Sleep Breath (2015) 19:377–384 DOI 10.1007/s11325-014-1031-8
ORIGINAL ARTICLE
Swallowing and breathing patterns during sleep in patients with obstructive sleep apnea Kazutomo Yagi & Alan A. Lowe & Najib T. Ayas & John A. Fleetham & Fernanda R. Almeida
Received: 8 April 2014 / Revised: 24 June 2014 / Accepted: 30 June 2014 / Published online: 24 July 2014 # Springer-Verlag Berlin Heidelberg 2014
Abstract Purpose The aims of this study were to determine the frequencies of swallowing and swallowing associated with arousals during sleep in patients with obstructive sleep apnea (OSA) and to determine whether these were associated with the severity of OSA and differed according to the preceding breathing route. Methods Standard audio-video polysomnography including an evaluation of swallowing-related elevation of the thyroid cartilage and breathing route (i.e., nasal or oronasal) was undertaken in an academic sleep laboratory. Fifty-six patients were analyzed (13 non-OSA patients, 17 mild, 10 moderate, and 16 severe OSA). Results The frequency of swallowing per hour of sleep was significantly higher in the severe OSA patients when compared to mild OSA patients (mild OSA, 3.1/h and severe OSA, 8.4/h). This was mainly due to the significantly higher frequency of swallowing associated with a respiratory event-related arousal in the severe OSA patients when compared to non- and mild OSA The institution at which the work was performed was the Faculty of Dentistry and University of British Columbia Hospital Sleep Disorder Program K. Yagi : A. A. Lowe : F. R. Almeida Department of Oral Health Sciences, The University of British Columbia, 2199 Wesbrook Mall, V6T 1Z3 Vancouver, BC, Canada K. Yagi (*) Department of Oral and Maxillofacial Prosthodontics and Oral Implantology, Institute of Health Biosciences, The University of Tokushima, 3-18-15 Kuramoto, 770-8504 Tokushima, Japan e-mail: [email protected] N. T. Ayas : J. A. Fleetham Department of Medicine, The University of British Columbia, 2211 Wesbrook Mall, V6T 2B5 Vancouver, BC, Canada
patients (non-OSA, 0.6/h; mild OSA, 1.0/h; severe OSA, 6.0/h), especially when swallowing was preceded by oronasal breathing (non-OSA, 0.2/h; mild OSA, 0.4/h; severe OSA, 4.2/h). Conclusions Swallowing frequency during sleep can increase with increasing OSA severity in most OSA patients. These events are predominately associated with respiratory eventrelated arousals and are more frequent when preceded by oronasal breathing. The observed swallowing under high ventilatory needs may compromise the maintenance of the pharynx as a conduit for airflow in OSA patients. Keywords Swallowing . Arousal . Breathing route . Obstructive sleep apnea . Apnea-hypopnea index
Introduction The pharynx serves as a common passage for breathing and swallowing. Swallowing interrupts breathing [1], serves in clearing the materials in the pharynx, and plays a defensive role in maintaining the pharynx itself as a conduit for airflow. Obstructive sleep apnea (OSA) is characterized by repetitive obstruction of the pharyngeal airway often resulting in oxygen desaturation and arousals from sleep [2]. In response to respiratory stimuli, arousals have been recognized as part of the respiratory defense mechanism [3]. In a series of frequent respiratory events and arousals in OSA patients, the incidence of swallowing and its relationship to arousal and the preceding airflow has not yet been substantially addressed. Numerous studies have addressed the frequency of swallowing during sleep with a variety of methodological differences in infants [4–7] and in adults [8–14] including healthy subjects [8–11, 13] and patients with OSA [14]. Non-invasive
378
studies of healthy adult subjects suggest that swallowing can be almost exclusively observed concomitant with a brief arousal mainly from sleep stages 1, 2, and REM [9]. Healthy subjects can swallow, on average, 3.7 times per hour of sleep [11], whereas OSA patients may swallow more frequently than do healthy subjects at least during sleep stage 2 [13, 14]. These findings taken together give rise to a view that swallowing in OSA patients may be associated with arousals that are subsequent to respiratory events. The only available observation of nocturnal swallowing in OSA patients is an aforementioned study where the act of swallowing was evaluated based on electromyographic activity alone [14], which may not necessarily represent a transient elevation of the thyroid cartilage [8, 9, 11, 12] with a transient interruption of airflow (swallowing apnea) peculiar to the act of swallowing. Detailed information is not available on actual airflow before swallowing, particularly in terms of breathing route (i.e., nasal or oronasal breathing). The purpose of the present study in OSA patients was to determine the frequencies of swallowing and swallowing associated with arousals during sleep and to determine whether these were associated with the severity of OSA and differed according to the preceding breathing route.
Sleep Breath (2015) 19:377–384
Scoring sleep stages, arousals, and respiratory events
Methods
Sleep stages were manually scored in 30-s epochs (American Academy of Sleep Medicine scoring manual [16]) by experienced and trained sleep technologists blinded to the signal of swallowing-related elevation of the thyroid cartilage and jaw movement. Arousals were scored [17] and classified into spontaneous, limb movement-related, and respiratory event-related arousals (respiratory arousals). Spontaneous arousals were defined as arousals not in association with either limb movements or respiratory events. Respiratory arousals were defined as arousals occurring immediately before or within a 5 s period after the termination of respiratory events. The arousal index indicates the mean number of arousals per hour of sleep. Note that an EEG arousal that lasted more than 15 s and proceeded to a wake epoch was not scored as arousal. Respiratory events were scored according to the criteria published in the American Academy of Sleep Medicine scoring manual [16]. Apnea was defined as cessation of both nasal and oral airflow with its duration more than 10 s. Hypopnea was defined as a reduction in nasal airflow greater than 30 % with a duration of more than 10 s associated with either a decrease in oxygen saturation by at least 3 % or EEG arousal. The apnea-hypopnea index (AHI) indicates the mean number of apneas and hypopneas per hour of sleep. OSA severity was defined based on AHI.
Subjects and sleep study
Analysis of swallowing and breathing route
Seventy five patients with suspected sleep disordered breathing were prospectively and consecutively enrolled for an OSA diagnosis in the University of British Columbia Hospital sleep disorder program. Exclusion criteria included the previous surgery on the soft palate, any form of therapy currently being received for OSA, and neuromuscular disease. Informed consent was approved by the University of British Columbia Human Ethics Committee. Attended audio-video overnight polysomnography included electroencephalogram (EEG), electrooculogram (EOG), chin electromyogram (EMG), nasal pressure transducer, oral thermistor, inductance plethysmograph, leg EMG, echocardiogram (ECG), and pulse oximetry monitors. An oral thermistor was connected to a nasal cannula with a customized holder (YG-122T, Nihon Kohden, Japan). Swallowing-related elevation of the thyroid cartilage was monitored using a non-invasive adhesive piezoelectric sensor (UARS sensor, Ambu A/S, Denmark) placed over the neck superior to the laryngeal prominence. Jaw movement was monitored using a magnetic resonance field transducer (JAWSENS, Nomics, Belgium) to record the vertical distance between the forehead and the lower jaw [15].
Fifty six of 75 patients were eligible for the subsequent analysis of swallowing and breathing route, and consisted of 13 non-OSA, 17 mild OSA, 10 moderate OSA, and 16 severe OSA patients. Exclusion criteria for the remaining 19 patients included a Periodic Limb Movement Index of 15 or greater [16] (16 patients), use of orthodontic retainers (2 patients), and the lack of complete audio-video recording (1 patient). Analysis of swallowing and breathing route in all sleep epochs was attempted. However, in five patients (three non-OSA and two moderate OSA patients), repositioning of the nasal cannula with the oral thermistor was needed by an attended sleep technologist during the sleep study. In these patients, the epochs that included the signal loss of nasal and oral airflow were not evaluated, and 82.8–96.1 % of total sleep epochs were analysed. Swallowing events were visually scored by the first author blinded to the EEG signals with the assistance of an audiovideo recording to avoid artifacts of body and head movements, cough, and vocalization. A swallowing event was defined as simultaneous signals of an increase in chin EMG activity, a transient elevation of the thyroid cartilage, and a transient interruption of nasal airflow (swallowing apnea) as shown in Fig. 1.
Sleep Breath (2015) 19:377–384
379
Fig. 1 Thirty second epoch sleep stage N2 recordings showing a a swallow associated with a spontaneous arousal preceded by nasal breathing (in the middle of the epoch) and a following subsidiary swallow (in the end of the epoch) in a mild OSA patient; b a swallow associated with an arousal preceded by oronasal breathing after a respiratory event (in the middle of the epoch) in a severe OSA patient. During swallowing, an early increase in chin EMG activity, a transient interruption of nasal airflow (swallowing apnea indicated by the solid bars), and a transient movement of the thyroid cartilage can be seen. Note that, in Fig. 1a, there are two swallows which are counted as one swallowing event from the perspective of the relationship between a swallowing event, EEG arousal, and breathing route that precedes a swallowing event, as described in the
methods. LOC-A2, left electrooculogram; C3-A2, left centrocephalic electrode; C4-A1, right centrocephalic electrode; O1-A2, left occipital electrode; O2-A1, right occipital electrode; Chin EMG, chin electromyogram; nasal pressure, airflow via the nose (inspiration corresponds to upward deflection); oral airflow, airflow via the oral cavity; thyroid cartilage, movement of the thyroid cartilage; jaw, the vertical distance between the forehead and the lower jaw (jaw closing corresponds to upward deflection); leg EMG, anterior tibialis electromyogram; sum, summation of the signals of inductance plethysmograph on the ribcage and abdomen; ribcage, inductance plethysmograph on the ribcage; abdomen, inductance plethysmograph on the abdomen
Swallowing events observed in the epochs staged as sleep were identified, and the frequency of swallowing per hour of sleep was calculated (i.e., the number of swallowing events per 120 sleep epochs evaluated). A swallowing event was sometimes repetitive. We selected and analyzed a swallow that occurred in isolation and the first swallow that was followed by subsidiary swallows with an interval of less than 10 s apart between the onsets of adjoining swallows. Breathing routes were classified in each 30-s epoch as nasal breathing or oral and oronasal breathing (We assigned oral breathing to oronasal breathing) as well as the absence of airflow. A nasal breathing epoch was defined as an epoch
containing at least one phasic signal from the nasal transducer alone, the amplitude of which was numerically defined to be more than or equal to fourfold of the background signal noise. An oronasal breathing epoch was defined as an epoch containing at least one phasic signal on the oral thermistor sensor, the amplitude of which was numerically defined to be more than or equal to fourfold of the background signal noise. The percentage of nasal breathing epochs per total sleep epochs evaluated was calculated. When a swallowing event was associated with an EEG arousal, it was classified as to its relationship to either a spontaneous, limb movement-related, or respiratory arousal.
380
Sleep Breath (2015) 19:377–384
In addition, the swallowing event was further classified as to its relationship with the preceding breathing route, either nasal or oronasal breathing, based on airflow signals for a 5 s period before the onset of a swallow. Repeatability of swallowing event identification To assess the repeatability of swallowing event identification, rescoring was done in 20 randomly selected patients, 2 months after the first scoring, and an intraclass correlation coefficient value between the first and second scorings was calculated. Statistical analysis Statistical tests were made using the Statistical Package for the Social Sciences (SPSS, SPSS Inc., Chicago, IL, USA). The Kruskal–Wallis analysis of variance assessed the differences in anthropometric and sleep variables, the frequency of swallowing per hour of sleep, and the percentage of nasal breathing epochs per total sleep epochs between the four patient groups. When the analysis of variance showed a P value less than 0.05, comparisons between the four patient groups were performed using the Scheffe test. Spearman’s
correlation tests were also performed. P values less than 0.05 were considered to be statistically significant.
Results Subjects and sleep variables Fifty-six of 75 patients were eligible for the analysis of swallowing and breathing route, and consisted of 13 nonOSA, 17 mild OSA, 10 moderate OSA, and 16 severe OSA subjects. Anthropometric and sleep variables of the 56 patients according to four patient groups based on AHI severity (Table 1) showed no significant difference in height, weight, body mass index, or sleep variables, except for age and arousal indices. Age was significantly higher in the severe OSA patients when compared to the non-OSA patients (P=0.024). The spontaneous arousal index was significantly lower in the severe OSA patients when compared to the mild OSA patients (P=0.009). In contrast, the respiratory arousal index was significantly higher in the severe OSA patients when compared to the non- (P
ORIGINAL ARTICLE
Swallowing and breathing patterns during sleep in patients with obstructive sleep apnea Kazutomo Yagi & Alan A. Lowe & Najib T. Ayas & John A. Fleetham & Fernanda R. Almeida
Received: 8 April 2014 / Revised: 24 June 2014 / Accepted: 30 June 2014 / Published online: 24 July 2014 # Springer-Verlag Berlin Heidelberg 2014
Abstract Purpose The aims of this study were to determine the frequencies of swallowing and swallowing associated with arousals during sleep in patients with obstructive sleep apnea (OSA) and to determine whether these were associated with the severity of OSA and differed according to the preceding breathing route. Methods Standard audio-video polysomnography including an evaluation of swallowing-related elevation of the thyroid cartilage and breathing route (i.e., nasal or oronasal) was undertaken in an academic sleep laboratory. Fifty-six patients were analyzed (13 non-OSA patients, 17 mild, 10 moderate, and 16 severe OSA). Results The frequency of swallowing per hour of sleep was significantly higher in the severe OSA patients when compared to mild OSA patients (mild OSA, 3.1/h and severe OSA, 8.4/h). This was mainly due to the significantly higher frequency of swallowing associated with a respiratory event-related arousal in the severe OSA patients when compared to non- and mild OSA The institution at which the work was performed was the Faculty of Dentistry and University of British Columbia Hospital Sleep Disorder Program K. Yagi : A. A. Lowe : F. R. Almeida Department of Oral Health Sciences, The University of British Columbia, 2199 Wesbrook Mall, V6T 1Z3 Vancouver, BC, Canada K. Yagi (*) Department of Oral and Maxillofacial Prosthodontics and Oral Implantology, Institute of Health Biosciences, The University of Tokushima, 3-18-15 Kuramoto, 770-8504 Tokushima, Japan e-mail: [email protected] N. T. Ayas : J. A. Fleetham Department of Medicine, The University of British Columbia, 2211 Wesbrook Mall, V6T 2B5 Vancouver, BC, Canada
patients (non-OSA, 0.6/h; mild OSA, 1.0/h; severe OSA, 6.0/h), especially when swallowing was preceded by oronasal breathing (non-OSA, 0.2/h; mild OSA, 0.4/h; severe OSA, 4.2/h). Conclusions Swallowing frequency during sleep can increase with increasing OSA severity in most OSA patients. These events are predominately associated with respiratory eventrelated arousals and are more frequent when preceded by oronasal breathing. The observed swallowing under high ventilatory needs may compromise the maintenance of the pharynx as a conduit for airflow in OSA patients. Keywords Swallowing . Arousal . Breathing route . Obstructive sleep apnea . Apnea-hypopnea index
Introduction The pharynx serves as a common passage for breathing and swallowing. Swallowing interrupts breathing [1], serves in clearing the materials in the pharynx, and plays a defensive role in maintaining the pharynx itself as a conduit for airflow. Obstructive sleep apnea (OSA) is characterized by repetitive obstruction of the pharyngeal airway often resulting in oxygen desaturation and arousals from sleep [2]. In response to respiratory stimuli, arousals have been recognized as part of the respiratory defense mechanism [3]. In a series of frequent respiratory events and arousals in OSA patients, the incidence of swallowing and its relationship to arousal and the preceding airflow has not yet been substantially addressed. Numerous studies have addressed the frequency of swallowing during sleep with a variety of methodological differences in infants [4–7] and in adults [8–14] including healthy subjects [8–11, 13] and patients with OSA [14]. Non-invasive
378
studies of healthy adult subjects suggest that swallowing can be almost exclusively observed concomitant with a brief arousal mainly from sleep stages 1, 2, and REM [9]. Healthy subjects can swallow, on average, 3.7 times per hour of sleep [11], whereas OSA patients may swallow more frequently than do healthy subjects at least during sleep stage 2 [13, 14]. These findings taken together give rise to a view that swallowing in OSA patients may be associated with arousals that are subsequent to respiratory events. The only available observation of nocturnal swallowing in OSA patients is an aforementioned study where the act of swallowing was evaluated based on electromyographic activity alone [14], which may not necessarily represent a transient elevation of the thyroid cartilage [8, 9, 11, 12] with a transient interruption of airflow (swallowing apnea) peculiar to the act of swallowing. Detailed information is not available on actual airflow before swallowing, particularly in terms of breathing route (i.e., nasal or oronasal breathing). The purpose of the present study in OSA patients was to determine the frequencies of swallowing and swallowing associated with arousals during sleep and to determine whether these were associated with the severity of OSA and differed according to the preceding breathing route.
Sleep Breath (2015) 19:377–384
Scoring sleep stages, arousals, and respiratory events
Methods
Sleep stages were manually scored in 30-s epochs (American Academy of Sleep Medicine scoring manual [16]) by experienced and trained sleep technologists blinded to the signal of swallowing-related elevation of the thyroid cartilage and jaw movement. Arousals were scored [17] and classified into spontaneous, limb movement-related, and respiratory event-related arousals (respiratory arousals). Spontaneous arousals were defined as arousals not in association with either limb movements or respiratory events. Respiratory arousals were defined as arousals occurring immediately before or within a 5 s period after the termination of respiratory events. The arousal index indicates the mean number of arousals per hour of sleep. Note that an EEG arousal that lasted more than 15 s and proceeded to a wake epoch was not scored as arousal. Respiratory events were scored according to the criteria published in the American Academy of Sleep Medicine scoring manual [16]. Apnea was defined as cessation of both nasal and oral airflow with its duration more than 10 s. Hypopnea was defined as a reduction in nasal airflow greater than 30 % with a duration of more than 10 s associated with either a decrease in oxygen saturation by at least 3 % or EEG arousal. The apnea-hypopnea index (AHI) indicates the mean number of apneas and hypopneas per hour of sleep. OSA severity was defined based on AHI.
Subjects and sleep study
Analysis of swallowing and breathing route
Seventy five patients with suspected sleep disordered breathing were prospectively and consecutively enrolled for an OSA diagnosis in the University of British Columbia Hospital sleep disorder program. Exclusion criteria included the previous surgery on the soft palate, any form of therapy currently being received for OSA, and neuromuscular disease. Informed consent was approved by the University of British Columbia Human Ethics Committee. Attended audio-video overnight polysomnography included electroencephalogram (EEG), electrooculogram (EOG), chin electromyogram (EMG), nasal pressure transducer, oral thermistor, inductance plethysmograph, leg EMG, echocardiogram (ECG), and pulse oximetry monitors. An oral thermistor was connected to a nasal cannula with a customized holder (YG-122T, Nihon Kohden, Japan). Swallowing-related elevation of the thyroid cartilage was monitored using a non-invasive adhesive piezoelectric sensor (UARS sensor, Ambu A/S, Denmark) placed over the neck superior to the laryngeal prominence. Jaw movement was monitored using a magnetic resonance field transducer (JAWSENS, Nomics, Belgium) to record the vertical distance between the forehead and the lower jaw [15].
Fifty six of 75 patients were eligible for the subsequent analysis of swallowing and breathing route, and consisted of 13 non-OSA, 17 mild OSA, 10 moderate OSA, and 16 severe OSA patients. Exclusion criteria for the remaining 19 patients included a Periodic Limb Movement Index of 15 or greater [16] (16 patients), use of orthodontic retainers (2 patients), and the lack of complete audio-video recording (1 patient). Analysis of swallowing and breathing route in all sleep epochs was attempted. However, in five patients (three non-OSA and two moderate OSA patients), repositioning of the nasal cannula with the oral thermistor was needed by an attended sleep technologist during the sleep study. In these patients, the epochs that included the signal loss of nasal and oral airflow were not evaluated, and 82.8–96.1 % of total sleep epochs were analysed. Swallowing events were visually scored by the first author blinded to the EEG signals with the assistance of an audiovideo recording to avoid artifacts of body and head movements, cough, and vocalization. A swallowing event was defined as simultaneous signals of an increase in chin EMG activity, a transient elevation of the thyroid cartilage, and a transient interruption of nasal airflow (swallowing apnea) as shown in Fig. 1.
Sleep Breath (2015) 19:377–384
379
Fig. 1 Thirty second epoch sleep stage N2 recordings showing a a swallow associated with a spontaneous arousal preceded by nasal breathing (in the middle of the epoch) and a following subsidiary swallow (in the end of the epoch) in a mild OSA patient; b a swallow associated with an arousal preceded by oronasal breathing after a respiratory event (in the middle of the epoch) in a severe OSA patient. During swallowing, an early increase in chin EMG activity, a transient interruption of nasal airflow (swallowing apnea indicated by the solid bars), and a transient movement of the thyroid cartilage can be seen. Note that, in Fig. 1a, there are two swallows which are counted as one swallowing event from the perspective of the relationship between a swallowing event, EEG arousal, and breathing route that precedes a swallowing event, as described in the
methods. LOC-A2, left electrooculogram; C3-A2, left centrocephalic electrode; C4-A1, right centrocephalic electrode; O1-A2, left occipital electrode; O2-A1, right occipital electrode; Chin EMG, chin electromyogram; nasal pressure, airflow via the nose (inspiration corresponds to upward deflection); oral airflow, airflow via the oral cavity; thyroid cartilage, movement of the thyroid cartilage; jaw, the vertical distance between the forehead and the lower jaw (jaw closing corresponds to upward deflection); leg EMG, anterior tibialis electromyogram; sum, summation of the signals of inductance plethysmograph on the ribcage and abdomen; ribcage, inductance plethysmograph on the ribcage; abdomen, inductance plethysmograph on the abdomen
Swallowing events observed in the epochs staged as sleep were identified, and the frequency of swallowing per hour of sleep was calculated (i.e., the number of swallowing events per 120 sleep epochs evaluated). A swallowing event was sometimes repetitive. We selected and analyzed a swallow that occurred in isolation and the first swallow that was followed by subsidiary swallows with an interval of less than 10 s apart between the onsets of adjoining swallows. Breathing routes were classified in each 30-s epoch as nasal breathing or oral and oronasal breathing (We assigned oral breathing to oronasal breathing) as well as the absence of airflow. A nasal breathing epoch was defined as an epoch
containing at least one phasic signal from the nasal transducer alone, the amplitude of which was numerically defined to be more than or equal to fourfold of the background signal noise. An oronasal breathing epoch was defined as an epoch containing at least one phasic signal on the oral thermistor sensor, the amplitude of which was numerically defined to be more than or equal to fourfold of the background signal noise. The percentage of nasal breathing epochs per total sleep epochs evaluated was calculated. When a swallowing event was associated with an EEG arousal, it was classified as to its relationship to either a spontaneous, limb movement-related, or respiratory arousal.
380
Sleep Breath (2015) 19:377–384
In addition, the swallowing event was further classified as to its relationship with the preceding breathing route, either nasal or oronasal breathing, based on airflow signals for a 5 s period before the onset of a swallow. Repeatability of swallowing event identification To assess the repeatability of swallowing event identification, rescoring was done in 20 randomly selected patients, 2 months after the first scoring, and an intraclass correlation coefficient value between the first and second scorings was calculated. Statistical analysis Statistical tests were made using the Statistical Package for the Social Sciences (SPSS, SPSS Inc., Chicago, IL, USA). The Kruskal–Wallis analysis of variance assessed the differences in anthropometric and sleep variables, the frequency of swallowing per hour of sleep, and the percentage of nasal breathing epochs per total sleep epochs between the four patient groups. When the analysis of variance showed a P value less than 0.05, comparisons between the four patient groups were performed using the Scheffe test. Spearman’s
correlation tests were also performed. P values less than 0.05 were considered to be statistically significant.
Results Subjects and sleep variables Fifty-six of 75 patients were eligible for the analysis of swallowing and breathing route, and consisted of 13 nonOSA, 17 mild OSA, 10 moderate OSA, and 16 severe OSA subjects. Anthropometric and sleep variables of the 56 patients according to four patient groups based on AHI severity (Table 1) showed no significant difference in height, weight, body mass index, or sleep variables, except for age and arousal indices. Age was significantly higher in the severe OSA patients when compared to the non-OSA patients (P=0.024). The spontaneous arousal index was significantly lower in the severe OSA patients when compared to the mild OSA patients (P=0.009). In contrast, the respiratory arousal index was significantly higher in the severe OSA patients when compared to the non- (P
