Abstract
Objective: To compare upper airway pressures in snorers and nonsnorers during sleep and wakefulness. Design: Case series of snorers and nonsnoring controls.
Setting: Sleep clinic of a university hospital.
Methods: We used open catheters to measure differential nasopharyngeal and hypopharyngeal pressures in 8 nonapneic snorers with excessive daytime tiredness and 10 healthy nonsnoring controls. Measurements were performed during sleep (with the mouth taped to ensure exclusively nasal breathing) and wakefulness. When awake, the subjects were either seated (with the head neutral, flexed, extended, or rotated) or recumbent (dorsal and lateral positions).
Main Outcome Measures: Comparison of pressures within the group as a function of body position and between the groups as a function of snoring.
Results: Differential nasal and pharyngeal pressures were similar in seated snorers and nonsnorers independently of head position. Assumption of recumbency resulted in significantly increased pharyngeal pressures in nonsnorers (26 18 Pa seated vs. 52 46 Pa recumbent, p < .05) and snorers (50 35 Pa seated vs. 93 38 recumbent, p < .01). The increase was higher in snorers than nonsnorers. During snoring, sleep differential pharyngeal pressures in snorers were markedly increased compared to quiet sleep (567 450 Pa during snoring epochs vs. 117.t 82 Pa during nonsnoring epochs, p < .01).
Conclusions: Compared to nonsnorers, recumbent nonapneic snorers have elevated differential pharyngeal pressures indicative of increased upper airway resistance and reduced airway patency; this is present during wakefulness and sleep.
Sommaire
Objectif: Comparer la pression des voies respiratoires superieures (VRS) des ronfleurs et des non-ronfleurs durant l'eveil et le sommeil.
Localisation: Clinique du sommeil d'un hopital universitaire.
Methode: Nous avons utilise des catheteres pour mesurer les pressions differentielles entre le nasopharynx et Phypopharynx de 8 ronfleurs non-apneiques avec fatigue diurne exageree et 10 controles non-ronfleurs. Durant le sommeil, les pressions ont ete mesurees avec la bouche fermee par du sparadrap pour assurer une respiration exclusivement nasale. Durant l'eveil, les mesures ont ete prises soft en position assise (avec la tete en position neutre, flechie, etendues, ou en rotation) soit en decubitus (dorsal ou lateral).
Mesures: Comparaison des pressions A l'interieur des groupes en fonction de la position et entre les grouper en fonction du ronflement.
Resultats: Les pressions differentielles sont les memes en position assise autant pour les ronfleurs que les non-ronfleurs quelle que soit la position de la tete. Le passage au decubitus augmente tes pressions pharyngees autant pour les non-ronfleurs (26 +/- 18 Pa assis vs 52 +/- 46 Pa couche, p < .05) et les ronfleurs (30 +/- 35 Pa assis vs 93 +/- 38 couche, p < .01). L'augmentation est plus grande chez les ronfleurs que les non-ronfleurs. Durant le ronflement, la difference de pression pharyngee des ronfleurs est encore plus marquee (567 +/- 450 Pa vs 117 +/- 82 Pa, p < .01)
Conclusions: Par rapport aux non-ronfleurs, les ronfleurs ont une pression pharyngee differentiel le elevee indicatrice d'une augmentation de la resistance des voies respiratoires superieures et d'une diminution de la permeabilite presenter autant durant l'eveil que le sommeil.
Key words: daytime tired snorers, differential nasal and pharyngeal pressures, nonsnorers
Sleep-related upper airway obstruction and changes in airway pressures have been studied by many investigators during the past two decades in attempts to elucidate the pathophysiology of the obstructive sleep apnea syndrome (OSAS). This syndrome is characterized by repetitive episodes of increased airflow resistance of upper airway segments, culminating in complete pharyngeal closure.13 The vast majority of patients with sleep apnea snore, suggesting that snoring may be a good surrogate marker of increased upper airway resistance. This is important in view of the recent work suggesting that repetitive episodes of increased upper airway resistance in nonapneic snorers may lead to similar pathologic consequences as in patients with OSAS.4 The term "upper airway resistance syndrome" (UARS) has been introduced to describe nonapneic patients who snore and are tired, fatigued, or sleepy during the day. However, because patients with UARS have been investigated much less than patients with OSAS, the opinions regarding the role of upper airway resistance and pharyngeal compliances5-13 differ among various investigators. These differences are due in part to inconsistent definitions of nonapneic snorers and to the fact that few sleep laboratories assess snoring objectively or measure ventilation directly.14-16
Consequently, the purpose of the present study was to test the hypothesis that upper airway resistance in nonapneic snorers with daytime tiredness is higher when compared to nonsnoring well-functioning controls.
Material and Methods
Eight male snoring subjects with the primary complaint of daytime tiredness were recruited. They were all medically healthy, on no medications, and had a normal ear, nose, and throat examination. A group of 10 healthy nonsnoring subjects without any daytime dysfunction served as control. Measurements of upper airway pressures were carried out during wakefulness (seated and recumbent) and sleep (recumbent).
All subjects had full nocturnal polysomnography, which included monitoring of electroencephalograms, electro-oculograms, anterior tibial electromyograms, electrocardiograms, oxygen saturation using pulse oximeter, and extensive measures of respiration including measurement of snoring sounds, abdominal and thoracic movements, airflow, and upper airway pressures. All polysomnograms were scored by a licensed sleep technologist according to the criteria of Rechtschaffen and Kales.17
Snoring was measured by using a sound meter and a microphone.lg The latter was placed on the forehead just above the level of the nasion. Sound pressure sensed by the microphone was measured by the sound meter, which has a measuring range of 40 to 120 kB and a relatively flat frequency response (+/- 2 dB between 30 and 2000 Hz). The output of the sound meter was sampled by the analogue-to-digital converter at a frequency of 5 Hz. With this set-up, normal breathing registers at less than 50 dB. Abdominal and thoracic movements were measured using inductance plethysmography (Respitrace). Airflow was measured using two methods: oronasal thermistors and modified continuous positive airway pressure (CPAP) mask serving as a pneumotachograph, which was securely applied to avoid leaks. Upper airway pressures were measured using two open catheters (infant feeding tubes 8F) with the lateral openings near their tips. They were inserted nasally and placed at the nasopharyngeal and hypopharyngeal levels (8 and 16 cm from the anterior nares, respectively). Differential pharyngeal pressures ((Delta)Ppharynx) were measured between the nasopharynx and hypopharynx. Differential nasal pressure ((Delta)Pnose) was measured between the nasopharynx and anterior nares. Posture was monitored by infrared video. To ensure exclusively nasal breathing, all subjects slept with their lips taped together.
During wakefulness, upper airway pressures were measured as a function of posture and head position. When seated, the measurements were carried out with the head in a neutral position, flexed, extended, and rotated. When recumbent, measurements were carried out in lateral and dorsal positions. Three series each of eight successive breathing cycles were recorded for each position. Immediately before and after each series, atmospheric zero was confirmed by instructing the subject to open the mouth and hold the breath.
All respiratory signals were transduced, amplified, and simultaneously displayed on a chart recorder (Grass Model 78D, Grass, USA), as well as digitized at 50 Hz. A desktop computer with custom-written software (Cole Rhinomanometry System, Toronto, ON) was used to compute and display respiratory rate, minute ventilation, tidal volume, inspiratory and expiratory flow, nasal and pharyngeal pressure, and resistance.
The data were analyzed using Student's t-tests for paired and unpaired observations as appropriate for comparisons within and between groups. Statistical significance was defined as p < .05.
Results
Snorers were significantly older than nonsnorers (Table 1) but had similar body mass index. Both groups were nonapneics (apnea/hypopnea index < 10), although snorers had more respiratory events per hour of sleep than nonsnorers.
Differential nasal and pharyngeal pressures during wakefulness and sleep are summarized in Table 2. Identical relationships were found for the calculated values of nasal and pharyngeal resistance.
Differential Nasal Pressure
((Delta)Pnose-Anterior Nares to Nasopharynx)
Wakefulness. There were no significant differences within groups for any seated or recumbent position. In addition, there was no difference between groups for any condition; in particular, assumption of recumbency did not produce any changes in nasal pressure in either group.
Sleep. In snorers, nasal pressure measured during sleep was significantly higher than that measured in recumbent posture during wakefulness. In nonsnorers, no significant differences in pressures measured during sleep and wakefulness were found.
Differential Pharyngeal Pressure
((Delta)Ppharynx-Nasopharynx to Hypopharynx)
Wakefulness. Although the results in Table 2 suggest that in both groups, pharyngeal pressures with the head flexed were higher than for other head postures, there were no statistically significant differences for different head postures within each group. Furthermore, there was no difference in pressures between the groups when patients were measured while seated with different head positions.
During recumbency, pharyngeal pressures were significantly higher than when patients were seated within each group. Furthermore, there was a significant difference between groups, with snorers having consistently higher pressures than nonsnorers. Changes from dorsal to lateral recumbency did not significantly alter pharyngeal pressures in either controls or snorers.
Sleep. During quiet (i.e., nonsnoring) breathing, pharyngeal pressures were unchanged by transition from wakefulness to sleep in both snorers and controls. In addition, no significant pressure changes related to sleep stages were detected in either group when snoring periods were omitted among snorers.
However, during snoring epochs, pharyngeal pressure was significantly increased in snorers compared to quiet breathing. This increase was present in REM and non-REM sleep, being most pronounced in nonREM sleep.
Discussion
In the present study, we found that (1) nasal pressures measured during wakefulness are similar in snorers and nonsnorers and do not vary with head to body position; (2) during snoring epochs in REM sleep and during quiet, nonsnoring sleep nasal resistance in snorers is higher than in nonsnorers; (3) pharyngeal pressure during recumbent wakefulness is higher in snorers than in nonsnorers; and (4) during snoring epochs in REM and non-REM sleep, pharyngeal pressure is higher in snorers, but during nonsnoring sleep, it is similar.
Differential Nasal Pressure
Previous investigations of nasal resistance and its impact on snoring and breathing disturbances in sleep have reached varying conclusions. Several authors found a close relationship between increased nasal resistance, snoring, and respiratory disturbances,5,10 whereas recent investigations do not lend support to this view.69 Our results showing higher nasal pressures during sleep in snorers are similar to those of Lenders et al.10 However, we found in addition that this increase in nasal pressure persists even in the absence of audible snoring. This suggests that the relationship between nasal resistance and snoring is probably nonlinear and complex.
We did not find significant differences in nasal pressure during wakefulness between snorers and nonsnorers, independently of body or head position. These findings are similar to those obtained by Miljeteig et al.,6,7 who found that nasal resistance was little affected by body posture in the majority of healthy subjects.
Lack of differences in nasal resistance during wakefulness is not surprising, given that neither the snorers nor the controls had any significant structural mucosal abnormalities of the nose during physical examination. However, there were differences in nasal pressure during sleep, implying that there may be functional differences in nasal mucosal properties between snorers and nonsnorers. It is possible that snorers have increased sensitivity to irritant stimuli (e.g., induced by the nasal catheter), increased filling of the capacitance vessels during sleep, or disturbed autonomic regulation of nasal resistance during sleep.
Differential Pharyngeal Pressure
These pressures were somewhat higher than those reported in earlier studies.13 This is partly explained by our definition, which was based on peak rather than average pressure.
Pharyngeal pressures measured in seated and awake snorers and nonsnorers were similar. Furthermore, neither snorers nor nonsnorers demonstrated any significant changes in pharyngeal pressure with head position. This finding is in contrast with the results of Liistro et al.,19 who found that pharyngeal resistance differs with head position, increasing during flexion and decreasing during extension. Our data show a similar trend, but the interindividual variability and small number of subjects did not permit statistical significance to be reached. It is possible that measurements in a larger group would demonstrate significant reduction in pharyngeal resistance during neck extension. If so, it would in part explain the common observation that many patients (particularly children) with obstructive sleep apnea prefer to sleep on their sides with the neck extended (i.e., opisthotonus) than with the neck flexed (i.e., in the fetal position).
On assumption of recumbency, pharyngeal pressures increased in nonsnorers and snorers when compared to the sitting position, with the latter group exhibiting a much larger increase. These findings are similar to those of Tvinnerheim et al.13 and suggest that the pharynx probably narrows passively in response to gravitational forces. It is possible that snorers have higher pharyngeal compliance than nonsnorers even during wakefulness, which would explain greater narrowing of the pharynx in this group.
During sleep, nonsnorers had similar pharyngeal pressures regardless of the particular sleep stage (REM or non-REM). However, snorers behaved differently, exhibiting almost sixfold higher pharyngeal pressures during snoring epochs (independently of sleep stage) than during nonsnoring sleep. It is interesting that despite higher nasal pressure during quiet (i.e., nonsnoring) breathing in snorers, no elevation in pharyngeal pressure was observed. This suggests that a significant correlation between nasal and pharyngeal pressures is unlikely. Since nasal resistance is a major contributing factor of transmural pressures in the upper airway, a passive and compliant pharynx should respond to it by altering its lumen-narrowing in inspiration and widening in expiration. This would lead to corresponding changes in resistance to airflow, which, in turn, would be reflected in alteration of pharyngeal pressure. This is contrary to what we observed, thus lending support to the results of several investigators 12,13 who did not find that passive pharyngeal compliance alone is a major contributing factor to pharyngeal obstruction during sleep; it is very likely that alterations in the tone of upper airway muscles during sleep make an important contribution to the properties of pharyngeal walls and consequent changes in pharyngeal lumen.
There are several possible reasons that account for the observed differences in pharyngeal pressures between snorers and nonsnorers on assumption of recumbency.
One possibility is that these differences are age related. It is possible that natural aging increases pharyngeal compliance by reducing the tone of upper airway muscles. This is probably not an important factor in our group of subjects; our snorers were not particularly old, and the age difference between them and nonsnorers, although statistically significant, is probably of minor clinical relevance. Consequently, it is unlikely that age alone is responsible for reduction of pharyngeal patency.
Another possibility is that snorers had increased fat deposition in the pharynx. This could reduce pharyngeal patency and increase compliance of pharyngeal walls. Although our snoring patients had similar body mass index as the nonsnoring controls, this does not preclude differences in regional fat distribution. Furthermore, it is possible that muscle to fat ratio in the pharynx decreases with age, so that our snoring patients have reduced muscle mass, thus adding to the pharyngeal resistance by decreasing airway patency.
A third possibility to be considered is a disturbance in the neuromuscular control. We found significantly higher differential pharyngeal peak pressures both in inspiration and expiration during snoring, reflecting a reduced pharyngeal airway patency and increased resistance in both phases of breathing. The increase in resistance during expiration demonstrates that narrowing of the pharynx persists despite positive pressure. One explanation for this may relate to disturbed dilator muscle activity during breathing in snorers. In nonsnoring subjects, decrease in pharyngeal patency during sleep is counterbalanced by an airflow-induced dilator muscle activity2,21; it is possible that this reflex is blunted in snorers, leading to excessive pharyngeal closure. In addition, there could be a variety of pathologic changes affecting upper airway calibre,22,23 including altered mucosal properties, as suggested above.
Our results have implications for better understanding of upper airway resistance syndrome. This syndrome, characterized by daytime dysfunction in the absence of sleep apnea, is thought to be secondary to repetitive episodes of increased upper airway resistance, leading to increased work of breathing, arousals, and sleep fragmentation. Although we did not perform objective measures of daytime function, it is noteworthy that our nonapneic snorers who complained of daytime tiredness had greater pharyngeal resistance than asymptomatic nonsnorers. This encouraging finding indicates the need for further studies in well-defined groups of nonapneic snorers and controls. These studies must include simultaneous measurements of pharyngeal resistance and arousals, as well as objective assessment of daytime function. It is only with the help of such studies that we can confirm the existence of upper resistance syndrome and understand its pathogenesis.
Conclusions
We found several significant differences in upper airway patency between snorers and nonsnorers, including reduction in nasal patency in snorers during sleep and elevation of differential pharyngeal pressures, indicative of reduced airway patency, in awake recumbent snorers and also during sleep when snoring is present. We speculate that these findings may be a result of reduction in pharyngeal muscle tone with age, altered mucosal properties, and/or differences in neuromuscular reflexes. Measurement of pharyngeal resistance, even during wakefulness, may add important information to the understanding and diagnosis of sleep-related upper airway obstruction. Finally, our results emphasize that nonapneic snorers with excessive daytime sleepiness constitute a specific category of patients in the continuum from snoring to obstructive sleep apnea.
Acknowledgement
The technical assistance of Victor Yap and Patrick Misale, Medical Engineering, St. Michael's Hospital, Toronto, is gratefully acknowledged, as well as the review by Dr. Mans Magnusson, ENT Department, University of Lund, Sweden.
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Received 06/12/99. Received revised 25/04/00. Accepted for publication 04/07/00.
Soren Berg, Philip Cole, and James S.J. Haight: Department of Otolaryngology, Victor Hoffstein: Department of Respirology, St. Michael's Hospital, Toronto, Ontario; Soren Berg: Department of Otolaryngology-Head and Neck Surgery, University of Lund, Lund, Sweden.
This study was supported by the University of Toronto and the University of Lund.
Address reprint requests to: Dr. Soren Berg, Department of Otorhinolaryngology-Head and Neck Surgery, University Hospital, S-221 85 Lung, Sweden.
Copyright Decker Periodicals, Inc. Apr 2001