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Published in: Dysphagia 4/2016

01-08-2016 | Original Article

Sleep Stage Coordination of Respiration and Swallowing: A Preliminary Study

Authors: Kentaro Okuno, Kanji Nohara, Etsuko Takai, Takayoshi Sakai, John A. Fleetham, Najib T. Ayas, Alan A. Lowe, Fernanda R. Almeida

Published in: Dysphagia | Issue 4/2016

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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.
Literature
2.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
3.
go back to reference Baijens LW, Speyer R. Effects of therapy for dysphagia in Parkinson’s disease: systematic review. Dysphagia. 2009;24:91–102.CrossRefPubMed Baijens LW, Speyer R. Effects of therapy for dysphagia in Parkinson’s disease: systematic review. Dysphagia. 2009;24:91–102.CrossRefPubMed
4.
5.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
6.
go back to reference Gleeson K, Eggli DF, Maxwell SL. Quantitative aspiration during sleep in normal subjects. Chest. 1997;111:1266–72.CrossRefPubMed Gleeson K, Eggli DF, Maxwell SL. Quantitative aspiration during sleep in normal subjects. Chest. 1997;111:1266–72.CrossRefPubMed
7.
8.
go back to reference 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. 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.
9.
go back to reference 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. 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.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
11.
go back to reference Nishino T, Hiraga K. Coordination of swallowing and respiration in unconscious subjects. J Appl Physiol (1985). 1991;70(3):988–93. Nishino T, Hiraga K. Coordination of swallowing and respiration in unconscious subjects. J Appl Physiol (1985). 1991;70(3):988–93.
12.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
13.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
14.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
15.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
16.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
17.
go back to reference Hadjikoutis S, Pickersgill TP, Dawson K, Wiles CM. Abnormal patterns of breathing during swallowing in neurological disorders. Brain. 2000;123(Pt 9):1863–73.CrossRefPubMed Hadjikoutis S, Pickersgill TP, Dawson K, Wiles CM. Abnormal patterns of breathing during swallowing in neurological disorders. Brain. 2000;123(Pt 9):1863–73.CrossRefPubMed
18.
go back to reference Nakazawa H, Sekizawa K, Ujiie Y, Sasaki H, Takishima T. Risk of aspiration pneumonia in the elderly. Chest. 1993;103(5):1636–7.CrossRefPubMed Nakazawa H, Sekizawa K, Ujiie Y, Sasaki H, Takishima T. Risk of aspiration pneumonia in the elderly. Chest. 1993;103(5):1636–7.CrossRefPubMed
19.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
20.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
21.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
23.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
24.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
25.
go back to reference 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. 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.
26.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
27.
go back to reference 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.PubMed 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.PubMed
28.
go back to reference Klahn MS, Perlman AL. Temporal and durational patterns associating respiration and swallowing. Dysphagia. 1999;14(3):131–8.CrossRefPubMed Klahn MS, Perlman AL. Temporal and durational patterns associating respiration and swallowing. Dysphagia. 1999;14(3):131–8.CrossRefPubMed
29.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
30.
go back to reference Sato K, Nakashima T. Sleep-related deglutition in patients with sleep apnea–hypopnea syndrome. Ann Otol Rhinol Laryngol. 2009;118(1):30–6.CrossRefPubMed Sato K, Nakashima T. Sleep-related deglutition in patients with sleep apnea–hypopnea syndrome. Ann Otol Rhinol Laryngol. 2009;118(1):30–6.CrossRefPubMed
31.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
32.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
Metadata
Title
Sleep Stage Coordination of Respiration and Swallowing: A Preliminary Study
Authors
Kentaro Okuno
Kanji Nohara
Etsuko Takai
Takayoshi Sakai
John A. Fleetham
Najib T. Ayas
Alan A. Lowe
Fernanda R. Almeida
Publication date
01-08-2016
Publisher
Springer US
Published in
Dysphagia / Issue 4/2016
Print ISSN: 0179-051X
Electronic ISSN: 1432-0460
DOI
https://doi.org/10.1007/s00455-016-9719-5

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