-5. https://doi.org/10.4103/2229-516X.112230
https://doi.org/10.4103/2229-516X.112230... .
YAWNING IN NEUROLOGICAL CLINICAL PRACTICE
Yawning may occur not only because of boredom, drowsiness, or by contagion but also in association with various diseases. Yawning is termed pathological, abnormal, or excessive if it is spontaneous, more frequent than generally perceived as normal, compulsive, and not triggered by appropriate stimuli including fatigue or boredom. No consensus definition exists concerning the frequency of yawns. A recent recommendation adopted the abnormal yawning frequency as three yawns per 15 minutes to decrease the likelihood that two subsequent, accidental yawns were counted as one episode with abnormal yawning2323. Krestel H, Weisstanner C, Hess CW, Bassetti CL, Nirkko A, Wiest R. Insular and caudate lesions release abnormal yawning in stroke patients. Brain Struct Funct. 2015 Mar;220(2):803-12. https://doi.org/10.1007/s00429-013-0684-6
https://doi.org/10.1007/s00429-013-0684-... .
Yawning can be present in the clinical picture of several neurological diseases, including stroke, multiple sclerosis, neuromyelitis optica spectrum disorders, parkinsonism, Parkinson's disease, migraine, vasovagal syncope, brain tumor, intracranial hypertension, Chiari malformation type I and epilepsy, and can be induced by drugs11. Walusinski O. Yawning in diseases. Eur Neurol. 2009;62(3):180-7. https://doi.org/10.1159/000228262
Yawning in sleep disorders
In general, excessive yawning occurs more frequently in patients with sleep disorders (e.g., insomnia and sleep obstructive apnea) and is most common in children and young adults1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
Excessive yawning in clinical conditions
Other clinical conditions associated with yawning are functional digestive disorders (e.g., dyspepsia and irritable bowel syndrome), motion sickness and hypoglycemia in diabetic patients under insulin therapy1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... . In addition, vasovagal syncopal or presyncopal episodes frequently present with yawning as well as malaise, dizziness, visual obscuration, nausea, pallor and loss of consciousness1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... . Excessive yawning has also been reported in patients with depression and can be caused by the many medications used in neurology, psychiatry and internal medicine1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... . This issue is discussed in the following section.
Drug-induced yawning
Drug-induced yawning represents a rare and frequently not very serious adverse side-effect1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... ,2424. Patatanian E, Williams NT. Drug-induced yawning—a review. Ann Pharmacother. 2011 Oct;45(10):1297-301. https://doi.org/10.1345/aph.1Q255
https://doi.org/10.1345/aph.1Q255... . Antidepressants, dopaminergic agents, opioids and benzodiazepines are the main pharmacologic classes associated with yawning1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1345/aph.1Q255... . The most widely-used antidepressants are serotonergic agents (selective serotonin reuptake inhibitors), including fluoxetine, paroxetine, escitalopram, venlafaxine and duloxetine1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1345/aph.1Q255... . Dopaminergic drugs include levodopa, dopaminergic agonists (pramipexole, ropinirole, rotigotine and apomorphine) and monoamine oxidase inhibitors1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1345/aph.1Q255... . Blin et al.2525. Blin O, Masson G, Azulay JP, Fondarai J, Serratrice G. Apomorphine-induced blinking and yawning in healthy volunteers. Br J Clin Pharmacol. 1990 Nov;30(5):769-73. https://doi.org/10.1111/j.1365-2125.1990.tb03848.x
https://doi.org/10.1111/j.1365-2125.1990... evaluated eight healthy volunteers, in 1990, after they used apomorphine and after a placebo, allowing 48 hours for the medication to be washed out. They found that this dopamine agonist induced blinking and yawning in all their participants. Another interesting finding is the occurrence of yawning in the withdrawal syndrome after prolonged use of opioids or coffee1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1345/aph.1Q255... . In 2007, Sommet et al.2626. Sommet A, Desplas M, Lapeyre-Mestre M, Montastruc JL; French Network of Pharmacovigilance Centers. Drug-induced yawning: a review of the French pharmacovigilance database. Drug Saf. 2007;30(4):327-31. https://doi.org/10.2165/00002018-200730040-00005
https://doi.org/10.2165/00002018-2007300... studied drug-induced yawning reported in the French Pharmacovigilance Database between 1985 and 2004. They found 28 reports involving 38 drugs, especially serotonergic agents, dopaminergic agents, opioids, and benzodiazepines2626. Sommet A, Desplas M, Lapeyre-Mestre M, Montastruc JL; French Network of Pharmacovigilance Centers. Drug-induced yawning: a review of the French pharmacovigilance database. Drug Saf. 2007;30(4):327-31. https://doi.org/10.2165/00002018-200730040-00005
https://doi.org/10.2165/00002018-2007300... .
Yawning and stroke
Yawning has been observed secondary to acute hemorrhagic or ischemic anterior or posterior circulation stroke2727. Renau-Lagranja J, Vilar-Ventura RM, Peinazo-Arias M. Simón-Gozalbo A, Claramonte B, Geffner-Sclarsky D. Yawning as a clinical sign of ischemic stroke. Rev Neurol. 2010;51:639-40.,2828. Gallup AC. Abnormal yawning in stroke patients: the role of brain thermoregulation. Front Neurosci. 2014 Sep;8:300. https://doi.org/10.3389/fnins.2014.00300
https://doi.org/10.3389/fnins.2014.00300... ,2929. Cattaneo L, Cucurachi L, Chierici E, Pavesi G. Pathological yawning as a presenting symptom of brain stem ischaemia in two patients. J Neurol Neurosurg Psychiatry. 2006 Jan;77(1):98-100. https://doi.org/10.1136/jnnp.2005.075267
https://doi.org/10.1136/jnnp.2005.075267... ,3030. Krasnianski M, Gaul C, Neudecker S, Behrmann C, Schlüter A, Winterholler M. Yawning despite trismus in a patient with locked-in syndrome caused by a thrombosed megadolichobasilar artery. Clin Neurol Neurosurg. 2003 Dec;106(1):44-6. https://doi.org/10.1016/S0303-8467(03)00045-3
https://doi.org/10.1016/S0303-8467(03)00... . In general, it indicates damage to the brainstem reticular formation and cortical and subcortical structures2727. Renau-Lagranja J, Vilar-Ventura RM, Peinazo-Arias M. Simón-Gozalbo A, Claramonte B, Geffner-Sclarsky D. Yawning as a clinical sign of ischemic stroke. Rev Neurol. 2010;51:639-40.,2929. Cattaneo L, Cucurachi L, Chierici E, Pavesi G. Pathological yawning as a presenting symptom of brain stem ischaemia in two patients. J Neurol Neurosurg Psychiatry. 2006 Jan;77(1):98-100. https://doi.org/10.1136/jnnp.2005.075267
https://doi.org/10.1136/jnnp.2005.075267... . In 2006, Cattaneo et al.2929. Cattaneo L, Cucurachi L, Chierici E, Pavesi G. Pathological yawning as a presenting symptom of brain stem ischaemia in two patients. J Neurol Neurosurg Psychiatry. 2006 Jan;77(1):98-100. https://doi.org/10.1136/jnnp.2005.075267
https://doi.org/10.1136/jnnp.2005.075267... published a case report of two patients with pathological yawning as a presenting symptom of brainstem ischemia involving the upper pons and the pontomesencephalic junction. Yawning has been described in patients with locked-in syndrome due to vertebrobasilar stroke caused by a thrombosed megadolichobasilar artery3030. Krasnianski M, Gaul C, Neudecker S, Behrmann C, Schlüter A, Winterholler M. Yawning despite trismus in a patient with locked-in syndrome caused by a thrombosed megadolichobasilar artery. Clin Neurol Neurosurg. 2003 Dec;106(1):44-6. https://doi.org/10.1016/S0303-8467(03)00045-3
https://doi.org/10.1016/S0303-8467(03)00... . Another potential cause of yawning in patients with stroke is intracranial hypertension or even herniation2727. Renau-Lagranja J, Vilar-Ventura RM, Peinazo-Arias M. Simón-Gozalbo A, Claramonte B, Geffner-Sclarsky D. Yawning as a clinical sign of ischemic stroke. Rev Neurol. 2010;51:639-40.. More recently, Krestel et al.2323. Krestel H, Weisstanner C, Hess CW, Bassetti CL, Nirkko A, Wiest R. Insular and caudate lesions release abnormal yawning in stroke patients. Brain Struct Funct. 2015 Mar;220(2):803-12. https://doi.org/10.1007/s00429-013-0684-6
https://doi.org/10.1007/s00429-013-0684-... studied 10 patients with acute anterior circulation stroke and yawning using neuroimaging (brain MRI with diffusion-weighted images). They found a correlation between ischemic lesions in the insula and caudate nucleus and a period of abnormal yawning and suggested that the insula may be the main region of the brain responsible for serotonin-mediated yawning2323. Krestel H, Weisstanner C, Hess CW, Bassetti CL, Nirkko A, Wiest R. Insular and caudate lesions release abnormal yawning in stroke patients. Brain Struct Funct. 2015 Mar;220(2):803-12. https://doi.org/10.1007/s00429-013-0684-6
https://doi.org/10.1007/s00429-013-0684-... . A rare and very interesting clinical condition involving yawning known as parakinesia brachialis oscitans is related to stroke and will be described below.
Parakinesia brachialis oscitans
Occasionally, in patients with acute hemiplegia, the onset of yawning is associated with an involuntary raising of the paralyzed arm3131. Walusinski O, Quoirin E, Neau JP. [Parakinesia brachialis oscitans]. Rev Neurol (Paris). 2005 Feb;161(2):193-200. French. https://doi.org/10.1016/S0035-3787(05)85022-2
https://doi.org/10.1016/S0035-3787(05)85... ,3232. Walusinski O, Neau JP, Bogousslavsky J. Hand up! Yawn and raise your arm. Int J Stroke. 2010 Feb;5(1):21-7. https://doi.org/10.1111/j.1747-4949.2009.00394.x
https://doi.org/10.1111/j.1747-4949.2009... . This phenomenon was named parakinesia brachialis oscitans in 2005 by Walusinski et al.3131. Walusinski O, Quoirin E, Neau JP. [Parakinesia brachialis oscitans]. Rev Neurol (Paris). 2005 Feb;161(2):193-200. French. https://doi.org/10.1016/S0035-3787(05)85022-2
https://doi.org/10.1016/S0035-3787(05)85... , who studied four cases and compared them with other cases published in the literature over the previous 150 years. Parakinesia brachialis oscitans was probably first described by Erasmus Darwin, the grandfather of Charles Darwin, in 1794, in his book "Zoonomia of the laws of organic life" 3131. Walusinski O, Quoirin E, Neau JP. [Parakinesia brachialis oscitans]. Rev Neurol (Paris). 2005 Feb;161(2):193-200. French. https://doi.org/10.1016/S0035-3787(05)85022-2
https://doi.org/10.1016/S0035-3787(05)85... . In their seminal paper, Walusinski et al. proposed a possible mechanism for this abnormal involuntary movement. They suggested that resection of the cortico-neocerebellar tract of the extrapyramidal system disinhibits the spino-archeocerebellar tract, enabling motor stimulation of the arm by the lateral reticular nucleus, which has a link with respiratory and locomotor rhythms.3131. Walusinski O, Quoirin E, Neau JP. [Parakinesia brachialis oscitans]. Rev Neurol (Paris). 2005 Feb;161(2):193-200. French. https://doi.org/10.1016/S0035-3787(05)85022-2
https://doi.org/10.1016/S0035-3787(05)85... Several case reports have since been published describing this phenomenon, including others by Walusinski et al. and a few other reports3232. Walusinski O, Neau JP, Bogousslavsky J. Hand up! Yawn and raise your arm. Int J Stroke. 2010 Feb;5(1):21-7. https://doi.org/10.1111/j.1747-4949.2009.00394.x
https://doi.org/10.1111/j.1747-4949.2009... ,3333. de Lima PM, Munhoz RP, Becker N, Teive HA. Parakinesia brachialis oscitans: report of three cases. Parkinsonism Relat Disord. 2012 Feb;18(2):204-6. https://doi.org/10.1016/j.parkreldis.2011.09.020
https://doi.org/10.1016/j.parkreldis.201... ,3434. Jung NY, Ahn BY, Park KH, Chung CS, Na DL, Kim EJ. A case of parakinesia brachialis oscitans. Clin Neurol Neurosurg. 2012 Feb;114(2):156-8. https://doi.org/10.1016/j.clineuro.2011.08.020
https://doi.org/10.1016/j.clineuro.2011.... ,3535. Meenakshisundaram R, Thirumalaikolundusubramanian P, Walusinski O, Muthusundari A, Sweni S. Associated movements in hemiplegic limbs during yawning. Front Neurol Neurosci. 2010;28:134-9. https://doi.org/10.1159/000307095
https://doi.org/10.1159/000307095... ,3636. Kang P, Dhand A. Teaching Video NeuroImages: movement of a paralyzed arm with yawning. Neurology. 2015 Apr;84(16):e118. https://doi.org/10.1212/WNL.0000000000001489
https://doi.org/10.1212/WNL.000000000000... ,3737. Farah M, Barcellos I, Boschetti G, Munhoz RP. Parakinesia Brachialis Oscitans: A Case Report. Mov Disord Clin Pract (Hoboken). 2015;2(4):436-7. https://doi.org/10.1002/mdc3.12234
https://doi.org/10.1002/mdc3.12234... . In 2013, Zorzetto et al.3838. Zorzetto FP, Braatz VL, Walusinski O, Teive HA. Parakinesia brachialis oscitans during thrombolytic therapy. BMJ Case Rep. 2013 Feb;2013(Feb):18. also published a case report of parakinesia brachialis oscitans in the setting of thrombolytic therapy (Figure 3). In 2015, Kang and Dhand3636. Kang P, Dhand A. Teaching Video NeuroImages: movement of a paralyzed arm with yawning. Neurology. 2015 Apr;84(16):e118. https://doi.org/10.1212/WNL.0000000000001489
https://doi.org/10.1212/WNL.000000000000... published a case report of a 63-year-old man who presented with an acute ischemic infarct in the left middle cerebral artery distribution, aphasia and paralysis of the right arm, which consistently rose to his chest when he yawned. After yawning, paralysis always resumed. In a recent publication, Alves et al.3939. Alves PN, Carvalho M, Reimão S, Castro J, Fonseca AC, Canhão P. Voluntary control of a plegic limb during yawning. J Neurol. 2018 Feb;265(2):433-5. https://doi.org/10.1007/s00415-017-8729-z
https://doi.org/10.1007/s00415-017-8729-... describe a patient who has voluntary control over that movement.
Parakinesia brachialis oscitans in a patient with right hemiplegia due to ischemic stroke.
Yawning, parkinsonism and Parkinson's disease
In general, yawning is used as an indicator of activity of the dopamine-oxytocin pathway1313. Collins GT, Eguibar JR. Neurophamacology of yawning. Front Neurol Neurosci. 2010;28:90-106. https://doi.org/10.1159/000307085
https://doi.org/10.1159/000307085... . In patients with Parkinson's disease (PD), it is associated with the presence of dopaminergic activity1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... ,1313. Collins GT, Eguibar JR. Neurophamacology of yawning. Front Neurol Neurosci. 2010;28:90-106. https://doi.org/10.1159/000307085
https://doi.org/10.1159/000307085... and has been considered an aura for an L-dopa-induced "on" state1717. Goren JL, Friedman JH. Yawning as an aura for an L-dopa-induced "on" in Parkinson's disease. Neurology. 1998 Mar;50(3):823. https://doi.org/10.1212/WNL.50.3.823
https://doi.org/10.1212/WNL.50.3.823... . It is very well known that PD patients who receive apomorphine injections (a direct D1/D2 dopamine receptor agonist) frequently present with yawning before positive motor effects, sometimes in association with penile erections4040. Chen JJ, Obering C. A review of intermittent subcutaneous apomorphine injections for the rescue management of motor fluctuations associated with advanced Parkinson's disease. Clin Ther. 2005 Nov;27(11):1710-24. https://doi.org/10.1016/j.clinthera.2005.11.016
https://doi.org/10.1016/j.clinthera.2005... . Yawning was described by von Economo in patients with acute encephalitis lethargica or postencephalitic parkinsonism88. Walusinski O. Historical perspectives. Front Neurol Neurosci. 2010;28:1-21. https://doi.org/10.1159/000307069
https://doi.org/10.1159/000307069... . Curiously, Sandyk et al.4141. Sandyk R. Excessive yawning and progressive supranuclear palsy. Int J Neurosci. 1987 May;34(1-2):123-4. https://doi.org/10.3109/00207458708985946
https://doi.org/10.3109/0020745870898594... reported a series of five patients with progressive supranuclear palsy (Richardson's syndrome) who presented with balance deficits, falls, oculomotor abnormalities and bursts of repeated yawning without any correlation with their dopaminergic treatment. In 2013, Giganti et al.4242. Giganti F, Guidi S, Ramat S, Zilli I, Raglione LM, Sorbi S et al. Yawning: a behavioural marker of sleepiness in de novo PD patients. Parkinsonism Relat Disord. 2013 Jul;19(7):703-4. https://doi.org/10.1016/j.parkreldis.2013.03.007
https://doi.org/10.1016/j.parkreldis.201... studied 18 untreated early-PD patients and compared them with 18 age-matched healthy controls. They showed that the circadian distribution of yawning was not altered in untreated patients with early-stage PD and concluded that yawning is a behavioral marker of sleepiness in de novo PD patients4242. Giganti F, Guidi S, Ramat S, Zilli I, Raglione LM, Sorbi S et al. Yawning: a behavioural marker of sleepiness in de novo PD patients. Parkinsonism Relat Disord. 2013 Jul;19(7):703-4. https://doi.org/10.1016/j.parkreldis.2013.03.007
https://doi.org/10.1016/j.parkreldis.201... .
Yawning and epilepsy
Yawning can occur in different epileptic syndromes1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... ,4343. Medrano V, Selles-Galiana MF, Fernández-Izquierdo S, Mallada-Frechin J, Díaz-González F, Piqueras-Rodríguez L. [Yawning and temporal lobe epilepsy]. Rev Neurol. 2005 Jul;41(1):63-4. Spanish.,4444. Yankovsky AE, Andermann F, Dubeau F. Video case report post-ictal forceful yawning in a patient with nondominant hemisphere epilepsy. Med Hypotheses. 2006;67:6-14.,4545. Kuba R, Musilová K, Brázdil M, Rektor I. Peri-ictal yawning lateralizes the seizure onset zone to the nondominant hemisphere in patients with temporal lobe epilepsy. Epilepsy Behav. 2010 Nov;19(3):311-4. https://doi.org/10.1016/j.yebeh.2010.07.004
https://doi.org/10.1016/j.yebeh.2010.07.... ,4646. Specchio N, Carotenuto A, Trivisano M, Cappelletti S, Vigevano F, Fusco L. Ictal yawning in a patient with drug-resistant focal epilepsy: video/EEG documentation and review of literature reports. Epilepsy Behav. 2011 Nov;22(3):602-5. https://doi.org/10.1016/j.yebeh.2011.08.013
https://doi.org/10.1016/j.yebeh.2011.08.... ,4747. Wasade VS, Balki I, Bowyer SM, Gaddam S, Mohammadi-Nejad AR, Nazem-Zadeh MR et al. Controllable yawning expressed as focal seizures of frontal lobe epilepsy. Epilepsy Behav Case Rep. 2016 Aug;6:61-3. https://doi.org/10.1016/j.ebcr.2016.08.005
https://doi.org/10.1016/j.ebcr.2016.08.0... ,4848. Nicotra A, Khalil NM, Owbridge P, Hakda M, Beitverda Y. Pathological yawning as an ictal seizure manifestation in the elderly. BMJ Case Reports 2012 Oct;2012. https://doi.org/10.1136/bcr-01-2012-5618
https://doi.org/10.1136/bcr-01-2012-5618... . It has been described in the peri-ictal period in children with infantile spasms and in patients with temporal lobe epilepsy (peri-ictal yawning preceding complex partial seizures or yawning in the post-ictal period)4343. Medrano V, Selles-Galiana MF, Fernández-Izquierdo S, Mallada-Frechin J, Díaz-González F, Piqueras-Rodríguez L. [Yawning and temporal lobe epilepsy]. Rev Neurol. 2005 Jul;41(1):63-4. Spanish.,4444. Yankovsky AE, Andermann F, Dubeau F. Video case report post-ictal forceful yawning in a patient with nondominant hemisphere epilepsy. Med Hypotheses. 2006;67:6-14.,4545. Kuba R, Musilová K, Brázdil M, Rektor I. Peri-ictal yawning lateralizes the seizure onset zone to the nondominant hemisphere in patients with temporal lobe epilepsy. Epilepsy Behav. 2010 Nov;19(3):311-4. https://doi.org/10.1016/j.yebeh.2010.07.004
https://doi.org/10.1016/j.ebcr.2016.08.0... ,44. Guggisberg AG, Mathis J, Schnider A, Hess CW. Why do we yawn? The importance of evidence for specific yawn-induced effects. Neurosci Biobehav Rev. 2011 Apr;35(5):1302-4. https://doi.org/10.1016/j.neubiorev.2010.12.004
https://doi.org/10.1016/j.neubiorev.2010... 88. Walusinski O. Historical perspectives. Front Neurol Neurosci. 2010;28:1-21. https://doi.org/10.1159/000307069
https://doi.org/10.1159/000307069... . In 2011, Specchio et al.4646. Specchio N, Carotenuto A, Trivisano M, Cappelletti S, Vigevano F, Fusco L. Ictal yawning in a patient with drug-resistant focal epilepsy: video/EEG documentation and review of literature reports. Epilepsy Behav. 2011 Nov;22(3):602-5. https://doi.org/10.1016/j.yebeh.2011.08.013
https://doi.org/10.1016/j.yebeh.2011.08.... reported ictal yawning in an adult patient with drug-resistant focal epilepsy. Kuba et al.4545. Kuba R, Musilová K, Brázdil M, Rektor I. Peri-ictal yawning lateralizes the seizure onset zone to the nondominant hemisphere in patients with temporal lobe epilepsy. Epilepsy Behav. 2010 Nov;19(3):311-4. https://doi.org/10.1016/j.yebeh.2010.07.004
https://doi.org/10.1016/j.yebeh.2010.07.... investigated the incidence and lateralizing value of peri-ictal yawning in patients with temporal lobe epilepsy who had undergone surgery for epilepsy. They observed peri-ictal yawning in 4.1% of 97 patients and, in 1.8% of these patients' 380 seizures, yawning occurred in the post-ictal period4545. Kuba R, Musilová K, Brázdil M, Rektor I. Peri-ictal yawning lateralizes the seizure onset zone to the nondominant hemisphere in patients with temporal lobe epilepsy. Epilepsy Behav. 2010 Nov;19(3):311-4. https://doi.org/10.1016/j.yebeh.2010.07.004
https://doi.org/10.1016/j.yebeh.2010.07.... . They also observed that peri-ictal yawning occurred only in patients with right-sided, nondominant temporal lobe epilepsy, suggesting that it may have a lateralizing value.4545. Kuba R, Musilová K, Brázdil M, Rektor I. Peri-ictal yawning lateralizes the seizure onset zone to the nondominant hemisphere in patients with temporal lobe epilepsy. Epilepsy Behav. 2010 Nov;19(3):311-4. https://doi.org/10.1016/j.yebeh.2010.07.004
https://doi.org/10.1016/j.yebeh.2010.07.... Wasade et al.4747. Wasade VS, Balki I, Bowyer SM, Gaddam S, Mohammadi-Nejad AR, Nazem-Zadeh MR et al. Controllable yawning expressed as focal seizures of frontal lobe epilepsy. Epilepsy Behav Case Rep. 2016 Aug;6:61-3. https://doi.org/10.1016/j.ebcr.2016.08.005
https://doi.org/10.1016/j.ebcr.2016.08.0... published an interesting case report, in 2016, of a young male who presented with controllable yawning expressed as focal seizures of frontal lobe epilepsy. In 2012, Nicotra et al.4848. Nicotra A, Khalil NM, Owbridge P, Hakda M, Beitverda Y. Pathological yawning as an ictal seizure manifestation in the elderly. BMJ Case Reports 2012 Oct;2012. https://doi.org/10.1136/bcr-01-2012-5618
https://doi.org/10.1136/bcr-01-2012-5618... discussed the case of an elderly patient who presented with pathological yawning as an ictal seizure manifestation.
Yawning and intracranial hypertension
Some patients with intracranial hypertension, brain swelling or herniation due to stroke, head trauma or brain tumors may present with yawning together with headache and seizures1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... . In 2014, Saura et al.4949. Saura H, Beppu T, Matsuura H, Asahi S, Uesugi N, Sasaki M et al. Intractable yawning associated with mature teratoma of the supramedial cerebellum. J Neurosurg. 2014 Aug;121(2):387-9. https://doi.org/10.3171/2014.4.JNS132243
https://doi.org/10.3171/2014.4.JNS132243... described intractable yawning associated with mature teratoma of the supramedial cerebellum. Yawning may also occur as a presenting symptom of Chiari malformation type 15050. Zebian B, Hogg FR, Fu RZ, Sivakumaran R, Stapleton S. Yawning as a presenting symptom of Chiari malformation Type I: report of 2 cases. J Neurosurg Pediatr. 2015 Jun;15(6):612-4. https://doi.org/10.3171/2014.11.PEDS14139
https://doi.org/10.3171/2014.11.PEDS1413... .
Migraine and yawning
Migraine represents a very common neurological problem, and the pathophysiology of migraine attacks has been shown to be related to dopaminergic transmission5151. Peroutka SJ. Dopamine and migraine. Neurology. 1997 Sep;49(3):650-6. https://doi.org/10.1212/WNL.49.3.650
https://doi.org/10.1212/WNL.49.3.650... ,5252. Akerman S, Goadsby PJ. Dopamine and migraine: biology and clinical implications. Cephalalgia. 2007 Nov;27(11):1308-14. https://doi.org/10.1111/j.1468-2982.2007.01478.x
https://doi.org/10.1111/j.1468-2982.2007... . In the premonitory phase, yawning can be present in association with malaise, somnolence and mood changes among other manifestations5151. Peroutka SJ. Dopamine and migraine. Neurology. 1997 Sep;49(3):650-6. https://doi.org/10.1212/WNL.49.3.650
https://doi.org/10.1111/j.1468-2982.2007... . Some migraineurs may experience excessive yawning during the visual aura before the attack5151. Peroutka SJ. Dopamine and migraine. Neurology. 1997 Sep;49(3):650-6. https://doi.org/10.1212/WNL.49.3.650
https://doi.org/10.1111/j.1468-2982.2007... . However, excessive yawning in migraine can be improved with dopamine receptor antagonists, which are effective therapeutic agents for this condition5151. Peroutka SJ. Dopamine and migraine. Neurology. 1997 Sep;49(3):650-6. https://doi.org/10.1212/WNL.49.3.650
https://doi.org/10.1111/j.1468-2982.2007... .
Yawning, multiple sclerosis and neuromyelitis optica spectrum disorders
Some patients with multiple sclerosis (MS) present with thermoregulatory dysfunction5353. Postert T, Pöhlau D, Meves S, Nastos I, Przuntek H. Pathological yawning as a symptom of multiple sclerosis. J Neurol. 1996 Mar;243(3):300-1. https://doi.org/10.1007/BF00868532
https://doi.org/10.1007/BF00868532... . Therefore, sleep problems and yawning could be symptoms of MS1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... ,5353. Postert T, Pöhlau D, Meves S, Nastos I, Przuntek H. Pathological yawning as a symptom of multiple sclerosis. J Neurol. 1996 Mar;243(3):300-1. https://doi.org/10.1007/BF00868532
https://doi.org/10.1007/BF00868532... . Gallup et al.5454. Gallup AC, Gallup GG Jr, Feo C. Yawning, sleep, and symptom relief in patients with multiple sclerosis. Sleep Med. 2010 Mar;11(3):329-30. https://doi.org/10.1016/j.sleep.2009.12.007
https://doi.org/10.1016/j.sleep.2009.12.... also showed that yawning can provide symptom relief in MS patients. In 1996, Postert et al.5353. Postert T, Pöhlau D, Meves S, Nastos I, Przuntek H. Pathological yawning as a symptom of multiple sclerosis. J Neurol. 1996 Mar;243(3):300-1. https://doi.org/10.1007/BF00868532
https://doi.org/10.1007/BF00868532... published a case report on pathological yawning as a symptom of MS and, in 2014, Lana-Peixoto et al.5555. Lana-Peixoto MA, Callegaro D, Talim N, Talim LE, Pereira SA, Campos GB. Pathologic yawning in neuromyelitis optica spectrum disorders. Mult Scler Relat Disord. 2014 Jul;3(4):527-32. https://doi.org/10.1016/j.msard.2014.04.002
https://doi.org/10.1016/j.msard.2014.04.... described nine patients with neuromyelitis optica spectrum disorders and excessive yawning unrelated to sleep deprivation or fatigue. They concluded that yawning may be a neglected symptom in neuromyelitis optica spectrum disorder5555. Lana-Peixoto MA, Callegaro D, Talim N, Talim LE, Pereira SA, Campos GB. Pathologic yawning in neuromyelitis optica spectrum disorders. Mult Scler Relat Disord. 2014 Jul;3(4):527-32. https://doi.org/10.1016/j.msard.2014.04.002
https://doi.org/10.1016/j.msard.2014.04.... .
Yawning and amyotrophic lateral sclerosis
Yawning can be observed in patients with amyotrophic lateral sclerosis (ALS)1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... . Williams5656. Williams DR. The yawning reflex: an upper motor neuron sign in amyotrophic lateral sclerosis. Neurology. 2000 Nov;55(10):1592-3. https://doi.org/10.1212/WNL.55.10.1592
https://doi.org/10.1212/WNL.55.10.1592... published a case report, in 2000, of a 64-year-old woman who presented with progressive, very frequent yawning characterized by bouts of 20 to 30 successive yawns in association with painful cramping and a sensation of choking. During the follow-up, the patient developed bulbar palsy, and an electromyogram confirmed the diagnosis of amyotrophic lateral sclerosis5656. Williams DR. The yawning reflex: an upper motor neuron sign in amyotrophic lateral sclerosis. Neurology. 2000 Nov;55(10):1592-3. https://doi.org/10.1212/WNL.55.10.1592
https://doi.org/10.1212/WNL.55.10.1592... . In 2007, Wicks5757. Wicks P. Excessive yawning is common in the bulbar-onset form of ALS. Acta Psychiatr Scand. 2007 Jul;116(1):76. https://doi.org/10.1111/j.1600-0447.2007.01025.x
https://doi.org/10.1111/j.1600-0447.2007... published a paper in which he noted that excessive yawning is a common sign in the bulbar-onset form of amyotrophic lateral sclerosis.
Yawning, autism and schizophrenia
Contagious yawning can be explained by the relationship between yawning and social empathy22. Guggisberg AG, Mathis J, Schnider A, Hess CW. Why do we yawn? Neurosci Biobehav Rev. 2010 Jul;34(8):1267-76. https://doi.org/10.1016/j.neubiorev.2010.03.008
https://doi.org/10.1016/j.physbeh.2008.0... ,1212. Walusinski O, Deputte BL. [The phylogeny, ethology and nosology of yawning]. Rev Neurol (Paris). 2004 Nov;160(11):1011-21. French. https://doi.org/10.1016/S0035-3787(04)71138-8
https://doi.org/10.1016/S0035-3787(04)71... ,2121. Gupta S, Mittal S. Yawning and its physiological significance. Int J Appl Basic Med Res. 2013 Jan;3(1):11-5. https://doi.org/10.4103/2229-516X.112230
https://doi.org/10.4103/2229-516X.112230... ,2222. Provine RR. Contagious behavior: an alternative approach to mirror-like phenomena. Behav Brain Sci. 2014 Apr;37(2):216-7. https://doi.org/10.1017/S0140525X13002458
https://doi.org/10.1017/S0140525X1300245... . Interestingly, in some psychiatric disorders, such as autism and schizophrenia, yawning is very rare1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... ,5858. Senju A, Maeda M, Kikuchi Y, Hasegawa T, Tojo Y, Osanai H. Absence of contagious yawning in children with autism spectrum disorder. Biol Lett. 2007 Dec;3(6):706-8. https://doi.org/10.1098/rsbl.2007.0337
https://doi.org/10.1098/rsbl.2007.0337... ,5959. Hacker H, Rössler W. Empathy in schizophrenia: impaired resonance. Eur Arch Psychiatry Clin Neurosci. 2009;259(6):353-61. https://doi.org/10.1007/s00406-009-0007-3
https://doi.org/10.1007/s00406-009-0007-... . In 2007, Senju et al.5858. Senju A, Maeda M, Kikuchi Y, Hasegawa T, Tojo Y, Osanai H. Absence of contagious yawning in children with autism spectrum disorder. Biol Lett. 2007 Dec;3(6):706-8. https://doi.org/10.1098/rsbl.2007.0337
https://doi.org/10.1098/rsbl.2007.0337... evaluated 24 children with autism spectrum disorder and 25 age-matched, normally-developing children, in terms of their frequency of yawning, using video clips of either yawning or control mouth movements. They concluded that contagious yawning is impaired in autism spectrum disorder, supporting the idea that contagious yawning is based on the capacity for empathy5858. Senju A, Maeda M, Kikuchi Y, Hasegawa T, Tojo Y, Osanai H. Absence of contagious yawning in children with autism spectrum disorder. Biol Lett. 2007 Dec;3(6):706-8. https://doi.org/10.1098/rsbl.2007.0337
https://doi.org/10.1098/rsbl.2007.0337... . Haker and Rössler5959. Hacker H, Rössler W. Empathy in schizophrenia: impaired resonance. Eur Arch Psychiatry Clin Neurosci. 2009;259(6):353-61. https://doi.org/10.1007/s00406-009-0007-3
https://doi.org/10.1007/s00406-009-0007-... , in 2009, compared changes in yawning patterns in a group of 43 schizophrenic patients and an age- and sex-matched group of healthy controls using a video with sequences of yawning, laughter and neutral faces. They observed that schizophrenic patients showed a significantly lower rate of yawning, suggesting that susceptibility to contagious yawning is reduced in patients with impaired social empathy5959. Hacker H, Rössler W. Empathy in schizophrenia: impaired resonance. Eur Arch Psychiatry Clin Neurosci. 2009;259(6):353-61. https://doi.org/10.1007/s00406-009-0007-3
Yawning – problems and solutions
Yawning can sometimes cause complications, such as mandibular subluxation, painful cramps in the geniohyoid muscle and fracture of the styloid apophysis1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... . More rarely, it can trigger an attack of glossopharyngeal neuralgia, idiopathic carotidynia or even Marin Amat syndrome, a form of acquired facial synkinesis manifesting as involuntary eyelid closure on jaw opening that often occurs following the aberrant regeneration of the facial nerve after a peripheral facial palsy1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... ,6060. Malhotra A. Marin-Amat syndrome: a case of acquired facial synkinesis. BMJ Case Rep. 2013 Jul;2013 jul18 1:bcr2013010030. https://doi.org/10.1136/bcr-2013-010030
https://doi.org/10.1136/bcr-2013-010030... . In contrast, yawning can improve Eustachian tube dysfunction and dysbaric facial paralysis and even acts as a therapy for vocal fatigue1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.1159/000307098... . Gallup and Gallup55. Gallup AC, Gallup GG Jr. Yawning and thermoregulation. Physiol Behav. 2008 Sep;95(1-2):10-6. https://doi.org/10.1016/j.physbeh.2008.05.003
https://doi.org/10.1016/j.physbeh.2008.0... studied the frequency of yawning as an initial signal of fever relief.
Yawning is a stereotyped physiological behavior that can be a sign or symptom of several neurological conditions, such as stroke (including stroke with parakinesia brachialis oscitans), parkinsonism and epilepsy. More rarely, yawning can occur in patients with intracranial hypertension, multiple sclerosis, migraine and amyotrophic lateral sclerosis and can be induced by drugs. It is rare in patients with autism spectrum disorders or schizophrenia1111. Walusinski O. Associated diseases. Front Neurol Neurosci. 2010;28:140-55. https://doi.org/10.1159/000307098
https://doi.org/10.4103/2229-516X.112230... ,2424. Patatanian E, Williams NT. Drug-induced yawning—a review. Ann Pharmacother. 2011 Oct;45(10):1297-301. https://doi.org/10.1345/aph.1Q255
https://doi.org/10.1345/aph.1Q255... ,2727. Renau-Lagranja J, Vilar-Ventura RM, Peinazo-Arias M. Simón-Gozalbo A, Claramonte B, Geffner-Sclarsky D. Yawning as a clinical sign of ischemic stroke. Rev Neurol. 2010;51:639-40.,3131. Walusinski O, Quoirin E, Neau JP. [Parakinesia brachialis oscitans]. Rev Neurol (Paris). 2005 Feb;161(2):193-200. French. https://doi.org/10.1016/S0035-3787(05)85022-2
https://doi.org/10.1016/S0035-3787(05)85... ,4242. Giganti F, Guidi S, Ramat S, Zilli I, Raglione LM, Sorbi S et al. Yawning: a behavioural marker of sleepiness in de novo PD patients. Parkinsonism Relat Disord. 2013 Jul;19(7):703-4. https://doi.org/10.1016/j.parkreldis.2013.03.007
https://doi.org/10.1016/j.parkreldis.201... ,5353. Postert T, Pöhlau D, Meves S, Nastos I, Przuntek H. Pathological yawning as a symptom of multiple sclerosis. J Neurol. 1996 Mar;243(3):300-1. https://doi.org/10.1007/BF00868532
https://doi.org/10.1007/BF00868532... ,5858. Senju A, Maeda M, Kikuchi Y, Hasegawa T, Tojo Y, Osanai H. Absence of contagious yawning in children with autism spectrum disorder. Biol Lett. 2007 Dec;3(6):706-8. https://doi.org/10.1098/rsbl.2007.0337
https://doi.org/10.1007/s00406-009-0007-... ,6161. Krestel H, Bassetti CL, Walusinski O. Yawning-Its anatomy, chemistry, role, and pathological considerations. Prog Neurobiol. 2018 Feb;161:61-78. https://doi.org/10.1016/j.pneurobio.2017.11.003
https://doi.org/10.1016/j.pneurobio.2017... .
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Senju A, Maeda M, Kikuchi Y, Hasegawa T, Tojo Y, Osanai H. Absence of contagious yawning in children with autism spectrum disorder. Biol Lett. 2007 Dec;3(6):706-8. https://doi.org/10.1098/rsbl.2007.0337
» https://doi.org/10.1098/rsbl.2007.0337
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Krestel H, Bassetti CL, Walusinski O. Yawning-Its anatomy, chemistry, role, and pathological considerations. Prog Neurobiol. 2018 Feb;161:61-78. https://doi.org/10.1016/j.pneurobio.2017.11.003
» https://doi.org/10.1016/j.pneurobio.2017.11.003
Correspondence: Hélio Afonso Ghizoni Teive; Rua General Carneiro 1103/102, Centro; 80060-150 Curitiba PR, Brasil. E-mail: hagteive@mps.com.br
Conflict of interest: There is no conflict of interest to declare.
Figure 1 The Yawner. Pieter Bruegel. The Elder.
(Reproduced from Google Images: www.pinterest.com, July, 26th, 2016).
Figure 2 Yawning – Neurotransmitters.
(Extracted, with permission, from Collins and Eguibar13).
Figure 3 Parakinesia brachialis oscitans in a patient with right hemiplegia due to ischemic stroke.
(Extracted, with permission, from Zorzetto et al.3838. Zorzetto FP, Braatz VL, Walusinski O, Teive HA. Parakinesia brachialis oscitans during thrombolytic therapy. BMJ Case Rep. 2013 Feb;2013(Feb):18.).
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The main goal of the Chef de Parti is to prepare food products according to the F&B standard recipes and to minimise waste to ensure food costs are in line with budget. The Chef de Parti enjoys working in a 5 star hotel environment, meeting special requests from guests, and being part of making exceptional culinary creations for the specific functions in the hotel.
NH Hotel Group is an international hotel chain with approximately 400 hotels over 30 countries in Europe, Africa and North- and South America. Part of the NH Hotel Group are the 4-star urban NH Hotels, the flagship NH Collection hotels and the nhow design hotels. The headquarters of the NH Hotel Group is located in Madrid.
NH Amsterdam Schiphol Airport has 419 rooms and is centrally located in the Netherlands. Working in this 4* Airport hotel means that you are part of an international work environment. At NH Amsterdam Schiphol Airport there is continuous anticipation of the busyness and different situations at Schiphol Airport. The hotel receives guests and crew members from all over the world. Furthermore, the hotel offers various facilities such as: a gym, a wellness center, an atmospheric bar / restaurant and a shuttle bus from the hotel to the airport.
Unique in the hospitality industry: a year-end bonus for every employee with a minimum of 50% of your monthly salary.
NH University: excellent training & (international) development opportunities.
Invite your friends and family for city trips in all of our NH Hotels worldwide ánd 30% discount on our restaurants and bars.
Excellent career opportunities: all employees of NH Hotel Group are given priority on internal vacancies worldwide.
We care for your health and therefore offer discounts on collective health insurance and financial services, a "bike plan" and discount at various gyms.


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Integrity Talking Points
Integrity Talking Points seeks to encourage conversations about trustworthiness and the spirit of service expected of everyone who works in New Zealand government agencies. " Integrity is a state of mind, it is not a set of rules." Beith Atkinson
Fraud fighter found fiddling
The British Serious Fraud Office has been found out making an unauthorised payoff to a former chief executive.
The National Audit Office has criticised the SFO for a £422,000 package paid to the chief executive when she "unexpectedly resigned". Her salary was £120,000 together with £27,000 for "benefits in kind" to cover commuting costs and accommodation costs. The irregular payment authorised by the then SFO Director, five days before leaving office, did not have the necessary approval of the Cabinet Office.
The incoming SFO Director asked the Treasury Solicitors Office to conduct an inquiry into the unjustified expenditure. The National Audit Office has now qualified the SFO accounts because due process was not followed in making these redundancy payment arrangements.
The BBC reports that the chairman of the Commons Public Accounts Committee was "astonished" that the SFO had agreed to the severance payment.
"The SFO showed a total disregard for taxpayers' money when they wrote out a five-figure cheque … (and) ignored Cabinet Office rules …"
www.nao.org.uk/publications/press_notice_home/1213/sfo_2011-12.aspx
www.bbc.co.uk/news/uk-20169306
Beith Atkinson, Serious Fraud Office (UK), unauthorised payments
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