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Sleep Stage Coordination of Respiration and Swallowing: A Preliminary Study

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Abstract

Swallowing is an important physiological response that protects the airway. Although aspiration during sleep may cause aspiration pneumonia, the mechanisms responsible have not yet been elucidated. We evaluated the coordination between respiration and swallowing by infusing water into the pharynx of healthy young adults during each sleep stage. Seven normal subjects participated in the study. During polysomnography recordings, to elicit a swallow we injected distilled water into the pharynx during the awake state and each sleep stage through a nasal catheter. We assessed swallow latency, swallow apnea time, the respiratory phase during a swallow, the number of swallows, and coughing. A total number of 79 swallows were recorded. The median swallow latency was significantly higher in stage 2 (10.05 s) and stage 3 (44.17 s) when compared to awake state (4.99 s). The swallow latency in stage 3 showed a very wide interquartile range. In two subjects, the result was predominantly prolonged compared to the other subjects. There was no significant difference in the swallow apnea time between sleep stages. The presence of inspiration after swallowing, repetitive swallowing, and coughing after swallowing was more frequent during sleep than when awake. This study suggests that the coordination between respiration and swallowing as a defense mechanism against aspiration was impaired during sleep. Our results supported physiologically the fact that healthy adult individuals aspirate pharyngeal secretions during sleep.

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Abbreviations

EEG:

Electroencephalography

EMG:

Electromyography

EOG:

Electrooculography

PSG:

Polysomnography

REM:

Rapid eye movement

References

  1. Logemann JA. Update on clinical trials in Dysphagia. Dysphagia. 2006;21:116–20.

    Article  PubMed  Google Scholar 

  2. Ashford J, McCabe D, Wheeler-Hegland K, Frymark T, Mullen R, Musson N, Schooling T, Hammond CS. Evidence-based systematic review: oropharyngeal dysphagia behavioral treatments. Part III—Impact of dysphagia treatments on populations with neurological disorders. J Rehabil Res Dev. 2009;46:195–204.

    Article  PubMed  Google Scholar 

  3. Baijens LW, Speyer R. Effects of therapy for dysphagia in Parkinson’s disease: systematic review. Dysphagia. 2009;24:91–102.

    Article  PubMed  Google Scholar 

  4. Marik PE. Aspiration pneumonitis and aspiration pneumonia. N Engl J Med. 2001;344:665–71.

    Article  CAS  PubMed  Google Scholar 

  5. Kikuchi R, Watabe N, Konno T, Mishina N, Sekizawa K, Sasaki H. High incidence of silent aspiration in elderly patients with community-acquired pneumonia. Am J Respir Crit Care Med. 1994;150:251–3.

    Article  CAS  PubMed  Google Scholar 

  6. Gleeson K, Eggli DF, Maxwell SL. Quantitative aspiration during sleep in normal subjects. Chest. 1997;111:1266–72.

    Article  CAS  PubMed  Google Scholar 

  7. Ertekin C. Voluntary versus spontaneous swallowing in man. Dysphagia. 2011;26(2):183–92.

    Article  PubMed  Google Scholar 

  8. Iber C, Ancoli-Israel S, Chesson AL, et al. The AASM manual for the scoring of sleep associated events: rules, terminology and technical specifications. 1st ed. Westchester: American Academy of Sleep Medicine; 2007.

    Google Scholar 

  9. Rechtschaffen A, Kales A. A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. Brain Information Service/Brain Research Institute, University of California; 1968.

  10. Ebihara T, Takahashi H, Ebihara S, Okazaki T, Sasaki T, Watando A, Nemoto M, Sasaki H. Capsaicin troche for swallowing dysfunction in older people. J Am Geriatr Soc. 2005;53(5):824–8.

    Article  PubMed  Google Scholar 

  11. Nishino T, Hiraga K. Coordination of swallowing and respiration in unconscious subjects. J Appl Physiol (1985). 1991;70(3):988–93.

    CAS  Google Scholar 

  12. Nishino T, Takizawa K, Yokokawa N, Hiraga K. Depression of the swallowing reflex during sedation and/or relative analgesia produced by inhalation of 50% nitrous oxide in oxygen. Anesthesiology. 1987;67:995–8.

    Article  CAS  PubMed  Google Scholar 

  13. Gross RD, Atwood CW Jr, Ross SB, Eichhorn KA, Olszewski JW, Doyle PJ. The coordination of breathing and swallowing in Parkinson’s disease. Dysphagia. 2008;23(2):136–45.

    Article  PubMed  Google Scholar 

  14. Kijima M, Isono S, Nishino T. Coordination of swallowing and phases of respiration during added respiratory loads in awake subjects. Am J Respir Crit Care Med. 1999;159(6):1898–902.

    Article  CAS  PubMed  Google Scholar 

  15. Kijima M, Isono S, Nishino T. Modulation of swallowing reflex by lung volume changes. Am J Respir Crit Care Med. 2000;162(5):1855–8.

    Article  CAS  PubMed  Google Scholar 

  16. Yamamoto F, Nishino T. Phasic vagal influence on the rate and timing of reflex swallowing. Am J Respir Crit Care Med. 2002;165(10):1400–3.

    Article  PubMed  Google Scholar 

  17. Hadjikoutis S, Pickersgill TP, Dawson K, Wiles CM. Abnormal patterns of breathing during swallowing in neurological disorders. Brain. 2000;123(Pt 9):1863–73.

    Article  PubMed  Google Scholar 

  18. Nakazawa H, Sekizawa K, Ujiie Y, Sasaki H, Takishima T. Risk of aspiration pneumonia in the elderly. Chest. 1993;103(5):1636–7.

    Article  CAS  PubMed  Google Scholar 

  19. Nakajoh K, Nakagawa T, Sekizawa K, Matsui T, Arai H, Sasaki H. Relation between incidence of pneumonia and protective reflexes in post-stroke patients with oral or tube feeding. J Intern Med. 2000;247(1):39–42.

    Article  CAS  PubMed  Google Scholar 

  20. Eckert DJ, White DP, Jordan AS, Malhotra A, Wellman A. Defining phenotypic causes of obstructive sleep apnea. Identification of novel therapeutic targets. Am J Respir Crit Care Med. 2013;188(8):996–1004.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Sands SA, Eckert DJ, Jordan AS, Edwards BA, Owens RL, Butler JP, Schwab RJ, Loring SH, Malhotra A, White DP, Wellman A. Enhanced upper-airway muscle responsiveness is a distinct feature of overweight/obese individuals without sleep apnea. Am J Respir Crit Care Med. 2014;190(8):930–7.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Martin-Harris B. Clinical implications of respiratory–swallowing interactions. Curr Opin Otolaryngol Head Neck Surg. 2008;16(3):194–9.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Hiss SG, Treole K, Stuart A. Effects of age, gender, bolus volume, and trial on swallowing apnea duration and swallow/respiratory phase relationships of normal adults. Dysphagia. 2001;16(2):128–35.

    Article  CAS  PubMed  Google Scholar 

  24. Martin-Harris B, Brodsky MB, Michel Y, Ford CL, Walters B, Heffner J. Breathing and swallowing dynamics across the adult lifespan. Arch Otolaryngol Head Neck Surg. 2005;131(9):762–70.

    Article  PubMed  Google Scholar 

  25. Martin BJ, Logemann JA, Shaker R, Dodds WJ. Coordination between respiration and swallowing: respiratory phase relationships and temporal integration. J Appl Physiol (1985). 1994;76(2):714–23.

    CAS  Google Scholar 

  26. Butler SG, Postma GN, Fischer E. Effects of viscosity, taste, and bolus volume on swallowing apnea duration of normal adults. Otolaryngol Head Neck Surg. 2004;131(6):860–3.

    Article  PubMed  Google Scholar 

  27. Preiksaitis HG, Mayrand S, Robins K, Diamant NE. Coordination of respiration and swallowing: effect of bolus volume in normal adults. Am J Physiol. 1992;263(3 Pt 2):R624–30.

    CAS  PubMed  Google Scholar 

  28. Klahn MS, Perlman AL. Temporal and durational patterns associating respiration and swallowing. Dysphagia. 1999;14(3):131–8.

    Article  CAS  PubMed  Google Scholar 

  29. Terzi N, Orlikowski D, Aegerter P, Lejaille M, Ruquet M, Zalcman G, Fermanian C, Raphael JC, Lofaso F. Breathing-swallowing interaction in neuromuscular patients: a physiological evaluation. Am J Respir Crit Care Med. 2007;175(3):269–76.

    Article  PubMed  Google Scholar 

  30. Sato K, Nakashima T. Sleep-related deglutition in patients with sleep apnea–hypopnea syndrome. Ann Otol Rhinol Laryngol. 2009;118(1):30–6.

    Article  PubMed  Google Scholar 

  31. Stanchina ML, Abu-Hijleh M, Chaudhry BK, Carlisle CC, Millman RP. The influence of white noise on sleep in subjects exposed to ICU noise. Sleep Med. 2005;6(5):423–8.

    Article  PubMed  Google Scholar 

  32. Saremi M, Grenèche J, Bonnefond A, Rohmer O, Eschenlauer A, Tassi P. Effects of nocturnal railway noise on sleep fragmentation in young and middle-aged subjects as a function of type of train and sound level. Int J Psychophysiol. 2008;70(3):184–91.

    Article  PubMed  Google Scholar 

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Acknowledgments

K.O. is the guarantor of the paper and takes responsibility for the integrity for the work as a whole, from inception to published articles. K.N., E.T., and S.T. contributed to conception and design. J.A.F., N.T.A., and A.A.L. contributed to drafting the manuscript for important intellectual content. F.R.A. contributed to analysis, interpretation, and drafting the manuscript. This work was supported by a Scientific Research Grant (C) (25463239) from the Japan Society for the Promotion of Science (JSPS). We thank Mrs. Mary Wong for her assistance in the statistical analysis and Ms. Samantha Song for her editorial assistance.

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Authors and Affiliations

  1. Department of Oral Health Sciences, Faculty of Dentistry, The University of British Columbia, 2199 Wesbrook Mall, Vancouver, BC, V6T 1Z3, Canada

    Kentaro Okuno, Alan A. Lowe & Fernanda R. Almeida

  2. Division of Functional Oral Neuroscience, Osaka University Graduate School of Dentistry, 1-8, Yamadaoka, Suita-City, Osaka, 565-0871, Japan

    Kentaro Okuno, Kanji Nohara, Etsuko Takai & Takayoshi Sakai

  3. Division of Respiratory Medicine, Department of Medicine, University of British Columbia, 2194 Health Sciences Mall, Vancouver, BC, V6T 1Z3, Canada

    John A. Fleetham & Najib T. Ayas

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  1. Kentaro Okuno
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  2. Kanji Nohara
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  3. Etsuko Takai
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  4. Takayoshi Sakai
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Correspondence to Kentaro Okuno.

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Okuno, K., Nohara, K., Takai, E. et al. Sleep Stage Coordination of Respiration and Swallowing: A Preliminary Study. Dysphagia 31, 579–586 (2016). https://doi.org/10.1007/s00455-016-9719-5

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  • DOI: https://doi.org/10.1007/s00455-016-9719-5

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