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. 2024 Jan 31;19(1):e0295232. doi: 10.1371/journal.pone.0295232

Exploring the dynamics of snoring in relation to sleep stages: Implications for gender differences, sleep position, and upper airway collapsibility

Masaaki Suzuki 1,2,*, Yuichi Kawai 1, Yoshihiro Funayama 2
Editor: Marco Zaffanello3
PMCID: PMC10830031  PMID: 38295094

Abstract

Objective

The purpose of this study was to determine the sleep stage during which isolated snoring occurs in children and adults, and to analyze changes after treatment of obstructive sleep apnea (OSA).

Methods

This retrospective study examined duration of snoring time and respiratory events during each sleep stage in adults and children who underwent polysomnography, had an apnea-hypopnea index (AHI) < 15/h and had snoring time ≥ 10% of total sleep time. Changes in duration of snoring time were also examined in adult patients after treatment with an oral appliance (OA).

Results

Snoring time was shown to be predominant during N3 and N2 sleep and less dominant during REM sleep in both children (n = 47) and adults (n = 93). These results were seen even in children with REM dependency. The percentage of snoring time during N3 sleep was more pronounced in women than in men among young adult patients aged < 40 years but was not significantly different between men and women overall. There were no significant differences in the percentage of snoring time in each sleep stage between young women with mild OSA and non-OSA. In children, there were no significant differences between boys and girls in the percentage of snoring time in any sleep stage. The percentage of snoring time during N3 was significantly higher sleep in the non-supine position than in the supine position in children, whereas no significant differences were noted between the supine and non-supine positions in any sleep stage in adults. OA treatment for adult patients (n = 20) significantly increased the percentage of snoring time during N3 sleep, although it significantly decreased AHI, total snoring time, and snoring time during N1 sleep and REM sleep.

Conclusions

Snoring presented exclusively during the N3 sleep stage, especially in young women with mild OSA, and in children with OSA, especially in the non-supine position. Snoring time during N3 sleep increased during OA treatment for OSA.

Introduction

Snoring is a respiratory sound originating in the upper airway during sleep that results from vibration of the pharyngeal wall and associated structures, which typically occurs during inspiration but can also occur during expiration [1]. Snoring can be classified into two main patterns: snoring associated with respiratory events, in which snoring occurs during or at the end of respiratory events such as apnea, hypopnea, or respiratory effort-related arousal during sleep; and snoring independent of respiratory events during sleep, referred to as isolated, primary, or simple snoring [2]. It is well known that respiratory events are often more pronounced during stage N2 sleep and rapid eye movement (REM) sleep, and it is speculated that differences exist between the sleep stage in which respiratory events appear and those in which isolated snoring appears. However, few studies have investigated snoring independent of respiratory events. Those studies using polysomnography (PSG) have revealed a higher snoring index during slow wave sleep compared with other sleep stages and a higher snoring index in all sleep stages in men without obstructive sleep apnea (OSA) compared with women without OSA [3] as well as in adult men and women with a mean apnea-hypopnea index (AHI) of 22 ± 15.9/h and 28 ± 17/h, respectively, indicating the inclusion of participants with moderate to severe OSA [4].

Against this background, this study sought to determine at which sleep stage isolated snoring occurs in children and adults, especially those with mild OSA and categorized by age group, and to analyze changes after OA treatment in adult patients.

Methods

This retrospective study comprised two parts. First, we analyzed data on duration of snoring time and respiratory events during each sleep stage from adults (age > 18 years) with AHI ≥ 5/h but < 15/h and children with AHI ≥ 1/h, both with ≥ 10% snoring time of total sleep time (TST). Second, among adult patients whose AHI and percentage of sleep time in N3 sleep showed improvement after treatment with an oral appliance (OA), we analyzed changes in duration of snoring time in TST during each sleep stage.

Polysomnography

All participants underwent standard type 1 in-laboratory overnight PSG (Alice 6; Philips Respironics, Pittsburgh, PA) for diagnosis and for determining OA-set outcome measurements. In brief, electroencephalography (C4/A1, C3/A2), electrooculography, submental surface electromyography, and electrocardiography using surface electrodes were performed. Nasal air flow was measured with pressure and thermistor sensors at the nostrils, and respiratory movements of the rib cage and abdomen were measured by inductive plethysmography. Percutaneous arterial oxygen saturation using finger pulse oximetry was also measured. Body position was measured using a position sensor, with a mercury switch attached to the anterior chest wall on the median line. A microphone was placed on the neck to detect snoring (dB > 20). Snoring events were scored manually, and then the PSG system automatically calculated total duration of snoring time. PSG measurements were scored manually by registered PSG technologists. Percentage of sleep time in TST (%sleep time), percentage of duration of respiratory events, and percentage of snoring time were calculated for each sleep stage. Adult patients with an obstructive AHI score ≥ 5/h but < 15/h were considered to have mild OSA, with an obstructive AHI score < 5/h indicating no OSA [5]. REM sleep dependency was identified when the value of AHI during REM sleep divided by the AHI during non-REM sleep was ≥ 2.

Treatment with an oral appliance

OAs were made of self-cured acrylic resin as described in our previous study [6]. Each OA was custom-made and adjusted individually by a dentist, with the participant instructed on its use. After taking impressions of the maxillary and mandibular dental arches, maxillary and mandibular portions were prepared separately to maintain the mandible in an anteriorly protruding position. If the patient complained of any discomfort in the temporomandibular joints or muscles after using the OA, the mandibular portion was set at a less-protruding position. This adjustment was repeated until the patient could wear the OA continuously without problem before the device-set PSG study was conducted. No OA titrations were performed. Device-set PSGs were basically performed 8 weeks after final device instruction.

Ethical consideration

The ethics committee at our institute approved this study (Approval No. Teirin 19–070) and written informed consent was obtained from all participants. The institutional review board waived the requirement to obtain consent from parents or guardians of minors in this study. Patients consented to the use of their PSG data for the study at the time of their first visit to our outpatient clinic. The PSG examinations and the oral appliance described in this study was implemented as standard-of-care. Patients who declined to take part in the study received the same care as the patients who agreed to take part in the study. Data were collected from 2018 to 2022. The authors conducted this study in December 2022. The source of data was a sleep center affiliated with a university hospital. The authors did not have access to information that could identify individual participants during or after data collection.

Statistics

Descriptive statistics for all variables are presented as the mean ± standard deviation. Paired and unpaired comparisons were evaluated by the Wilcoxon signed rank test and Mann–Whitney U test, respectively. Changes in values among three sleep parameters were evaluated by one-way analysis of variance. Bonferroni correction was applied for multiple comparisons (post hoc tests). Statistical significance was set at p < 0.05. All statistical analyses were performed using the IBM Statistical Package for Social Science (ver. 26; IBM Inc., Armonk, NY).

Results

In the first part of this study, we analyzed data from 93 adults with mild OSA (mean age, 38.7 ± 14.3 years; mean AHI, 10.2 ± 3.1/h; mean body mass index [BMI], 23.3 ± 3.9 kg/m2) and 47 children with OSA (mean age: 7.5 ± 2.5, range 3–12; mean AHI: 5.0 ± 4.0/h). In the adult patients with mild OSA (Fig 1a), %sleep time was 13.6% ± 5.7% during N1 sleep, 59.2% ± 6.8% during N2, 8.4% ± 6.4% during N3, and 18.6% ± 6.0% during REM sleep, and percentage of respiratory events was 25.3% ± 15.3% during N1 sleep, 37.6% ± 16.5% during N2, 1.7% ± 4.7% during N3, and 35.4% ± 21.1% during REM sleep. Percentage of snoring time in TST was 7.5% ± 6.0 during N1 sleep, 68.2% ± 15.2 during N2, 12.9% ± 13.2 during N3, and 11.4% ± 9.5 during REM sleep. There were significant differences among the three parameters in every stage. In children with OSA (Fig 1b), %sleep time was 6.2% ± 3.2% during N1 sleep, 36.1% ± 11.3% during N2, 40.4% ± 13.7% during N3, and 17.3% ± 5.3% during REM sleep, and percentage of respiratory events was 23.9% ± 19.3 during N1 sleep, 32.4% ± 23.4% during N2, 10.3% ± 13.3% during N3, and 29.2% ± 23.0% during REM sleep. Percentage of snoring time in TST was distributed 7.9% ± 5.5 during N1, 34.3% ± 17.1 during N2, 44.2% ± 21.9 during N3, and 13.65 ± 12.4 during REM sleep. In ad hoc analyses, we found no significant difference between %sleep time and percentage of snoring time in any sleep stage, whereas there were significant differences between these two parameters and percentage of respiratory events in N1, N3, and REM sleep.

Fig 1. Distribution of percentage of sleep time, respiratory events, and snoring time in each sleep stage in (a) adults with mild OSA (n = 93) and (b) children with OSA (age 3–12 years, n = 47).

Fig 1

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Black short-dashed line: percentage of sleep time. Blue long-dashed line: percentage of respiratory events. Red solid line: percentage of snoring time. *Significant difference between the three parameters. †Significant differences between percentage of respiratory events and the other two parameters. N.S.: not significant.

In a comparison between all men (n = 34; mean AHI: 10.7/h ± 2.6; mean age: 34.3 ± 10.4; mean BMI: 24.3 kg/m2 ± 3.2) and all women (n = 59; mean AHI: 9.8/h ± 3.4; age: 41.2 ± 15.6; BMI: 22.4 kg/m2 ± 4.3), we found no significant differences in AHI (p = 0.88) or age (p = 0.08) but significant differences in BMI (p = 0.001). We also found no significant difference in percentage of snoring time in any sleep stage between them (Fig 2a). However, among adult patients aged < 40 years, percentage of snoring time was significantly higher in women (n = 33) than in men (n = 29) during stage N3 sleep (p = 0.03), whereas we found no significant differences in percentage of respiratory events (Fig 3). In addition, we compared the percentage of snoring time between women aged < 40 years with mild OSA and non-OSA (n = 15, mean age: 31.7 ± 9.6, mean AHI: 2.4/h ± 1.4, mean BMI 24.5 kg/m2 ± 4.5). There were no significant differences in the percentage of snoring time in any sleep stage. In children, we found no significant differences in AHI (p = 0.15) or age (p = 0.45) between boys (n = 30; mean AHI, 4.3 ± 3.8/h; mean age, 7.8 ± 2.7 years) and girls (n = 17; mean AHI, 6.1 ± 4.2/h; mean age, 7.2 ± 2.5 years) and no significant difference in percentage of snoring time in any sleep stage (Fig 2b).

Fig 2. Comparison of percentage of snoring time in each sleep stage between (a) men (n = 34) and women (n = 59) with mild OSA and (b) between boys (n = 30) and girls (n = 17) with OSA.

Fig 2

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Blue dashed line: men or boys: Red solid line: women or girls. N.S.: not significant.

Fig 3. Comparison of percentage of (a) snoring time and (b) respiratory events in each sleep stage between young men (n = 29) and young women (n = 33) aged < 40 years with mild OSA.

Fig 3

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Blue dashed line: men. Red solid line: women. N.S.: not significant. *Significant difference.

We compared the percentage of snoring time between the supine and non-supine (i.e., left and right lateral, and prone) positions. In adult patients (n = 93), there were no significant differences in the percentage of snoring time between the supine and non-supine positions in any sleep stage (Fig 4a). However, in children (n = 47), the percentage of snoring time in the non-supine position was significantly higher during N3 sleep (p = 0.046) and significantly lower during N1 sleep (p = 0.043) compared with the supine position (Fig 4b). A similar tendency was also seen in adult women aged < 40 years (n = 33) but the difference was not significant (no figure).

Fig 4. Comparison of percentage of snoring time in each sleep stage between the supine and non-supine positions in (a) adults with mild OSA (n = 93) and (b) children with OSA (n = 47).

Fig 4

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Blue dashed line: supine position. Red solid line: non-supine position. N.S.: not significant. *Significant difference.

In a comparison between adult patients with REM sleep dependency (n = 51; mean AHI, 9.8 ± 3.1/h; age, 40.4 ± 13.9 years; BMI, 23.6 ± 4.1 kg/m2) and those without (n = 42; mean AHI, 10.6 ± 3.1/h; age, 36.6 ± 14.7 years; BMI, 23.0 ± 3.7 kg/m2), we found no significant difference in AHI (p = 0.26), age (p = 0.09), or BMI (p = 0.55). Percentage of snoring time in adult patients with REM sleep dependency was significantly higher during REM sleep (p = 0.01) and lower during N1 sleep (p = 0.01) than in adult patients without REM sleep dependency (Fig 5a), although these percentages were much lower than for respiratory events during each sleep stage. When we compared children with REM sleep dependency (n = 20; mean AHI, 4.6 ± 4.0/h; mean age, 7.7 ± 2.7 years) and those without (n = 27; mean AHI, 5.2 ± 4.1/h; mean age, 7.2 ± 2.3 years), we also found no significant differences in AHI (p = 0.9) or age (p = 0.45), but also found no significant difference in percentage of snoring time in any sleep stage between the two groups (Fig 5b).

Fig 5. Comparison of percentage of snoring time in each sleep stage (a) between adult patients with (n = 51) and without REM-dependency (n = 42) and (b) between children with (n = 20) and without REM-dependency (n = 27).

Fig 5

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REM-dependency: REM AHI/non-REM AHI ≥ 2. Green dashed line: patients with REM-dependency. Pink solid line: patients without REM-dependency.

In the second part of this study, we examined the effects of OA treatment on snoring in 20 adult patients (mean age, 47.9 ± 13.6 years; mean AHI, 16.2 ± 4.9/h; mean BMI, 24.9 ± 4.7 kg/m2). OA treatment significantly decreased AHI from 16.2 ± 4.9/h to 10.1 ± 4.9/h (p < 0.001) and increased the percentage of N3 sleep in TST from 4.4% ± 4.9% to 9.0% ± 4.6% (p < 0.001). When we compared snoring time in TST between before and after OA treatment, there was a significant increase in percentage of snoring time during N3 sleep (p = 0.028) and significant decreases in total snoring time (from 41.8% ± 14.1% to 30.3% ± 18.8%, p = 0.05) and in snoring time during N1 (p = 0.002) and REM (p = 0.007) during OA treatment (Fig 6).

Fig 6. Comparison of percentage of snoring time in total sleep time (TST) in each sleep stage before and after oral appliance (OA) treatment.

Fig 6

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Blue dashed line: patients before OA treatment. Red solid line: patients after OA treatment.

Discussion

This study obtained several novel findings. First, snoring time was shown to be predominant during N3 and N2 sleep and less dominant during REM sleep in adult patients with mild OSA and children with OSA. This tendency was seen even in children with REM dependency. Second, percentage of snoring time during N3 sleep was more pronounced in women than in men among adult patients aged < 40 years with mild OSA, while there were no significant differences between men and women overall. There were no significant differences in the percentage of snoring time in any sleep stage between young women with mild OSA and non-OSA. Third, the percentage of snoring time during N3 sleep was significantly higher in the non-supine position than in the supine position in children. Fourth, in adult patients whose AHI and percentage of N3 sleep stage were improved with OA treatment, snoring time during N3 sleep increased significantly during OA treatment, but total snoring time and snoring time during N1 and REM sleep were significantly improved. To our knowledge, this study is the first to use PSG to analyze the stage of sleep at which isolated snoring occurs in adult patients with mild OSA by age group, and in children with OSA, and to analyze changes after OA treatment for OSA.

Do respiratory events always develop from snoring events?

Snoring is considered a prelude to a respiratory event during sleep. Respiratory arousals that accompany respiratory events shift deep sleep to shallow sleep, whereas snoring events without arousals do not alter sleep stage. It can be assumed that deep sleep can occur only when there are few or no respiratory events. Thus, snoring presents predominantly during deep sleep while respiratory events present during shallow sleep. Snoring events are thought to develop into respiratory events during non-REM sleep. In contrast, in this study, snoring was found to be less dominant and respiratory events predominant during REM sleep. REM sleep diminishes genioglossus activity secondary to the cholinergic mediated inhibition of hypoglossal motor output; therefore, REM sleep is simply a period of increased vulnerability of the upper airway [7]. In addition, thoracic respiration is reduced and abdominal respiration via the phrenic nerve becomes dominant during REM sleep. On the other hand, consolidation of recognition memory and modulation of emotional reactivity are most crucial during REM sleep. During REM sleep, strong reactivation of brain areas implicated in daytime memory function and overnight reprocessing of emotional memories would be supported [8]. As protection of the brain might be most important during REM sleep, breathing that becomes unstable in REM sleep shifts to a respiratory event without going through snoring.

Collapsibility of the pharyngeal wall may be highest during REM sleep, followed by N1, N2, and N3 sleep. Snoring may require some degree of pharyngeal wall retention; thus, although snoring is likely to occur during N3 sleep, respiratory events are not. The hypothesis that a snoring event develops into a hypopnea/apnea event could be true during non-REM sleep but not always true during REM sleep.

Sex differences in snoring during non-REM sleep

This study revealed that snoring during slow wave sleep was more pronounced in women than in men among younger adults aged < 40 years with mild OSA. Upper airway collapsibility, which is determined by measuring critical closing pressure (i.e., positive or negative pressure accompanying airway collapse), is reported to be greater in men than in women after controlling for BMI, age, and apnea severity [9]. Likewise, healthy men have exhibited a significantly higher increase in pharyngeal resistance in response to inspiratory loading during non-REM sleep compared to women despite a similar ventilatory response to the load [10]. In addition, central chemoreflex sensitivity is greater in males than in females, indicating that ventilator response to carbon dioxide and hypoxemia is increased in men compared to women [11]. The effect of estrogen and/or progesterone on the chemical control of breathing might play a role in the prevalence of sleep-disordered breathing [11]. These sex differences could account for the lower incidence of respiratory events and higher incidence of isolated snoring during N3 sleep in women compared to men. Isolated snoring without arousal usually does not shift deep sleep to shallow sleep as mentioned above. The reduced airway resistance in women due to increased tonicity of upper airway muscles is positively correlated with progesterone levels. This might partially explain the differences between younger and older females [12].

Can patients always decrease snoring by sleeping in a non-supine position?

Positional dependency is a common phenotype. It is reported that the supine position impairs sleep quality primarily through increased respiratory events and sleep fragmentation [13]. The primary pathophysiology of positional dependence is regarded as an anatomical issue [14]. Differences in the distribution of soft tissue surrounding the pharyngeal airway suggest that tissue pressure might vary axially depending on the direction of gravity relative to the patient’s position [14]. One study reported that body posture significantly influenced the pharyngeal critical closing pressure, with mean values of 0.3 ± 0.5 cm H2O for lateral body posture and 2.5 ± 0.5 cm H2O for supine body posture, which accounts for less pharyngeal collapsibility in the lateral position compared with the supine position [15]. Pharyngeal airway patency in children also has been reported to improve in the non-supine position compared with the supine position [16]. Respiratory events would be more likely to occur when the pharyngeal wall is vulnerable to collapse; however, snoring might be more likely to occur when retention of the pharyngeal wall is somewhat sustained. Our results suggested that retention of the pharyngeal wall during N3 is more sustained in the non-supine position compared with the supine position, especially in children. A lateral position would decrease respiratory events but might increase snoring during N3 sleep, and thus the hypothesis that patients can decrease snoring by sleeping in a non-supine position may not always be true during N3 sleep, especially in children.

Is residual snoring during treatment caused only by lack of pharyngeal patency?

Experimental studies have shown that the pharyngeal critical closing pressure progressively increases from negative levels to positive levels as the severity of OSA increases, indicating the mechanism underlying residual snoring after treatment is due to lack of pharyngeal opening [17]. However, our results suggest that changes in N3 sleep reflect residual snoring during OA treatment. Residual snoring during or after treatment can be affected not only by lack of pharyngeal opening but also by changes in sleep stages. Therefore, one reason CPAP users snore during treatment is insufficient pressure, but another reason could be increased deep sleep.

Study limitations

In this study, we analyzed only duration of snoring time and not sound pressure level as measured in decibels. In research using advanced technology, sound pressure can be measured with high quality visual resolution [18]. In addition, sound analysis of snoring has recently been expanded by applying machine learning methods to PSG measurements [19], while electrophysiological signal recordings with PSG revealed the effects of snoring sounds on electroencephalography and electrocardiography signals [20]. Sensory and digital devices developed with computer-based learning methods have made it possible to diagnose and treat snoring and OSA [21]. Analyses using these advanced technologies might highlight additional aspects of snoring.

Second, the relationship between snoring and complications such as hypertension has not been evaluated. Several previous researchers have shown an independent association between snoring sound intensity and daytime blood pressure in patients with OSA and even in those without OSA [22–25]. Besides snoring associated with respiratory events, exposure to vibratory stimuli caused by isolated snoring can damage the endothelial cells in arterial walls, which may trigger an inflammatory cascade leading to carotid atherosclerosis [26–28].

In conclusion, snoring time was predominant during the N3 and N2 sleep stage, especially in children with OSA and in young women aged < 40 years with mild OSA. Snoring time during N3 sleep increased during OA treatment in adult patients when OA treatment improved their AHI and percentage of N3 sleep. The hypothesis that a hypopnea/apnea event develops from a snoring event could be true during non-REM sleep but not always during REM sleep. The hypothesis that patients can decrease snoring by sleeping in a non-supine position may not always be true during N3 sleep, especially in children. Residual snoring during or after treatment could be affected not only by lack of pharyngeal opening but also by changes in sleep stages.

Supporting information

S1 Data

(XLS)

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S1 Checklist. STROBE statement—Checklist of items that should be included in reports of observational studies.

(DOCX)

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Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

This was not an industry-supported study. All authors have indicated no financial conflicts of interest. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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  • 26.Lee SA, Amis TC, Byth K, Larcos G, Kairaitis K, Robinson TD, et al. Heavy snoring as a cause of carotid artery atherosclerosis. Sleep. 2008;31:1207–1213. doi: 10.5665/sleep/31.9.1207 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Kim J, Pack AI, Riegel BJ, Chirinos JA, Hanlon A, Lee SK, et al. Objective snoring time and carotid intima-media thickness in nonapneic female snorers. J Sleep Res. 2017;26:147–150. doi: 10.1111/jsr.12471 Epub 2016 Dec 6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Cho JG, Witting PK, Verma M, Wu BJ, Shanu A, Kairaitis K, et al. Tissue vibration induces carotid artery endothelial dysfunction: a mechanism linking snoring and carotid atherosclerosis? Sleep. 2011;34:751–757. doi: 10.5665/SLEEP.1042 [DOI] [PMC free article] [PubMed] [Google Scholar]

Decision Letter 0

Marco Zaffanello

25 May 2023

PONE-D-23-01986During which sleep stages does isolated snoring occur in children and adults?PLOS ONE

Dear Dr. Suzuki,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Please submit your revised manuscript by Jul 09 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

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If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Marco Zaffanello

Academic Editor

PLOS ONE

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When submitting your revision, we need you to address these additional requirements.

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2. You indicated that you had ethical approval for your study. In your Methods section, please ensure you have also stated whether you obtained consent from parents or guardians of the minors included in the study or whether the research ethics committee or IRB specifically waived the need for their consent.

3. In your Data Availability statement, you have not specified where the minimal data set underlying the results described in your manuscript can be found. PLOS defines a study's minimal data set as the underlying data used to reach the conclusions drawn in the manuscript and any additional data required to replicate the reported study findings in their entirety. All PLOS journals require that the minimal data set be made fully available. For more information about our data policy, please see http://journals.plos.org/plosone/s/data-availability.

"Upon re-submitting your revised manuscript, please upload your study’s minimal underlying data set as either Supporting Information files or to a stable, public repository and include the relevant URLs, DOIs, or accession numbers within your revised cover letter. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. Any potentially identifying patient information must be fully anonymized.

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We will update your Data Availability statement to reflect the information you provide in your cover letter.

Additional Editor Comments (if provided):

Dear Authors,

We would like to congratulate you on your research review focusing on snoring and sleep breathing disorders, which has received valuable feedback from the two reviewers. It is evident that your work addresses a common and significant issue that disrupts sleep health worldwide.

Reviewer 1 has suggested two specific improvements. Reviewer 2, who acknowledges the importance of your manuscript's findings. The decision is Major Revision

Considering the reviewers' expert opinions and constructive suggestions will greatly contribute to the overall quality and impact of your articles. We encourage you to carefully incorporate these revisions, ensuring that the revised manuscript effectively addresses the reviewers' feedback. We appreciate your dedication to advancing the field and look forward to reviewing the revised version of your work.

Best regards

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Partly

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: COMMENTS

Among the events that disrupt sleep health in the world, snoring and sleep breathing disorders are common and well known. I find the research review necessary and important. My suggestions and comments to the authors explaining the "relationship between snoring and sleep stages" in adults and children in their articles are as follows:

Comment 1: Presenting the "percentage of snoring time in TST" values in a table makes it easy to see each value (for the Results section).

Comment 2: For the discussion section, innovative diagnosis and treatments should be presented, apart from the classical treatment of snoring Treatment with an oral appliance. Recently, snoring sound analyzes have been performed meticulously and successfully with machine learning methods applied to polysomnographic measurements (1). In this way, the effects of snoring sound on brain waves (ElectroEncephaloGram, EEG (2), respiration and heart (ElectroCardioGram)) are revealed by examining electrophysiological signal recordings in PSG. Again, by developing sensory and digital devices with computer-based learning methods, diagnosis and treatment of snoring and sleep breathing disorders is done (3).

1. M. Kayabekir, M. Yağanoğlu, C. Köse (2022). SNOROSALAB: A Method Facilitating the Diagnosis of Sleep Breathing Disorders Before Polysomnography, IRBM, Volume 43, Issue 4,

Pages 259-271, ISSN 1959-0318, https://doi.org/10.1016/j.irbm.2021.08.002.

(https://www.sciencedirect.com/science/article/pii/S1959031821000993)

2. Kayabekir, M., & Yağanoğlu, M. (2022). The relationship between snoring sounds and EEG signals on polysomnography. Sleep & breathing = Schlaf & Atmung, 26(3), 1219–1226. https://doi.org/10.1007/s11325-021-02516-8

3. Yağanoğlu, M., Kayabekir, M., & Köse, C. (2017). SNORAP: A Device for the Correction of Impaired Sleep Health by Using Tactile Stimulation for Individuals with Mild and Moderate Sleep Disordered Breathing. Sensors (Basel, Switzerland), 17(9), 2006. https://doi.org/10.3390/s17092006

Comment 3: For the study limitations section: The position of the snorer during sleep in NREM and REM sleep processes is very important in terms of reducing and treating snoring. Correct position of the person during sleep in bed (left or right side, less on his back); It improves NREM and REM sleep durations (3, 4). The results of this study do not provide information about the relationship between snoring and its position, especially in snoring women under the age of 40 and children aged 7 years.

4. Kayabekir M. (2018). Int J Respir Pulm Med, 5:096 Volume 5 | Issue 2 DOI: 10.23937/2378-3516/1410096

Reviewer #2: A manuscript with important findings regarding NREM slow-wave sleep impact on OSA. One important key factor in any respiratory event (including snoring) in sleep apnea is body position. This manuscript does not include any information about body position. Adding this information can affect results and conclusions, therefore must be considered. I suggest some references to the manuscript discussion: Body posture as a factor determining sleep quality in patients using non-invasive ventilation https://pubmed.ncbi.nlm.nih.gov/36973594/

Effect of Sleeping Position on Upper Airway Patency in Obstructive Sleep Apnea Is Determined by the Pharyngeal Structure Causing Collapse https://doi.org/10.1093/sleep/34.4.541

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Dr. Murat Kayabekir

Reviewer #2: Yes: Daniel Alfaiate

**********

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2024 Jan 31;19(1):e0295232. doi: 10.1371/journal.pone.0295232.r002

Author response to Decision Letter 0

2 Aug 2023

Reviewer #1:

We would like to thank the reviewer for the latest review and we have answered each of the points below. The paper has been checked by a native English-speaking medical editor. We hope that this more substantial reworking of the manuscript is satisfactory.

Among the events that disrupt sleep health in the world, snoring and sleep breathing disorders are common and well known. I find the research review necessary and important. My suggestions and comments to the authors explaining the "relationship between snoring and sleep stages" in adults and children in their articles are as follows:

Comment 1: Presenting the "percentage of snoring time in TST" values in a table makes it easy to see each value (for the Results section).

Thank you for pointing this out. For clarity, all numbers are presented in numerical form. See figures.

Comment 2: For the discussion section, innovative diagnosis and treatments should be presented, apart from the classical treatment of snoring Treatment with an oral appliance. Recently, snoring sound analyzes have been performed meticulously and successfully with machine learning methods applied to polysomnographic measurements (1). In this way, the effects of snoring sound on brain waves (ElectroEncephaloGram, EEG (2), respiration and heart (ElectroCardioGram)) are revealed by examining electrophysiological signal recordings in PSG. Again, by developing sensory and digital devices with computer-based learning methods, diagnosis and treatment of snoring and sleep breathing disorders is done (3).

Thank you for pointing this out. We have added this limitation with references to the Discussion.

Comment 3: For the study limitations section: The position of the snorer during sleep in NREM and REM sleep processes is very important in terms of reducing and treating snoring. Correct position of the person during sleep in bed (left or right side, less on his back); It improves NREM and REM sleep durations (3, 4). The results of this study do not provide information about the relationship between snoring and its position, especially in snoring women under the age of 40 and children aged 7 years.

Thank you very much for pointing this out. We compared the percentage of snoring time between the supine and non-supine (i.e., left and right lateral, and prone) positions.

In adult patients (n = 93), there were no significant differences in the percentage of snoring time between the supine and non-supine positions in any sleep stage (Fig. 4a). However, in children (n = 47), the percentage of snoring time in the non-supine position was significantly higher during N3 sleep (p = 0.046) and significantly lower during N1 sleep (p = 0.043) compared with the supine position (Fig. 4b). A similar tendency was also seen in adult women aged < 40 years (n = 33) but the difference was not significant.

We have added these findings to the Results section and figures, and we have revised the discussion accordingly.

Reviewer #2:

We would like to thank the reviewer for the latest review and we have answered each of the points below. The paper has been checked by a native English-speaking medical editor. We hope that this more substantial reworking of the manuscript is satisfactory.

A manuscript with important findings regarding NREM slow-wave sleep impact on OSA. One important key factor in any respiratory event (including snoring) in sleep apnea is body position. This manuscript does not include any information about body position. Adding this information can affect results and conclusions, therefore must be considered.

Thank you very much for pointing this out. We compared the percentage of snoring time between the supine and non-supine (i.e., left and right lateral, and prone) positions.

In adult patients (n = 93), there were no significant differences in the percentage of snoring time between the supine and non-supine positions in any sleep stage (Fig. 4a). However, in children (n = 47), the percentage of snoring time in the non-supine position was significantly higher during N3 sleep (p = 0.046) and significantly lower during N1 sleep (p = 0.043) compared with the supine position (Fig. 4b). A similar tendency was also seen in adult women aged < 40 years (n = 33) but the difference was not significant.

We have added these findings to the Results section and figures, and we have revised the discussion accordingly.

Attachment

Submitted filename: Response to Reviewers PLOS ONE.docx

Click here for additional data file. (17.2KB, docx)

Decision Letter 1

Marco Zaffanello

8 Nov 2023

PONE-D-23-01986R1During which sleep stages does isolated snoring occur in children and adults?PLOS ONE

Dear Dr. Suzuki,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Please submit your revised manuscript by Dec 23 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

  • A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.

  • An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Marco Zaffanello

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments (if provided):

This study appears to address several issues related to snoring, sleep stages, and obstructive sleep apnea (OSA).

The study's title mentions "isolated snoring," but much of the content focuses on snoring in patients with OSA and during different sleep stages. This discrepancy can confuse readers and may not fully reflect the actual scope of the study. the title could be more accurate and representative. For instance, "Exploring the Dynamics of Snoring in Relation to Sleep Stages and Obstructive Sleep Apnea: Implications for Gender Differences and Upper Airway Collapsibility" might be a more suitable option. However, this is not strictly necessary..

The study highlights that snoring is more predominant during N3 and N2 sleep stages and less present during REM sleep. These findings appear to align with some of the existing knowledge about sleep physiology and snoring. However, the discussion in the first passage and the description of the study results need to be more accurately presented. In the discussion, it is stated that snoring is predominant during deep sleep (N3) and less present during REM sleep, while the study suggests that snoring was less predominant during N3 and N2 sleep stages and more present during REM sleep. However, the discussion seems to contradict these results, creating confusion.

The study identifies significant gender differences in the percentages of snoring time, particularly during N3 sleep. This observation can have important implications for understanding the dynamics of OSA and gender-related sleep disorders.

The analysis of upper airway collapsibility and its relationship with snoring are relevant aspects of the study. The discovery that this collapsibility is greater in men after controlling for factors like BMI, age, and the severity of apnea adds an additional layer of understanding to the cause of snoring in patients with OSA.

The investigation into the effects of oral appliance (OA) treatment on snoring is intriguing. The significant reduction in the apnea-hypopnea index (AHI) and changes in sleep stages after treatment indicate that OA may be effective in improving sleep-related breathing disorders.

In summary, the study provides valuable insights into the relationship between snoring, sleep stages, and OSA, despite some discrepancies between the title and the content. However, for greater clarity, it would be helpful to improve the consistency between the discussion and the reported results, as well as to consider a title more suited to the actual scope of the research.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #2: The authors have adequately addressed comments raised in a previous round of review therefore this manuscript is now acceptable for publication

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #2: Yes: Daniel Alfaiate

**********

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2024 Jan 31;19(1):e0295232. doi: 10.1371/journal.pone.0295232.r004

Author response to Decision Letter 1

15 Nov 2023

We would like to thank the reviewer for the latest review and we have answered each of the points below. We review the reference list to ensure that it is complete and correct. We hope that this more substantial reworking of the manuscript is satisfactory.

Additional Editor Comments

This study appears to address several issues related to snoring, sleep stages, and obstructive sleep apnea (OSA).

The study's title mentions "isolated snoring," but much of the content focuses on snoring in patients with OSA and during different sleep stages. This discrepancy can confuse readers and may not fully reflect the actual scope of the study. the title could be more accurate and representative. For instance, "Exploring the Dynamics of Snoring in Relation to Sleep Stages and Obstructive Sleep Apnea: Implications for Gender Differences and Upper Airway Collapsibility" might be a more suitable option. However, this is not strictly necessary..

Thank you for your wonderful suggestion. We agree and have changed the title to “Exploring the Dynamics of Snoring in Relation to Sleep Stages: Implications for Gender Differences, Sleep Position, and Upper Airway Collapsibility”. Since we analyzed the percentage of snoring time of non-OSA women, we do not want to include the word "OSA" in the title.

The study highlights that snoring is more predominant during N3 and N2 sleep stages and less present during REM sleep. These findings appear to align with some of the existing knowledge about sleep physiology and snoring. However, the discussion in the first passage and the description of the study results need to be more accurately presented. In the discussion, it is stated that snoring is predominant during deep sleep (N3) and less present during REM sleep, while the study suggests that snoring(respiratory events?) was less predominant during N3 and N2 sleep stages and more present during REM sleep. However, the discussion seems to contradict these results, creating confusion.

Thank you for pointing this out. Words and sentences were deleted and added to maintain consistency in the Discussion section.

Attachment

Submitted filename: renamed_359ed.docx

Click here for additional data file. (15.6KB, docx)

Decision Letter 2

Marco Zaffanello

20 Nov 2023

Exploring the Dynamics of Snoring in Relation to Sleep Stages: Implications for Gender Differences, Sleep Position, and Upper Airway Collapsibility.

PONE-D-23-01986R2

Dear Dr. Suzuki,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

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Kind regards,

Marco Zaffanello

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

All comments have been addressed

Reviewers' comments:

Acceptance letter

Marco Zaffanello

8 Jan 2024

PONE-D-23-01986R2

PLOS ONE

Dear Dr. Suzuki,

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team.

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PLOS ONE Editorial Office Staff

on behalf of

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Academic Editor

PLOS ONE

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