|
 
 |
| ORIGINAL ARTICLE |
|
| Year : 2021 | Volume
: 5
| Issue : 3 | Page : 48-52 |
|
Mouth breathing during sleep and persistence of OSA after adeno-tonsillectomy in non-obese children
Brigitte Kim-yook Fung1, Mei-yee Lau2, Shuk-yu Leung2, Rebecca Suk-yin Wong1, Ka-li Kwok2, Daniel Kwok-keung Ng3
1 Physiotherapy Department, Kwong Wah Hospital, Hong Kong SAR, China
2 Department of Paediatrics and Adolescent Medicine, Kwong Wah Hospital, Hong Kong SAR, China
3 Department of Paediatrics and Adolescent Medicine, Kwong Wah Hospital, Hong Kong SAR, China; Department of Paediatrics, Hong Kong Sanatorium & Hospital, Hong Kong SAR, China
| Date of Submission | 13-Sep-2021 |
| Date of Decision | 20-Apr-2022 |
| Date of Acceptance | 08-May-2022 |
| Date of Web Publication | 01-Aug-2022 |
Correspondence Address:
Brigitte Kim-yook Fung
Department of Physiotherapy, Kwong Wah Hospital, 25 Waterloo Road, Hong Kong SAR
China
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/prcm.prcm_17_21
Objective: To evaluate the relationship between the percentage of total sleep time with mouth breathing (SMBP) and post-adeno-tonsillectomy apnea-hypopnea index (AHI) in non-obese children. Materials and Methods: Non-obese obstructive sleep apnea (OSA) children with pre- and post- TandA PSG done between August 2011 and February 2019 were reviewed and mouth breathing during sleep was manually scored. Percentage of total sleep time with mouth breathing (SMBP) was calculated. Its correlation with post-operative AHI >1.5/h was studied. Results: Fifty-nine children were included in the analysis and 47 of the study group (79.7%) were male. The mean age at pre-operative PSG was 9.2+/-3.1 years. The mean AHI dropped from 8.3+/-19.8 to 4.1+/-11.6 (P < 0.001). Thirty-one (50.8%) were cured of OSA defined as AHI<=1.5/h. There was a statistically significant positive correlation between post-operative log-transformed AHI and log-transformed SMBP (r=0.265, P = 0.044). The optimal SMBP for detecting residual OSA was 10.5%. The sensitivity, specificity, positive predictive value, negative predictive value and Youden Index were 0.86, 0.37, 0.57, 0.73 and 0.23, respectively. Post-operative children with SMBP >10.5% had higher risk for residual OSA (OR 4.2, 95%CI: 1.2–15.0, P = 0.029). Conclusion: Obstructive sleep apnea children with mouth breathing for more than 10.5% of total sleep time are more likely to have residual OSA after TandA. Keywords: Adenoidectomy, child, mouth breathing, obstructive sleep apnea, tonsillectomy
How to cite this article:
Fung BK, Lau My, Leung Sy, Wong RS, Kwok Kl, Ng DK. Mouth breathing during sleep and persistence of OSA after adeno-tonsillectomy in non-obese children. Pediatr Respirol Crit Care Med 2021;5:48-52 |
How to cite this URL:
Fung BK, Lau My, Leung Sy, Wong RS, Kwok Kl, Ng DK. Mouth breathing during sleep and persistence of OSA after adeno-tonsillectomy in non-obese children. Pediatr Respirol Crit Care Med [serial online] 2021 [cited 2023 Apr 1];5:48-52. Available from: https://www.prccm.org/text.asp?2021/5/3/48/353122 |
| Introduction | |  |
Mouth breathing (MB) is a respiratory dysfunction with prevalence ranging from 12–55% in children[1],[2],[3],[4] and it is often the consequence of increased nasal resistance usually due to allergic rhinitis and/or adeno-tonsillar hyperplasia.[5] Healthy subjects usually breathe through the nose and spend an average of 96% of total sleep time (TST) with nasal breathing.[6] Increase in MB is associated with a backward and downward displacement of the mandible and tongue leading to an increased tendency of upper airway collapse during sleep, i.e. obstructive sleep apnea (OSA).[7] Tonsillectomy and adenoidectomy (TandA) improves obstructive sleep apnea syndrome (OSAS) but does not completely eliminate it.[8],[9] Persistent MB might be one of the reasons for the persistence of OSA after TandA. Furthermore, persistent MB pattern would have an abnormal impact on the upper airway growth and the neuromuscular responsiveness to inspiration, an essential feature to prevent collapse of the pharynx during inspiration..[10] To date, the report of MB was based on questionnaire, otorhinolaryngological examination or polysomnography (PSG).[1],[2],[3],[4],[11] Three studies were published in evaluating the normal values of MB during sleep. The largest study done involved 90 children and the upper limit of normal was suggested to be 15% of TST.[6] Another study of 10 children suggested the upper limit of normal to be 35% of TST.[12] A study of 10 normal adults found MB occurred in 4% of TST.[13] The purpose of this study was to evaluate the relationship between MB during sleep and post TandA apnea -hypopnea index (AHI).
| Materials and Methods | | |
Subject selection
This was a retrospective study of a group of non-obese children (body mass index, BMI-z score <1.645) who had TandA. Children were included if they had pre-operative and post-operative PSG conducted between August 2011 and February 2019 in the sleep laboratory. Exclusion criteria included children with (1) pre-operative PSG AHI<1.5/h; (2) older than 18 years of age at the time of first PSG; (3) children who previously had a TandA before the study period; (4) significant medical illnesses like cardiac, respiratory or renal insufficient or dysmorphic syndrome; (5) poor quality of PSG, e.g. inadequate sleep duration, poor signals making reading impossible. This study was approved by the research ethics committee of the Kowloon Central/Kowloon East Clusters of the Hospital Authority in Hong Kong (KC/KE-18–0151/ER-4).
Polysomnography
PSG were performed by qualified sleep technologists in the Paediatric Sleep Laboratory in Kwong Wah Hospital in Hong Kong. Standardized PSG was recorded with electroencephalogram (C3-A2,C4-A1, O1-A2, O2-A1, F3-A2, F4-A1), right and left electro-oculogram (EOG), chin submental electromyogram, electrocardiograhy (ECG), nasal flow through a nasal pressure transducer to detect nasal breathing, pulse oximetry (SpO2), oximeter plethysmography waveform, thoracic and abdominal respiratory inductance belt, digital synchronized infrared video and sound monitoring, and transcutaneous carbon dioxide pressure (TCM 4, Radiometer, Copenhagen, Denmark), position sensor, snoring microphone, anterior tibialis electromyogram, intercostal respiratory electromyogram and diaphragmatic respiratory electromyogram. The recording was carried out using a digital polysomnography system (Profusion Sleep 3, Compumedics, Australia). For detection of MB, oral thermistor (Protech, WA, USA) was used afterward.
Apnea and hypopnea were scored according to AASM.[14] In the current study, MB was defined as an increase by >=50% of amplitude from baseline as obtained by the oral thermal sensor associated with thoracic-abdominal movement and the presence of flow limitation in nasal cannula lasting more than 2 consecutive breaths during sleep. During bio-calibration, patient was instructed to close the mouth and breathe through the nose and the baseline signal from the oral thermal sensor was adjusted to zero. This has helped to minimize the artifact in MB signal created by nasal breathing. The duration of MB was scored manually and the time of MB was reported as percentage of time during sleep spent in mouth breathing (SMBP).[6] In the current study, we used AHI >1.5/h to define OSA..[15],[16],[17]
Sleep questionnaire
Data of the Chinese version of modified Epworth Sleepiness Scale (mESS),[18] OSAS quality of life survey (OSA-18) score,[19] and Sleep-Related Breathing Disorder (SRBD) scale of the Paediatric Sleep Questionnaire (PSQ)[20] during pre-operative and post-operative PSG were reviewed. PSQ is a validated tool to assess sleep disorders by Chervin et al.[21] In the current study, the validated Taiwan version of PSQ was used[20] to provide a Chinese version of SRBD.
Statistics
Pre-operative and post-operative demographic data, including age, gender, weight, height, PSG parameters, mESS score, OSA-18 score and SRBD scare were collected. BMI (kg/m2) was calculated and converted into BMI z-score by using normal value published for Hong Kong Chinese children[22] by using the Cole’s LMS method.[23] Non-Obese was defined as the BMI z-score<=1.645 (<=95th percentile). The normality of data was assessed by Shapiro-Wilk test. Continuous variables were presented as the mean+/- standard deviation (SD). Paired t-test was used for comparing continuous variables such as age, weight, height, BMI z-score, PSG parameters, mESS score, OSA-18 score and SRBD score before and after operation. McNemar test was used for comparing paired categorical variable. As some of parameters, i.e. AHI, DI, PaCO2>50mmHg, mouth breathing % of TST and mESS score were skewed, they were transformed by natural log. For the value of zero, the value of 0.1 was added to allow it to be transformed by natural log. Pearson’s correlation coefficient analysis was used for assessing the association between AHI and the percentage of total mouth breathing during sleep time. Youden index (sensitivity +specificity – 1)[24] was used for determining the optimal cut-off value of the percentage of total sleep time spent mouth breathing. A p- value <0.05 was considered statistically significant. All statistical analyses were performed using IBM SPSS Statistics for Windows, Version 22.0 (IBM Corp. in Armonk, NY, USA).
| Results | | |
A total of 66 non-obese children underwent TandA and had pre-operative and post-operative PSG during the studied period. Seven children were excluded because of following reasons: one pre-operative PSG AHI<1.5/h, two with Down syndrome, four without oral thermistor in pre-operative PSG. Therefore, 59 children were included in the analysis with 47 boys (79.7%). The mean age at pre-operative PSG was 9.2+/-3.1 years. The mean age at operation was 10.5 +/- 3.1 years. The mean length of time between TandA and post-operative PSG was 0.9+/-0.6 years. The mean AHI dropped from 8.3+/-19.8 to 4.1+/-11.6 (P < 0.001). Thirty-one (50.8%) children were cured of OSA (AHI<=1.5) after the operation. The mean SpO2 nadir increased from 88.2+/-7.9% to 91.6+/-3.9% (P < 0.001). The mean SMBP dropped from 27.6+/-15.2% to 17.9+/-12.9% (P < 0.001). The mean SRBD scales and mean OSA-18 scores dropped from 8.7+/-4.5 to 4.7+/-3.0 (P < 0.001) and from 59.2+/-20.7 to 48.8+/-14.7 (P = 0.001), respectively. [Table 1] | Table 1: Demographic, anthropometric, PSG parameters and questionnaire data at the time of pre-operative and post-operative PSG, n=59
Click here to view |
After operation, the AHI values had a significant correlation with them SMBP (r=0.265, P = 0.044) [Figure 1]. SMBP >10.5% yielded the best Youden index of 0.23. The sensitivity, specificity, positive predictive value, negative predictive value for the SMBP >10.5% were 0.86, 0.37, 0.57, 0.73 respectively [Table 2]. In the current study, the odds of post-operative children with SMBP >10.5% having residual OSA was 4.2 times that of those withy SMBP <=10.5% of %TST-MB (95%CI: 1.2–15.0, P = 0.029) [Table 3]. | Figure 1: Correlation between post-operative log-transformed AHI and the percentage of total mouth breathing during sleep time
There was a statistically significant positive correlation between post-operative log-transformed AHI and log-transformed total mouth breathing during sleep time, Pearson correlation = 0.265, p = 0.044
Click here to view |
 | Table 2: Receiver operating characteristic (ROC) curve analysis of post-operative percentage of total mouth breathing during sleep time for detecting residual OSA (AHI>1.5/hr)
Click here to view |
 | Table 3: Post-operative percentage of total mouth breathing during sleep time and residual OSA, n=59
Click here to view |
| Discussion | | |
Kim and Guilleminault[12] suggested MB during sleep could be measured by recording obtained from the modified cannula with oral scoop. In Kim and Guilleminault study, the 30 seconds epoch would be defined as MB if more than 50% of the epoch showed oral air flow by using this definition, the cut off point for MB was defined as a minimum of 35% of TST based on that study with 10 children. In another study,[25] it was suggested that the normal “nasal breathing” children had an average of around 4% of TST MB and the maximum duration of MB was 10% asleep in asymptomatic children with normal PSG. Upper limit of normal for MB during sleep was suggested to be 15% of TST.[25] The current study was the first report that demonstrated MB during sleep as a significant risk factor for persistent OSAS after TandA. This corroborated previous study that suggested 15% of TST MB to be abnormal.
The main difference between the current study and the previous two studies were (1) previous studies used a modified cannula with oral scoop[12],[25] and (2) the method of counting MB. The oral scoops are not commonly available whereas the oral thermistor used in the present study was readily available. Method used in counting MB as the exact duration in seconds in the current study was more labor intensive and probably more accurate compared with the method of counting MB as epoch in the previous two studies. This difference probably accounted for the difference in the result.
Cure rate of TandA was 50.8% in the current study and this was similar to the 55% reported in a previous meta-analysis.[8] This center reported in 2010[9] that 45% of 44 children were cured of OSA after TandA. Lee et al[6] also suggested that 26 children out of the 64 children who had the TandA done persisted to have the OSA symptoms and 55% of these patients had the problem of MB.
Chronic MB leads to structural change of the airway as it was identified in a study that the mandible was more retruded in MB children[26] with a greater inclination of the mandibular and occlusal plane than the nasal breathing group. Matheus et al[27] reported that both airway volume, area and minimum axial area were significantly reduced in the MB group. Chronic MB also had high arch palate.[28] MB during growth periods in children led to clockwise rotation of the mandible, with a disproportionate increase in anterior lower vertical face height and decreased posterior facial height,[29] resulting in the adenoid face. Furthermore, MB led to increased surface tension of the fluid lining the pharyngeal mucosa while nasal breathing reduced surface tension.[30] Surface tension is important in the genesis of OSA as reducing surface tension with surfactant in patients with OSA reduced the number of folds in the upper airway,[31] improved upper airway collapsibility and reduced OSA severity.[32]
Treatment of chronic MB would be an important part of management of childhood OSAS and this includes intensive treatment of allergic rhinitis after TandA. Myofunctional therapy was reported to be effective as an adjunct treatment for childhood OSA.[8],[33],[34],[35] Myofunctional therapy comprises of orofacial exercises, breathing re-education and body work.[6] However, all these studies did not demonstrate the direct impact of myofunctional therapy on MB. Further intervention studies are required to assess the impact of myofunctional therapy on MB and the impact of treatment of MB on AHI.
The main limitation of the current paper was the rather small sample size of 59 children who had OSAS. Future study with a larger population looking at the impact of treating mouth breathing on the AHI is warranted.
| Conclusion | | |
Obstructive sleep apnea children with mouth breathing for more than 10.5% of total sleep time are more likely to have residual OSA after TandA.
Contributors’ statements
BK Fung and DK Ng, designed the study, supervised all aspects of the research, supervised analyses, interpreted the results, wrote sections of the initial draft, and reviewed and approved the final version.
M Lau, S Leung, RS Wong and K Kwok conducted and interpreted analyses, wrote sections of the initial draft, and reviewed and approved the final version.
All authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.
Financial support and sponsorship
This work was supported by the Tung Wah Group of Hospitals Research Fund 2018/2019.
Conflicts of interest
The authors have no conflicts of interest to this article to disclose.
| References | | |
| 1. | Abreu RR, Rocha RL, Lamounier JA, Guerra AF. Prevalence of mouth breathing among children. J Pediatr (Rio J) 2008;84:467-70.  |
| 2. | Leal RB, Gomes MC, Granville-Garcia AF, Goes PS, de Menezes VA. Impact of breathing patterns on the quality of life of 9- to 10-year-old schoolchildren. Am J Rhinol Allergy 2016;30:147-52. |
| 3. | Tachibana M, Kato T, Kato-Nishimura K, Matsuzawa S, Mohri I, Taniike M. Associations of sleep bruxism with age, sleep apnea, and daytime problematic behaviors in children. Oral Dis 2016;22:557-65. |
| 4. | Bonuck KA, Chervin RD, Cole TJ, Emond A, Henderson J, Xu L, et al. Prevalence and persistence of sleep disordered breathing symptoms in young children: A 6-year population-based cohort study. Sleep 2011;34:875-84. |
| 5. | Sateia MJ, Thorpy MJ. Classification of sleep disorders; Avidan AY. Non-rapid eye movement parasomnias: Clinical spectrum, diagnostic features, and management. In: Kryger M, Roth T, Dement WC, editors. Principles and Practices of Sleep Medicine. 6th ed. Philadelphia, PA: Elsevier; 2017. p. 618-26;981-92. |
| 6. | Lee SY, Guilleminault C, Chiu HY, Sullivan SS. Mouth breathing, “nasal disuse,” and pediatric sleep-disordered breathing. Sleep Breath 2015;19:1257-64. |
| 7. | Lee SH, Choi JH, Shin C, Lee HM, Kwon SY, Lee SH. How does open-mouth breathing influence upper airway anatomy? Laryngoscope 2007;117:1102-6. |
| 8. | Ng DK, Huang YS, Teoh OH, Preutthipan A, Xu ZF, Sugiyama T, et al. The Asian Paediatric Pulmonology Society (APPS) position statement on childhood obstructive sleep apnea syndrome. Pediatr Respirol Crit Care Med 2017;1:26-38. [Full text] |
| 9. | Ng DK, Wong JC, Chan CH, Leung LC, Leung SY. Ambulatory blood pressure before and after adenotonsillectomy in children with obstructive sleep apnea. Sleep Med 2010;11:721-5. |
| 10. | Guilleminault C, Sullivan SS. Towards restoration of continuous nasal breathing as the ultimate treatment goal in pediatric obstructive sleep apnea. Pediatr Neonatal Biol 2014;1:1-5. |
| 11. | Yi LC, Jardim JR, Inoue DP, Pignatari SS. The relationship between excursion of the diaphragm and curvatures of the spinal column in mouth breathing children. J Pediatr (Rio J) 2008;84:171-7. |
| 12. | Kim JH, Guilleminault C. The nasomaxillary complex, the mandible, and sleep-disordered breathing. Sleep Breath 2011;15:185-93. |
| 13. | Fitzpatrick MF, Driver HS, Chatha N, Voduc N, Girard AM. Partitioning of inhaled ventilation between the nasal and oral routes during sleep in normal subjects. J Appl Physiol (1985) 2003;94:883-90. |
| 14. | Iber C, Ancoli-Israel S, Chesson A, Quan SF. The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications. Westchester, IL: American Academy of Sleep Medicine; 2007. |
| 15. | Uliel S, Tauman R, Greenfeld M, Sivan Y. Normal polysomnographic respiratory values in children and adolescents. Chest 2004;125:872-8. |
| 16. | Traeger N, Schultz B, Pollock AN, Mason T, Marcus CL, Arens R. Polysomnographic values in children 2-9 years old: Additional data and review of the literature. Pediatr Pulmonol 2005;40:22-30. |
| 17. | Witmans MB, Keens TG, Davidson Ward SL, Marcus CL. Obstructive hypopneas in children and adolescents: Normal values. Am J Respir Crit Care Med 2003;168:1540. |
| 18. | Chan EY, Ng DK, Chan CH, Kwok KL, Chow PY, Cheung JM, et al. Modified epworth sleepiness scale in chinese children with obstructive sleep apnea: A retrospective study. Sleep Breath 2009;13:59-63. |
| 19. | Franco RA Jr, Rosenfeld RM, Rao M. First place–resident clinical science award 1999. Quality of life for children with obstructive sleep apnea. Otolaryngol Head Neck Surg 2000;123:9-16. |
| 20. | Huang YS, Wang CH, Guilleminault C. An epidemiologic study of sleep problems among adolescents in north taiwan. Sleep Med 2010;11:1035-42. |
| 21. | Chervin RD, Hedger K, Dillon JE, Pituch KJ. Pediatric sleep questionnaire (Psq): Validity and reliability of scales for sleep-disordered breathing, snoring, sleepiness, and behavioral problems. Sleep Med 2000;1:21-32. |
| 22. | Leung SS, Cole TJ, Tse LY, Lau JT. Body mass index reference curves for chinese children. Ann Hum Biol 1998;25:169-74. |
| 23. | Cole TJ. The Lms method for constructing normalized growth standards. Eur J Clin Nutr 1990;44:45-60. |
| 24. | Youden WJ. Index for rating diagnostic tests. Cancer 1950;3:32-5. |
| 25. | Valera FC, Trawitzki LV, Anselmo-Lima WT. Myofunctional evaluation after surgery for tonsils hypertrophy and its correlation to breathing pattern: A 2-year-follow up. Int J Pediatr Otorhinolaryngol 2006;70:221-5. |
| 26. | Chung Leng Muñoz I, Beltri Orta P. Comparison of cephalometric patterns in mouth breathing and nose breathing children. Int J Pediatr Otorhinolaryngol 2014;78:1167-72. |
| 27. | Alves M Jr, Baratieri C, Nojima LI, Nojima MC, Ruellas AC. Three-dimensional assessment of pharyngeal airway in nasal- and mouth-breathing children. Int J Pediatr Otorhinolaryngol 2011;75:1195-9. |
| 28. | Grippaudo C, Paolantonio EG, Antonini G, Saulle R, La Torre G, Deli R. Association between oral habits, mouth breathing and malocclusion. Acta Otorhinolaryngol Ital 2016;36:386-94. |
| 29. | Harari D, Redlich M, Miri S, Hamud T, Gross M. The effect of mouth breathing versus nasal breathing on dentofacial and craniofacial development in orthodontic patients. Laryngoscope 2010;120:2089-93. |
| 30. | Kirkness JP, Madronio M, Stavrinou R, Wheatley JR, Amis TC. Surface tension of upper airway mucosal lining liquid in obstructive sleep apnea/hypopnea syndrome. Sleep 2005;28:457-63. |
| 31. | Kairaitis K, Foster S, Amatoury J, Verma M, Wheatley JR, Amis TC. Pharyngeal mucosal wall folds in subjects with obstructive sleep apnea. J Appl Physiol (1985) 2015;118:707-15. |
| 32. | Jokic R, Klimaszewski A, Mink J, Fitzpatrick MF. Surface tension forces in sleep apnea: The role of a soft tissue lubricant: A randomized double-blind, placebo-controlled trial. Am J Respir Crit Care Med 1998;157:1522-5. |
| 33. | Guilleminault C, Huang YS. Pediatric obstructive sleep apnea: A short review of clinical aspects. Pediatr Respirol Crit Care Med 2017;1:39-45. [Full text] |
| 34. | Huang YS, Guilleminault C. A review of treatment options in paediatric sleep-disordered breathing. Pediatr Respirol Crit Care Med 2017;1:54-58. [Full text] |
| 35. | Villa MP, Brasili L, Ferretti A, Vitelli O, Rabasco J, Mazzotta AR, et al. Oropharyngeal exercises to reduce symptoms of Osa after At. Sleep Breath 2015;19:281-9. |
[Figure 1]
[Table 1], [Table 2], [Table 3]
|
Search Pubmed for