Sleep status and oral function in patients with obstructive sleep apnea

doi:10.21203/rs.3.rs-3953395/v1

Background

Patients with obstructive sleep apnea (OSA) have been reported to have narrowed always during sleep and a reduced capacity to expand the upper airways. Therefore, we examined the oral function of patients with OSA by comparing the results of a questionnaire survey on sleep status and the measurement of maximum tongue pressure between them and healthy controls.

Methods

Twenty-nine patients were enrolled in the OSA group and 29 in the control group. Each participant completed a sleep status questionnaire. Tongue pressure was measured three times, and the highest value was defined as the maximum tongue pressure.

Results

The OSA group had significantly higher percentages of mouth opening during sleep and xerostomia upon awakening than dhe the control group (p = 0.01 and p < 0.001, respectively). The maximum tongue pressure was significantly lower in the OSA than in the control group (p = 0.016).

Conclusion

It is speculated that the activity of the genioglossus muscle, as well as that of other muscles in the patients with OSA, is lower than that healthy participants during tongue pressure generation, which is a momentary action. It is suggested that myofanctional therapy can help improve respiratory function during sleep by increasing the strength of the tongue muscles and upper airway dilator muscles, which also enlarge the upper airway in patients with OSA.

obstructive sleep apnea

tongue pressure

sleep status

oral function

the genioglossus muscle

Obstructive sleep apnea (OSA) is characterized by obstruction of the upper airway during sleep that leads to oxygen desaturation, repeated arousals resulting in fragmented sleep, and excessive daytime sleepiness¹, which causes a decrease in the quality of life.

The activity and elasticity of the upper airway dilator muscles during wakefulness as well as during sleep may have different characteristics between patients with OSA and healthy participants. In OSA, poor upper airway dilator muscle effectiveness is an important phenotype that may result from poor coordination of the neural drive to the various upper airway dilator muscles during sleep^2,3, due to mechanical and histological changes of muscle fiber^4,5. Regarding the pathogenesis of OSA, it is clear that sleep-induced changes in pharyngeal neuromuscular control are paramount and intract synergistically with anatomic characteristics^6,7. Stimulation of the genioglossus (GG) muscle, the largest upper airway dilator muscle, reduces upper airway collapsibility in OSA⁸. However, the mechanism of the lack of activated tongue muscles to maintain patency during sleep is still unclear ^9,10.

Tongue muscle activity is driven by phasic and tonic inputs from the central level and local reflexes triggered by negative airway pressure during inspiration¹¹. During inspiration, the posterior tongue moves forward, and the upper airway dilates. It has been reported that both phasic inspiratory and tonic components of GG EMG recording may be higher in patients with OSA than in healthy participants during wakefulness¹². The upper airway dilator muscles are involved not only in respiratory function but also in swallowing and articulatory function by coordination of a complex neuromuscular system.

Continuous oral breathing during sleep directly affects the position and strength of the tongue as well as that of the orofacial muscles, thereby causing abnormal airway development and sleep-disordered breathing (SDB) in pediatric OSA¹³. Even in adult OSA, it is speculated that oral breathing affects to upper airway collapse during sleep. We hypothesized that tongue muscles as well as upper airway dilator muscles during breathing, had unique characteristics in the patients with OSA compared to healthy participants. Futrhermore, we hypothesized that differences exist in perioral muscle and tongue activity in the patients with OSA. Therefore, we conducted a questionnaire survey on sleep status and measured the maximum tongue pressure ―an oral function assessment― in patients with OSA and healthy participants.

Participants

Twenty-nine patients with OSA (mean age 50.76 ± 10.68 years, 20 males and nine females) who visited Kyushu Dental University Hospital for oral appliance (OA) therapy were enrolled in this study (OSA group). The inclusion criterion was a diagnosis of OSA with no other sleep disorders based on overnight polysomnography performed at a medical institution lasting at least 5 h.

Furthermore, we included 29 healthy participants (mean age 47.76 ± 9.96 years, 21 males and eight females) who matched the age distribution, body mass index(BMI) of the OSA group(control group). This control group was recruited from patients who came to our hospital for dental treatment other than OSA therapy, their families, and dental staffs. They did not exhibit OSA symptoms, and their sleep partner had indicated no snoring and apnea for the last 3 months. The exclusion criteria comprised a history of orthodontic treatment and consecutive missing teeth that would require removable denture application.

The aims and potential risks of the study were explained, and informed consent was obtained from all participants.

Questionnaire survey on sleep status

All participants were asked to answer a questionnaire on sleep status. The questions requested details regarding sleep duration, ease of falling asleep (easy, normal, or difficult), ease of waking up (easy, normal, or difficult), degree of sound sleep (good, normal, or bad), opening of the mouth during sleep (yes, no, or unknown), and xerostomia (yes, no, or unknown). All participants completed the Japanese version of the Epworth sleepiness scale (ESS) [14] to evaluate daytime sleepiness.

Maximum tongue pressure

The tongue pressure was measured three times using a tongue pressure-measuring device (TPM-02, JMS, Hiroshima) ¹⁵. All participants were placed in a relaxed sitting position and asked to place the balloon in their mouth, holding the plastic pipe at the midpoint of their central incisors with closing lips. They were asked to raise their tongues and compress the small balloon onto the palate for approximately 7 seconds with maximum voluntary effort, and the maximum value was recorded. This measurement was performed three times, with the 30 seconds resting time and rinsing the mouth between each measurement. The mean value of the three measurements was defined as the maximum tongue pressure for each participant.

Statistical analysis

All statistical analyses were performed using SPSS for Macintosh version 22.0 software (SPSS, Chicago, IL, USA). The Shapiro-Wilk test was used to assess the normality of the distribution of data. Pearson’s chi-squared test was used to compare the proportion of females and males and sleep status (ease of falling asleep, ease of waking up, degree of sound sleep, mouth opening, and xerostomia) between the two groups. Significant differences in mean values between the two groups were assessed using the parametric Student’s unpaired t-test for ESS and sleep duration and the non-parametric Mann-Whitney U test for maximum tongue pressure. A significant difference was set at p < 0.05, which was two-tailed.

No significant differences were observed between the two groups regarding age, sex, body mass index, or mean sleep duration, and sleep status (Table 1). In the questionnaire survey on sleep status, no significant difference was observed in sleep duration and the percentage of poor sleep onset (p = 0.623, p = 0.196, respectively). The percentages of poor wakefulness and sound sleep were significantly higher in the OSA group than in the control group (p = 0.002 and p < 0.001, respectively). ESS was significantly higher in the OSA group than in the control group (p = 0.002). The OSA group had significantly higher percentages of mouth opening during sleep and xerostomia upon awakening than that the control group (p = 0.001 and p < 0.001, respectively) (Table 2). Maximum tongue pressure in the OSA group was 34.4 (28.5- 39.4), while that in the control group was 41.7 (37.9- 44.0). It was significantly lower in the OSA group than in the control group (p = 0.004) (Fig.1).

Although no significant differences were observed in mean sleep duration and falling asleep between the two groups, the OSA group had a significantly higher ESS score and reported poorer wakefulness and sound sleep than did the control group. Excessive daytime sleepiness is one of the most common symptoms of OSA. In OSA, repetitive apnea or hypopnea occurs during sleep. Long-lasting low levels of arterial blood oxygen saturation lead to an increase in the partial pressure of carbon dioxide in arterial blood. These events are often accompanied by arousal responses. Therefore, repetitive sleep fragmentation leads to excessive daytime sleepiness, difficulty in waking up, and restless sleep despite patients with OSA easily falling asleep.

In swallowing studies, maximum tongue pressure is useful for assessing the level of swallowing function. Tongue pressure decreases with aging. Despite the mean age of OSA group being younger than 60s, this study revealed that the maximum tongue pressure within the OSA group was significantly lower compared to the control group, closely mirroring that of healthy participants in their 60-70s, as reported by Utanohara et al.¹⁵. Low tongue pressure is likely to cause problems not only during swallowing but also respiratory. It was reported that low tongue pressure plays a significant role in the development of OSA because it is typically related to a malfunction of the upper airway dilators muscle¹⁶. Moreover, O'Connor-Reina et al. ¹⁷ demonstrated that low maximum tongue pressure is related to upper airway collapse.

The GG muscle controls the tongue protrusion and points the tip of the tongue upward depending on the contraction ¹⁸. It has been reported that the activity of the GG muscle of patients with OSA is decreased during sleep^19,20. In contract, the GG muscles ^21,12 and the tensor palatini¹² ―an upper airway dilator muscle― exhibit greater EMG activities than those of healthy participants during wakefulness. Several previous studies suggested that the point of smallest pharyngeal airway size in apnea commonly occurs behind the soft palate, with collapse during sleep often occurring at this same site ²². As a result, the muscles controlling palatal position would be expected to be quite active during wakefulness in patients with OSA as a neuromuscular compensation for deficient anatomy. Research has indicated that specific muscles like the geniohyoid, anterior belly of the digastric, mylohyoid, and posterior fiber of the posterior GG are closely associated with higher tongue pressure²³. It is speculated that the activity of the GG muscle, as well as that of other muscles in the patients with OSA, is lower than in healthy participants during tongue pressure generation, which is a momentary action.

Patients with OSA are more likely to have decreased perioral function and muscle strength in the muscles involved in upper airway patency than healthy participants, which may lead to snoring and sleep apnea. Habitual mouth breathing during sleep causes snoring and apnea, and mouth opening during sleep causes xerostomia^24–28. The OSA group showed a significantly higher percentage of mouth opening during sleep and xerostomia upon awakening than that the control group. Mouth opening during sleep causes tongue depression and upper airway obstruction, resulting in snoring and apnea. Causes of mouth breathing include chronic sinusitis, allergies, rhinitis of inflammatory origin, and an abnormal nasal septum²⁹. Constant mouth opening may also cause decreased lip closure during sleep. In this study, the presence of mouth opening and xerostomia during sleep were assessed only from only participants self-reporting. It is necessary to observe sleep dynamics in order to evaluate these factors objecrively. In the future, investigating the lip-closure ability of patients with OSA is crucial.

Jaw-opening ³⁰ and lingual exercises^31,32 have been introduced to treat dysphagia and are expected to strengthen the suprasternal muscle group. There is also a relationship between OSA and craniofacial structure, including mouth breathing resulting from difficulty in closing the lips, narrow dentition, and a large tongue or a long upper airway ³³.It has been reported that physical exercise targeting the myofascial region as an adjuvant therapy for OSA over a fixed period of time can be helpful for the improvement of snoring, daytime sleepiness, quality of sleep, and reduction of neck circumference³⁴. The modality of muscle activity with continuous physical exercise in the submental region might be changed, and the upper airway mighe be kept open during sleep. Villa et al. ³⁵ concluded that tongue pressure by using the Iowa oral performance instrument was significantly lower in children with SDB than in healthy controls, and they suggested that increasing it using myofunctional therapy can be a useful tool to treat SDB. It is suggested that these methods can help improve respiratory function during sleep by increasing the strength of the tongue muscles and upper airway dilator muscles, which also enlarge the upper airway in patients with OSA.

This study had some limitations. The OSA group was recruited from patients with OSA who required OA therapy, which may not be characteristic of the broader population with OSA, as many are candidates for alternative intervention such as continuous positive airway pressure therapy or surgical treatment. The control group, comprised of healthy participants, did not undergo sleep tests as a definitive diagnosis. Therefore, the presence of undiagnosed OSA among these participants cannot be entirely excluded. Often, individuals without subjective OSA symptoms or reports from partners of snoring or apnea may resist recommendations for sleep studies, including pulse oximetry.

In this study, 29 patients with OSA and 29 healthy participants completed a questionnaire on their sleep status, and their maximum tongue pressure was also measured. The OSA group had a significantly higher percentage of mouth opening during sleep and xerostomia upon awakening and significantly lower maximum tongue pressure than did the control group.

obstructive sleep apnea: OSA

the genioglossus muscle: the GG muscle

electromyography :EMG

sleep-disordered breathing: SDB

oral appliance: OA

body mass index: BMI

Epworth sleepiness scale: ESS

apnea-hypopnea index: AHI

standard deviation: SD

Ethics approval and consent to participate: All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments of comparable ethical standards. This study was approved by the Ethics Committee of Kyushu Dental University (approval number: 21-38; approved on March 9, 2022).

Informed consent was obtained from all participants included in this study.

Consent for publication: Not applicable

Availlability of data and maerials: The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Competing interests: The authors declare no conflicts of interest.

Funding: This study did not receive any funding.

Auther’s contributions: Dr. Eri Makihara and Dr. Juwon Lee have full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Dr. Takafumi Watanabe and Dr. Hiromichi Ogusu made special contributions to data collection. Dr. Shin-ichi Masumi and Dr. Seung-Woo Lee made a special contribution to writing and editing assistance.

Acknowledgments: We would like to thank Editage (www.editage.com) for English language editing.

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Table 1. Comparison of participants characteristics between two groups

		OSA group (n=29)	Control group (n=29)	P value
Gender (male/female), n		20/9	21/8	0.773^†
Age, years, mean± SD		50.76±10.68	47.76±9.96	0.273^‡
BMI, kg/m²,mean± SD		23.84±3.17	22.67±2.94	0.152^‡
AHI,mean± SD		17.87±11.61	-	-
Sleep duration, hours, mean± SD		6.64±1.12	6.76±0.85	0.623^‡
ESS		9.59±5.49	5.48±4.16	0.002^‡
Ease of falling asleep (%)	easy	55	66	0.196^†
	normal	35	34
	difficult	10	0
Ease of waking up (%)	easy	14	42	0.002^**†
	normal	34	48
	difficult	52	10
Degree of sound sleep (%)	good	3	21	<0.001^***†
	normal	35	65
	bad	62	14

^†Pearson’s chi-squared test

^‡Student’s unpaired t-test

* p<0.05

** p<0.01

***p<0.001

BMI, body mass index; AHI, apnea-hypopnea index; ESS，Epworth sleepiness scale; SD, standard deviation

Table 2. Comparison of the percentage of mouth opening and xerostomia in two groups

		OSA group (n=29)	Control group (n=29)	P value
Opening mouth (%)	close	14	59	0.001^**†
	open	83	41
	unknown	3	0
Xerostomia (%)	dry	79	24	<0.001^***†
	not dry	0	72
	unknown	21	4

^†Pearson’s chi-squared test

* p<0.05

** p<0.01

***p<0.001

The OSA group had significantly higher percentage of mouth opening during sleep and percentage of xerostomia upon awakening than the control group (p=0.001 and p<0.001, respectively)

No competing interests reported.

Sleep status and oral function in patients with obstructive sleep apnea

Status:

Version 1

Abstract

Background

Methods

Results

Conclusion

Figures

Background

Materials and methods

Participants

Questionnaire survey on sleep status

Maximum tongue pressure

Statistical analysis

Results

Discussion

Conclusion

Abbreviations

Declarations

References

Tables

Additional Declarations

Status:

Version 1