Eur Arch Otorhinolaryngol DOI 10.1007/s00405-014-3302-1
REVIEW ARTICLE
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.
Keywords Yawning Excessive daytime sleepiness Obstructive sleep apnea Sleep phases
T. Catli (&) Department of Otorhinolaryngology, Bozyaka Teaching and Research Hospital, Karabag˘lar, 35170 Izmir, Turkey e-mail: [email protected]
Introduction
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 [1]. 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
123
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 [7]. Yawning is an easily observable and quantifiable physiological phenomenon, which is believed to be associated with a feeling of comfort [8]. 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 [9]. 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 [10]. 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)
123
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 [11]. 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 [7]. 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)
Sitting reading
investigated with Spearman’s rho correlation analysis. p \ 0.05 was considered statistically significant.
Results
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)
46.07 (±12.7)a
51.55 (±10.2)a
Male
20
61
Female
23
25
27.47
31.79
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 [12]. 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
Group 2
p*
AHI
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86.5
REVIEW ARTICLE
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.
Keywords Yawning Excessive daytime sleepiness Obstructive sleep apnea Sleep phases
T. Catli (&) Department of Otorhinolaryngology, Bozyaka Teaching and Research Hospital, Karabag˘lar, 35170 Izmir, Turkey e-mail: [email protected]
Introduction
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 [1]. 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
123
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 [7]. Yawning is an easily observable and quantifiable physiological phenomenon, which is believed to be associated with a feeling of comfort [8]. 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 [9]. 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 [10]. 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)
123
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 [11]. 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 [7]. 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)
Sitting reading
investigated with Spearman’s rho correlation analysis. p \ 0.05 was considered statistically significant.
Results
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)
46.07 (±12.7)a
51.55 (±10.2)a
Male
20
61
Female
23
25
27.47
31.79
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 [12]. 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
Group 2
p*
AHI
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86.5
