Eur Arch Otorhinolaryngol DOI 10.1007/s00405-014-3302-1
Importance of yawning in the evaluation of excessive daytime sleepiness: a prospective clinical study Tolgahan Catli • Mustafa Acar • Deniz Hanci Osman Kursat Arikan • Cemal Cingi
Received: 12 June 2014 / Accepted: 19 September 2014 Ó Springer-Verlag Berlin Heidelberg 2014
Abstract As a dark and not fully understood side of human nature, yawning is believed to be a signs of various physiological or pathological behaviors of human. In this study, we aimed to investigate the importance of yawning in the evaluation of sleepiness. One hundred and twentynine snorers who were suspected to have obstructive sleep apnea syndrome underwent polysomnography and were asked to fill the Epworth sleepiness scale. The number of yawnings of patients was counted during the day following polysomnography. Patients were stratified into two groups: those have apnea hypopnea index \5 (n = 43, group 1) and those have apnea hypopnea index [30 (n = 86, group 2). Mean duration of sleep phases, oxygen saturations, sleep efficacies, yawning frequencies and Epworth scores of the groups were compared. Correlations of yawning
frequency with Epworth scores, duration of sleep phases and mean oxygen saturations were investigated. Sleep efficacies were similar between the groups (p [ 0.05). Yawning frequencies in group 1 and group 2 were 43.48 and 75.76 (mean rank), respectively (p \ 0.01). Mean N1, N2, N3 phase durations and oxygen saturations were significantly lower in group 2 (p \ 0.01). While there was a negative correlation between yawning frequency and duration of the non-REM phases and mean oxygen saturation (r = -0.53 and r = -0.31, respectively, p \ 0.05), yawning frequency was positively correlated with Epworth scores (r = 0.46, p \ 0.05). In addition to the shortened phases of sleep, increased Epworth score and decreased oxygen saturation, increased yawning frequency may indicate sleep deprivation.
Study was conducted at Yunus Emre State Hospital ENT Department, Eskisehir, Turkey.
T. Catli (&) Department of Otorhinolaryngology, Bozyaka Teaching and Research Hospital, Karabag˘lar, 35170 Izmir, Turkey e-mail: [email protected]
M. Acar Department of Otorhinolaryngology, Yunus Emre State Hospital, Eskisehir, Turkey D. Hanci Department of Otorhinolaryngology, Liv Hospital, Istanbul, Turkey O. K. Arikan Department of Otorhinolaryngology, Numune Teaching and Research Hospital, Adana, Turkey C. Cingi Department of Otorhinolaryngology, Medical Faculty, Eskisehir Osmangazi University, Eskisehir, Turkey
Obstructive sleep apnea (OSA) syndrome is characterized by deprivation of sleep quality due to the repetitive collapse of the pharyngeal airway and numerous arousals to resume ventilation . Although sleep-related events such as apnea, hypopnea, arousal, reduced oxygen saturation and altered sympathetic system activity are the basic aspects of this syndrome, various consequences of these sleep events such as excessive daytime sleepiness (EDS), social problems, increased likelihood of traffic and occupational accidents, increased cardiovascular events and stroke incidence may occur in the short or long term [2–4]. Among these symptoms, signs and complications, EDS seems to be associated with some of the unfavorable results
Eur Arch Otorhinolaryngol
of OSA, such as increased risk of motor vehicle accidents, work-related accidents, cognitive and psychosocial problems. With the increased awareness of clinicians and people about the importance and possible complications of OSA syndrome, numerous studies have been published regarding different aspects of this disease [5, 6]. A variety of objective and subjective test batteries have been developed for the accurate evaluation of OSA-related EDS. The most commonly used objective and subjective tests are multiple sleep latency test (MSLT), maintenance of wakefulness test (MWT), OSLER (Oxford SLEep Resistance) test and Epworth sleepiness scale (ESS). Since objective methods are complex, expensive and time consuming, ESS is the most frequently used simple, inexpensive, self-administered questionnaire that evaluates and rates EDS in sleep disorders . Yawning is an easily observable and quantifiable physiological phenomenon, which is believed to be associated with a feeling of comfort . Although this familiar act is a routine part of humans’ daily life, it is no more than 40 years that yawning has been a matter of investigation with advances in neuropharmacology. Yawning is a sophisticated ritual that comprises inspiration phase at the beginning, an acme period characterized with the extensive contraction of the mimic muscles together with a momentary interruption of breathing and a final expiration phase, which involves the relaxation of all participating muscles. Various physiological and pathological associations have been proposed with yawning in recent years . While various topics such as ‘‘arousal, brain cooling, social empathy, ear pressure and brain hypoxia’’ have been associated with its physiological aspect, numerous pathological conditions such as ‘‘migraine, depression, Parkinson’s disease, renal insufficiency, gastro-esophageal reflux’’ have also been associated with the occurrence of altered quantity and quality of yawning . Although there is a common belief regarding the association between yawning and sleepiness among people from different cultures, there are few studies which investigate this association in the medical literature. At this point, we aimed to investigate the importance of yawning in the evaluation of EDS.
Materials and methods One hundred and twenty-nine adult snorers who were suspected to have OSA syndrome were recruited to participate in this prospective, non-randomized, controlled study. Ethical committee of the institution approved the study protocol, and all participants provided informed consent. Specified inclusion criteria were as follows: (1)
age [18 years, (2) a willingness to fill ESS and undergo full-night polysomnography (PSG) in hospital, (3) a willingness to count their yawning frequencies during the day following PSG. Patients with a sleep duration of less than 4 h on PSG, patients with mild or moderate OSA (AHI [ 5 and \30), patients taking hypnotic medication and patients who were not capable of counting their yawning frequencies were excluded from the study. Full-night PSG recordings (EmblaÒ N7000 PSG recording systems-USA) have been performed at the same sleep laboratory by the same team. Patients were stratified into two groups: those with apnea hypopnea index (AHI) \5 as simple snorers (n = 43, group 1) and those with AHI [ 30 as severe OSA (n = 86, group 2). Other data recorded during the PSG study were ‘‘duration of sleep phases (N1, N2, N3, REM %), sleep efficacies (%), mean oxygen saturation (SaO2) and yawning frequencies (YF)’’. These data were evaluated and compared between the groups. Additionally, correlations between ‘‘YF and ESS score’’, ‘‘YF and mean SaO2’’ and ‘‘YF and duration of sleep phases’’ were investigated. Sleep study (full-night PSG) and phases of sleep EmblaÒ N7000 PSG recording system (USA) was used for the assessment of sleep. PSG recordings included electroencephalogram (EEG), electrooculogram (EOG), along with submental and bilateral anterior tibialis electromyogram (EMG) (recorded by surface electrodes). Other recordings were ‘‘airflow (by thermistors), arterial oxygen saturation (SaO2) (by a pulse oximetry), abdominal and thoracic respiratory movements (by a thoraco-abdominal inductance plethysmography), electrocardiogram (ECG), body position, and snoring’’. Analysis and classification of the sleep phases were performed according to American Academy of Sleep Medicine Task Force criteria . EEG waves were analyzed considering their frequencies, amplitudes and synchronization patterns. Three different phases of non-REM sleep ‘‘N1, N2, N3’’ and REM stages of sleep were calculated as percentage (%) of the whole sleep time. Epworth sleepiness scale Turkish version of ESS has been used in the evaluation of sleepiness . Patients were asked to score themselves on a self-rating scale that evaluated their likelihood of falling asleep in eight different daily circumstances over the previous month before they underwent the sleep study. Scale had four different chance of dozing (0 = no chance of dozing, 1 = slight chance of dozing, 2 = moderate chance of dozing, 3 = high chance of dozing) on eight different situations (Table 1-ESS). The ESS score is the sum of the
Eur Arch Otorhinolaryngol Table 1 The Epworth Sleepiness Scale Situation
Chance of dozing (enter number below)
investigated with Spearman’s rho correlation analysis. p \ 0.05 was considered statistically significant.
Watching TV Sitting, inactive in a public place (e.g., a theater or a meeting) As a passenger in a car for an hour without a break Lying down to rest in the afternoon when circumstances permit Sitting and talking to someone Sitting quietly after lunch without alcohol In a car, when stopped for a few minutes in the traffic Total How likely are you to doze off or fall asleep in the following situations, in contrast to feeling just tired? This refers to your usual way of life in recent times. Even if you have not done some of these things recently, try to work out how they would have affected you. Use the following scale to choose the most appropriate number for each situation Scale: 0 = would never doze, 1 = slight chance of dozing, 2 = moderate chance of dozing, 3 = high chance of dozing
eight item scores and ranges from minimum ‘‘0’’ to maximum ‘‘24’’. Higher ESS scores indicated greater daytime sleepiness.
One hundred and twenty-nine adult patients (81 men and 48 women) who met the inclusion criteria were the subjects of this analysis. Mean (± SD) ages of the groups were 46.07 ± 12.76 and 51.55 ± 10.26 years for group 1 and 2, respectively (p \ 0.05). Demographic findings of the groups are summarized in Table 2. Sleep efficacies were similar between the groups (p [ 0.05). Yawning frequencies were 43.48 and 75.76 (mean rank) in group 1 and group 2, respectively (p \ 0.01). Mean frequency of yawning was 4 to 5 times/day and 10 to 11 times/day for groups 1 and 2, respectively. Mean SaO2 was 93.81 ± 1.84 and 91.52 ± 2.6 in group 1 and group 2, respectively (p \ 0.01). In group 1, mean durations of N1,N2 and N3 were significantly longer, while mean ESS scores were significantly lower than group 2 (p \ 0.05). Comparisons of PSG variables (AHI, sleep efficacy, duration of the ‘‘N1, N2, N3 and REM’’ phases of sleep, mean oxygen saturation) are summarized in Table 3. Correlation analysis of the variables revealed a significant positive correlation between YF and ESS scores (r = 0.46, p \ 0.01); however, negative correlations were observed between YF and Table 2 Demographic findings in simple snorers (group 1) and heavy OSA patients (group 2) Group 1 (n:43)
Group 2 (n:86)
Counting of yawning Patients were asked to count their yawning frequencies during the day after the full-night sleep study, They were also told not to nap during the daytime and to go to sleep between 10:00 pm and 11:00 pm. Thus, standardization of the time period between waking up from sleep study (approximately 07:00 am) and falling in sleep (approximately between 10.00 pm and 11.00 pm) has been achieved among the groups. Statistical analysis Statistical analysis of the data was conducted with SPSS. 21.0 version . Homogeneity of the data was evaluated with the Kolmogorov–Smirnov test. The groups were compared by using Student’s t test (for normally distributed data), while yawning frequencies were compared with Mann–Whitney U test (for non-normally distributed data). Parametric values were presented as mean ± SD, while non-parametric values were presented as mean Rank. Categorical variables were compared using Chi square test. The correlations between the independent variables were
Mean age** Gender
BMI (kg/m2)** * p [ 0.05, ** p \ 0.05 a
Mean ± SD (standard deviation)
Table 3 PSG variables Group 1
AHI Apnea hypopnea index, SE Sleep efficacy, N1,2,3 Non-REM sleep 1,2,3, R REM sleep Bold values are statistically significant at p* \ 0.05
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duration of N3 phase of sleep (%) (r = -0.53, p \ 0.01) and YF and SaO2 (r = -0.31, p \ 0.01).
Discussion EDS, which is one of the most frequent and troublesome complaints of OSA syndrome, is associated with various unfavorable consequences of this disease such as increased likelihood of traffic accidents, interpersonal problems and reduced productivity . EDS is also reported to reduce quality of life (QOL) in OSA patients . Although the exact molecular mechanisms and factors underlying EDS are not well understood, investigators have ascribed the presence of EDS to nocturnal hypoxemia or sleep fragmentation or both [14, 15]. In OSA patients, increased circulating levels of tumor necrosis factor-a (TNF-a), which results from hypoxia-induced central nervous system inflammation, might play a role in the emerging of sleepiness . Our findings are in agreement with the knowledge that reduced oxygen saturations during apneic episodes might induce hypoxia-related neuronal inflammation in OSA patients, and thus EDS may occur due to the hypoxia-related neuronal damages. Additionally, our findings suggest that decreased oxygen saturation seems to be related with increased sleepiness and YF in OSA patients. Similar to our findings, Schiller stated in his study that yawning was associated with decreased SaO2 and increased carbon dioxide (CO2) concentrations in the human central nervous system . In our study, we showed that yawning frequency is negatively correlated with SaO2 and positively correlated with excessive daytime sleepiness and this correlations are consistent with previous findings. In OSA patients, as hypoxia induced central nervous system alterations, sleep fragmentations may lead to sleepiness [18, 19]. Several reports stated that each arousal and each fragmentation results in increased EDS. Previously, Roure et al., stated that sleep apnea and sleep disruption were not the primary determinants of EDS in all OSA patients ; however, since AHI is correlated with the ESS score we may suggest that as a patient has more apnea/hypopnea during sleep, it is possible for the patient to experience much more excessive daytime sleepiness. Moreover, since the sleep efficacies of our groups were similar, it is possible to suggest that EDS might be related to other factors than sleep efficacy, such as ‘‘decreased SaO2, shortened N3 phases of sleep and increased AHI’’. Concerning about the duration of sleep phases and its relation with excessive daytime sleepiness, it is not impossible to ascribe EDS to shortened N3 phase of sleep according to our findings. While the duration of REM phase of sleep is similar between the groups in our study, significant shortening of the non-REM phases, ‘‘especially the
most restorative N3 phase’’, might be associated with increased ESS scores and eventually increased yawning frequencies. Studies that investigated biorhythm of yawning have stated that yawning has certain characteristics, which reflects its complicated nature. For example, yawning peaks in the beginning of the morning immediately after awaking. Another peak occurs in the late afternoon and finally it reaches its maximum level late in the evening, especially close to bedtime . Similar to these observations, our findings indicate another physiological aspect of this mysterious bio-act. In other words, yawning seems to have a close interaction with diurnal rhythm of the human nature and also with other biologic necessities as sleeping. A previous study, which investigated the association of yawning with the transition between periods of high level activity and low level activity or arousal, stated that yawning was surely only one means of regulating arousal and activity; it may well be a marker of altered level of arousal, rather than a cause . In the light of our findings and other observations, it is possible to associate yawning with sleep. Studies evaluated human adults, provided evidence that yawning occurs approximately 7–8 times a day . An average yawning frequency of our groups was 4–5 and 10–11 per day for groups 1 and 2, respectively. Discrepancy of these average scores might be related to various ‘‘not well-known’’ characteristics of the act of yawning. It is obvious that we need more studies regarding the dark sides of yawning in human. In the light of our results, we may conclude that similar to the shortened N3 phase of sleep, increased Epworth scores and decreased oxygen saturations, increased frequency of yawning may indicate sleep deprivation as well. Our findings revealed that daily frequency of yawning seems related to the degree of EDS of a patient. Physicians who involved with obstructive sleep apnea may adapt ‘‘yawning’’ to their clinical practice in order to predict the sleepiness of their patient. Conflict of interest interest.
Authors declare that there is no competing
Ethical standard The ethics committee of Adana Numune Training and Research Hospital approved the study protocol, and all participants provided informed consent.
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