Chest ACCP Member Benefits
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Guest Access | Sign In via User Name/Password
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (29)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Teramoto, S.
Right arrow Articles by Fukuchi, Y.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Teramoto, S.
Right arrow Articles by Fukuchi, Y.
(Chest. 1999;116:17-21.)
© 1999 American College of Chest Physicians

Impaired Swallowing Reflex in Patients With Obstructive Sleep Apnea Syndrome*

Shinji Teramoto, MD, FCCP; Eiichi Sudo, MD; Takeshi Matsuse, MD; Eijiro Ohga, MD; Takeo Ishii, MD; Yasuyoshi Ouchi, MD and Yoshinosuke Fukuchi, MD, FCCP

* From the Department of Geriatric Medicine (Drs. Teramoto, Sudo, Matsuse, Ohga, Ishii, and Ouchi), Tokyo University Hospital; and the Department of Respiratory Medicine (Dr. Fukuchi), Juntendo University, Tokyo, Japan.

Correspondence to: Shinji Teramoto, MD, FCCP, Department of Geriatric Medicine, Tokyo University Hospital, 7–3-1 Hongo Bunkyo-ku Tokyo, Japan 113-8655; e-mail: shinjit-tky{at}umin.ac.jp


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: The swallowing reflex is well coordinated with breathing patterns in normal humans. However, patients with obstructive sleep apnea syndrome (OSAS) may have a swallowing disorder that reflects the abnormal function of nerves and muscles in the suprapharynx.

Objective: To examine the relationship between the swallowing function and sleep-disordered breathing in patients with OSAS.

Participants: Twenty patients with OSAS with a mean (± SD) age of 53.4 ± 8.9 years old, and 20 age-matched control subjects with a mean age of 51.4 ± 9.1 years old.

Methods: OSAS was diagnosed using the recordings of overnight polysomnography. The swallowing function in the subject was tested using a swallowing provocation test. The swallowing reflex was determined according to the following criteria: latent time (LT), the time following a bolus injection of distilled water at the suprapharynx to the onset of swallowing; inspiratory suppression time (IST), the time from the termination of swallowing to the next onset of inspiration; and threshold volume, the minimum volume of water (range, 0.4 to 2 mL) that could evoke the swallowing response.

Results: Whereas the LT values in patients with OSAS were larger than the LT values in the control subjects, the IST values (which may reflect the switching mechanism from deglutition apnea to breathing) were actually shorter. In addition, a greater bolus volume was necessary to elicit swallowing in patients with OSAS than was necessary in the control subjects.

Conclusion: Patients with OSAS are likely to exhibit an impaired swallowing reflex, probably due to the perturbed neural and muscular function of the upper airways.

Key Words: aspiration • obstructive sleep apnea syndrome • sleep-disordered breathing • sleep study • swallowing reflex


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Because the pharynx is a shared conduit for swallowing and respiration, it is well known that the breathing cycle is well coordinated with the swallowing in humans.1 2 3 4 5 6 The process of inspiration and expiration (the breathing cycle) is very precisely linked with the swallowing reflex via the supralaryngeal nerve. However, the anatomical configuration of the pharynx also allows for the possibility of aspiration of material into the lower airways during bolus passage, particularly in elderly patients with cerebrovascular disorders.7 8 9 10 11 12 13 14 15

The condition and function of the pharynx and upper airways may be affected by nocturnal disturbed breathing and obstructive sleep apnea syndrome (OSAS).16 17 Although the mechanisms of apnea termination in obstructive sleep apnea have not been fully elucidated, mechanoreceptor feedback from the respiratory muscles of the oropharynx have been thought to play an important role in apnea termination.18 19 Nasal continuous positive airway pressure (nCPAP) has been established as the first line of therapy for OSAS; it has been reported, however, that nCPAP exerts an inhibitory influence on the water-induced swallowing reflex.20 In addition, several investigators21 22 23 have reported that gastroesophageal reflux (GER) is increased in patients with OSAS. Taken together, it appears that the swallowing mechanism may be affected by mechanical and/or chemical stimuli, including apnea and positive pressures in the upper airways. Because abnormalities of neural networks in the area of the suprapharynx are implicated in the cause and/or results of obstructive sleep apneas, it is possible that patients with OSAS have an abnormal swallowing reflex due to impaired neural/muscular function at the upper airways. However, the relationship between sleep-disordered breathing and the swallowing reflex has not been extensively studied.

The aim of this study was to examine the relationship between the swallowing function and sleep-disordered breathing in patients with OSAS.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Subjects
Twenty patients with OSAS (15 men and 5 women; mean [± SD] age, 53.5 ± 8.9 years old; range, 35 to 66 years old) and 20 age-matched control subjects (14 men and 6 women; mean age, 51.4 ± 9.1 years old; range, 30 to 68 years old) were studied. OSAS was defined as the presence on polysomnography of > 10 obstructive or mixed apneas/hypopneas per hour of sleep in association with a history of snoring and excessive daytime sleepiness. None of the study participants consumed alcohol on a regular basis, nor did they take hypnotics, sedatives, analgesics, or medications having known effects on ventilation and swallowing.24 In addition, current or ex-smokers were excluded from this study, because the pharyngeal reflexes may be affected by smoking. The demographic and anthropometric data relevant to the study are shown in Table 1 . All study participants gave their informed consent. None of the participants had abnormal spirometric results in a sitting position, nor did they have histories of cardiopulmonary disease or neuromuscular disorders. To use as spirometric indexes, we chose the best of three maximal flow-volume curves using a dry rolling seal spirometer (model DRS-360; Fukuda Sangyo; Chiba, Japan) before the sleep study, with the best being defined as the curve with the highest sum of FVC and FEV1.25 26


View this table:
[in this window]
[in a new window]

  		Table 1. Demographic and Anthropometric Data*

 
Swallowing Provocation Test
Swallowing function was tested using a swallowing provocation test.27 Briefly stated, the swallowing reflex was induced by a bolus injection of 0.4, 0.8, 1.2, 1.6, or 2 mL of distilled water into the suprapharynx through a 5F small nasal catheter (internal diameter, 0.5 mm) at a supine position. Swallowing was identified by submental electromyogram (EMG) activity and by visual observation of the characteristic laryngeal movement. EMG activity was recorded from surface electrodes on the chin. The volume of water that was injected was recorded as a pressure difference by a pressure transducer on a 4-channel chart recorder (Nihon Kohden; Tokyo, Japan). The study participants were unaware of the timing of the actual injection, which took place near the end of expiration. A volume of water was injected within 1 to 2 s in order to keep the velocity of injection similar between trials. The swallowing reflex was determined by the following: (1) the latency of the response (the latent time [LT]), which is the time from injection to the onset of swallowing; (2) the inspiratory suppression time (IST), which is the time from swallowing termination to the next onset of inspiration; and (3) the threshold volume, which is the minimum volume of water that could evoke swallowing. The values for LT, IST, and threshold volume were compared between the patients with OSAS and the control subjects.

Sleep Study
For the polysomnographic study, all subjects were admitted for two or more consecutive nights. Polysomnography consisted of 8 h of overnight monitoring that was done by using a standard technique. Respiratory effort was measured using respiratory inductance plethysmography (Respitrace; Non-Invasive Monitoring Systems; Miami Beach, FL), and airflow at the nose and mouth was measured with thermistors.28 Surface electrodes were applied to obtain an EEG, an electro-oculogram, an ECG, and a record of heart rate. Arterial oxygen saturation (SaO2) was recorded by a pulse oximeter (model 502-P; Criticare Systems; Waukesha, WI). A polygraph was used to record data on a 6-channel chart recorder (Nihon Kohden) and on floppy disk via personal computer (model NEC 9801; NEC; Tokyo, Japan). In study participants who slept for < 6 h as determined by EEG and electro-oculogram, repeat sleep studies were performed to assess whether poor sleep led to a missed diagnosis or an inaccurate estimation of disease severity. Apnea was defined as the cessation of oronasal airflow for > 10 s, and hypopnea was defined as a reduction >= 50% in the oronasal flow in relation to the prevailing value during the preceding normal breathing, with the reduction lasting for at least 10 s. Desaturation was not a criterion for scoring either apnea or hypopnea. In this study, OSAS was determined by calculating the apnea plus hypopnea index (AHI) of > 10 episodes/h. To examine the relationship between the severity of OSAS and the swallowing reflex, we determined the correlation between AHI and variables relating to the swallowing reflex (LT and IST) using a simple regression analysis.

Statistical Analysis
The Mann-Whitney nonparametric test was used to compare the results in patients with OSAS and the control subjects. The relationships between AHI and variables relating to the swallowing reflex were determined by a simple regression analysis. The analyses were performed using appropriate software (StatView 4.0; Abacus Concepts; Berkeley, CA). The data are presented as mean (± SD). A p value < 0.05 was considered to be statistically significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
In the current study, all of the participants in both the OSAS group and the control group were obese: body mass index of 29.1 ± 2.0 vs 28.1 ± 3.3, respectively. Spirometric indexes and arterial blood gas variables were within normal range in all study participants. Anthropometric and pulmonary function data are shown in Table 1 . In the OSAS group, all 20 patients had moderate to severe OSAS (> 10 obstructive or mixed apnea/hypopnea episodes per hour of sleep) and the mean AHI was 20.6 ± 9.4. In the control group, no subjects had more than five apnea/hypopnea episodes per hour (the AHI was less than five), and the mean AHI was 0.9 ± 1.0 (Table 2 ; p < 0.01). Although the baseline value of SaO2 in patients with OSAS was not different from the baseline value in the control subjects, the nadir SaO2 values were considerably lower in patients with OSAS than in control subjects (p < 0.01).


View this table:
[in this window]
[in a new window]

  		Table 2. Summary of Sleep Studies*

 
The swallowing reflex was judged using the LT for swallowing following a bolus injection of a volume of water at the suprapharynx. All acts of swallowing were observed during the transition from expiration to inspiration. While the LT in the control subjects was <= 2.1 s, the LT in half of the patients with OSAS was > 2.0 s (Fig 1 ). The mean value of LT for patients with OSAS was significantly longer than that for the control subjects (p < 0.05). The mean IST was significantly shorter in patients with OSAS than in control subjects: 1.95 ± 1.03 vs 3.28 ± 1.28 s, respectively (p < 0.05; Fig 2 ). The threshold volume for evoking a swallowing response varied from 0.4 to 2 mL of water in all participants (Fig 3 ). The threshold volume of water was greater in patients with OSAS than in the control subjects; although 0.4 mL of saline could induce swallowing in each control subject, > 0.8 mL of water was necessary to elicit swallowing in 5 of 20 patients with OSAS. The relationship between the severity of OSAS (as indicated by the AHI) and variables related to the swallowing reflex are depicted in Figure 4 , top, and Figure 4 , bottom. Although no significant correlation was measured between AHI and LT, AHI was negatively correlated with IST (r = 0.357; p = 0.024).



View larger version (17K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1. A representation of the latency for the swallowing reflex induced by a bolus of water in 20 patients with OSAS and in 20 age-matched control subjects (CTRL). The latency for swallowing initiation was judged using LT on the recording of submental EMG activity.

 


View larger version (19K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2. A representation of IST (expressed in seconds) in 20 patients with OSAS and in 20 age-matched control subjects (CTRL), as timed from swallowing termination to the next onset of inspiration.

 


View larger version (16K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 3. A representation of threshold volume (expressed in milliliters) of water that could evoke swallowing in 20 patients with OSAS and in 20 age-matched control (CTRL) subjects.

 


View larger version (18K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 4. The relationships between the severity of OSAS as indicated by AHI and swallowing reflex. Top, the relationship between the AHI and LT for swallowing reflex in all subjects (n = 40). Bottom, the relationship between the AHI and the IST in all subjects (n = 40).

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The present study demonstrated that the water-stimulated swallowing reflex, as determined using the LT, is delayed in patients with OSAS when compared to control subjects without OSAS. In our experience, the mean value of LT in normal volunteers is 1.7 ± 0.7 s27 ; thus, the current LT data for the control subjects were comparable to the normal values in healthy volunteers. However, the LT in patients with OSAS was longer than the LT in the control subjects. It has been suggested that a longer LT is an index for the risk of aspiration and aspiration pneumonia.29 Furthermore, the duration of IST before the initiation of the next breath following a swallowing movement was significantly shorter in patients with OSAS than in the control subjects without OSAS. IST may be an index reflecting the switching mechanism between deglutition apnea and breathing in relation to the swallowing movement in the upper airways. Thus, both the longer LT and the shorter IST in patients with OSAS may be parameters of a swallowing disorder that is associated with aspiration, because the next breath after swallowing stimulation may start before a complete terminus of the current deglutition. Furthermore, a greater volume of bolus water was necessary to induce the swallowing reflex in patients with OSAS than in the control subjects. In the control subjects, 0.4 mL of water was sufficient to elicit swallowing; however, > 1.2 mL of water was necessary to initiate swallowing in some patients with OSAS. These results suggest that the swallowing reflex is significantly impaired in patients with OSAS. Because the close reciprocal coupling between swallowing and breathing is a substantial protective mechanism for aspiration, the shorter duration of IST may influence the chances of aspiration occurring in patients with OSAS.

It has been reported21 22 23 that many patients with OSAS complain of sleep-related heartburn and the regurgitation of gastric contents into the pharynx. One may assume that patients with OSAS are predisposed to GER because of obesity and lowered inspiratory intrathoracic pressures during OSA. Kerr and coworkers23 have reported that nCPAP can correct the sleep apnea-related predisposition to GER in patients with OSAS. Although the authors have failed to demonstrate an obvious temporal association between OSA and GER, they have found that arousal and swallowing are clearly associated with reflux and the drop in esophageal pH.

The current study could not determine a direct causal relationship between swallowing disorder and sleep-disordered breathing. The LT did not correlate with the severity of OSAS (as indicated by the AHI; Fig 4 , top). However, the AHI was negatively correlated with IST (Fig 4 , bottom). The results suggest that severe OSAS may perturb the transition from inspiration to expiration during deglutition in patients, resulting in an increased vulnerability to aspiration. It would be reasonable to speculate that OSAS is a primary disorder that leads to an abnormality in the swallowing reflex, because nocturnal disordered breathing over a long period may cause abnormal receptor functions and/or the impaired function of afferent nerves to the higher brain, including the respiratory and swallowing centers. This speculation is also supported by the inhibition of the swallowing reflex in humans that occurs in response to nCPAP.20

Another explanation for the impaired swallowing reflex in patients with OSAS is that hypoxia and hypercapnia during the night may depress the swallowing reflex. It has been suggested30 that hypoxia depresses the swallowing reflex in cats. Although a simple extrapolation of our results to a clinical situation may not be entirely valid, it is possible that the impaired coupling between swallowing and breathing enhances the chances of aspiration of regurgitated material in patients with OSAS. This, along with obesity and a lowered inspiratory intrathoracic pressure, may explain the vulnerability of patients with OSAS to gastroesophageal aspiration into the airways.


   Footnotes
 
Supported by a grant from the Smoking Research Foundation of Japan.

Abbreviations: AHI = apnea plus hypopnea index; EMG = electromyogram; GER = gastroesophageal reflux; IST = inspiratory suppression time; LT = latent time; nCPAP = nasal continuous positive airway pressure; OSAS = obstructive sleep apnea syndrome; SaO2 = arterial oxygen saturation

Received for publication August 3, 1998. Accepted for publication February 16, 1999.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Smith, J, Wolkove, N, Colacone, A, et al (1989) Coordination of eating, drinking and breathing in adults. Chest 96,578-582
  2. Paydarfar, D, Gilbert, RJ, Poppel, CS, et al (1995) Respiratory phase resetting and airflow changes induced by swallowing in humans. J Physiol (Lond) 483,273-288
  3. Wilson, SL, Thach, BT, Broulliette, RT, et al (1981) Coordination of breathing and swallowing in human infants. J Appl Physiol 50,851-858
  4. Shaker, R, Ren, J, Zamir, Z, et al (1994) Effect of aging, position, and temperature on the threshold volume triggering pharyngeal swallows. Gastroenterology 98,396-402
  5. Nishino, T, Yonezawa, H, Honda, Y (1985) Effects of swallowing on the pattern of continuous respiration in human adults. Am Rev Respir Dis 132,1219-1222
  6. Selly, WG, Flack, FC, Ellis, RE, et al (1989) Respiratory patterns associated with swallowing: part 1; the normal adult pattern and changes with age. Age Ageing 18,168-172
  7. Chen, CH, Lai, CL, Tsai, TT, et al (1997) Foreign body aspiration into the lower airway in Chinese adults. Chest 112,129-133
  8. Gleeson, K, Eggli, DF, Maxwell, SL (1997) Quantitative aspiration during sleep in normal subjects. Chest 111,1266-1272
  9. Huxley, EJ, Viroslav, J, Gray, WR, et al (1978) Pharyngeal aspiration in normal subjects and patients with depressed consciousness. Am J Med 64,564-586
  10. Feinberg, MJ, Knebl, J, Tully, J, et al (1990) Aspiration and the elderly. Dysphagia 5,61-71
  11. Matsuse, T, Oka, T, Kida, K, et al (1996) Importance of diffuse aspiration bronchiolitis caused by chronic occult aspiration in the elderly. Chest 110,1289-1293
  12. Teramoto, S, Fukuchi, Y, Ouchi, Y (1996) Oxygen desaturation on swallowing in patients with stroke: what does it mean [letter]? Age Ageing 25,333-334
  13. Niederman, MS, Fein, AM (1986) Pneumonia in the elderly. Clin Geriatr Med 2,241-268
  14. Teramoto, S, Matsuse, T, Ouchi, Y (1998) Foreign body aspiration into the lower airways may not be unusual in older adults. Chest 113,1733-1734
  15. Teramoto, S, Matsuse, T, Oka, T, et al (1998) Investigation of effects of anesthesia and age on aspiration in mice using LacZ gene transfer by recombinant E1-deleted adenovirus vectors. Am J Respir Crit Care Med 158,1914-1919
  16. Chan, CS, Woolcock, AJ, Sullivan, CE (1993) Nocturnal asthma: role of snoring and obstructive sleep apnea. Am Rev Respir Dis 147,314-320
  17. Radwan, L, Maszczyk, Z, Koziorowski, A, et al (1995) Control of breathing in obstructive sleep apnea and in patients with the overlap syndrome. Eur Respir J 8,542-545
  18. Kimoff, RJ, Cheong, TH, Olha, AE, et al (1994) Mechanisms of apnea termination in obstructive sleep apnea: role of chemoreceptor and mechanoreceptor stimuli. Am J Respir Crit Care Med 149,707-714
  19. Wilcox, PG, Pare, PD, Road, JD, et al (1990) Respiratory muscle function during obstructive sleep apnea. Am Rev Respir Dis 142,533-539
  20. Nishino, T, Sugimori, K, Kohchi, A, et al (1989) Nasal constant positive airway pressure inhibits the swallowing reflex. Am Rev Respir Dis 140,1290-1293
  21. Samelson, CF (1989) Gastroesophageal reflux and obstructive sleep apnea. Sleep 12,475-476
  22. Diaz, S, Esteban, E, Piro, JM, et al (1990) Utility of CPAP in gastroesophageal reflux [letter]. Chest 97,1275
  23. Kerr, P, Shoenut, JP, Miller, T, et al (1992) Nasal CPAP reduces gastroesophageal reflux in obstructive sleep apnea syndrome. Chest 101,1539-1544
  24. Nishino, T, Tagaito, Y, Isono, S (1996) Cough and other reflexes on irritation of airway mucosa in man. Pulm Pharmacol 9,285-292
  25. Teramoto, S, Fukuchi, Y, Nagase, T, et al (1992) Quantitative assessment of dyspnea during exercise before an after bullectomy for giant bulla. Chest 102,1362-1366
  26. Teramoto, S, Fukuchi, Y, Orimo, H (1993) Effects of anticholinergic drug on dyspnea and gas exchange during exercise in patients with chronic obstructive pulmonary disease. Chest 103,1774-1782
  27. Marumo, K, Homma, S, Fukuchi, Y (1995) Postgastrectomy aspiration pneumonia. Chest 107,453-456
  28. Teramoto, S, Fukuchi, Y, Nagase, T, et al (1992) Analysis of nocturnal disturbed breathing in the elderly using desaturation index. Jpn J Geriatr (in Japanese) 29,554-558
  29. Nakazawa, H, Sekizawa, K, Ujiie, Y, et al (1993) Risk of aspiration pneumonia in the elderly. Chest 103,1636-1637
  30. Nishino, T, Kohchi, T, Honda, Y, et al (1986) Differences in the effects of hypercapnia and hypoxia on the swallowing reflex in cats. Br J Anaesth 58,903-908



This article has been cited by other articles:


Home page
 Am. J. Respir. Cell Mol. Bio.Home page
J. J. Atkinson and S. D. Shapiro
Neutrophil-mediated eosinophil transmigration: parting the red sea or leaving bread crumbs.
Am. J. Respir. Cell Mol. Biol., June 1, 2006; 34(6): 645 - 646.
[Full Text] [PDF]

Home page
 J. Immunol.Home page
R. Renckens, J. J. T. H. Roelofs, S. Florquin, A. F. de Vos, H. R. Lijnen, C. van't Veer, and T. van der Poll
Matrix Metalloproteinase-9 Deficiency Impairs Host Defense against Abdominal Sepsis
J. Immunol., March 15, 2006; 176(6): 3735 - 3741.
[Abstract] [Full Text] [PDF]

Home page
 Journal of the American Dental AssociationHome page
K. R. MAGLIOCCA and J. I. HELMAN
Obstructive sleep apnea: Diagnosis, medical management and dental implications
J Am Dent Assoc, August 1, 2005; 136(8): 1121 - 1129.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Respir. Cell Mol. Bio.Home page
T. S. Wilkinson, S. Potter-Perigo, C. Tsoi, L. C. Altman, and T. N. Wight
Pro- and Anti-Inflammatory Factors Cooperate to Control Hyaluronan Synthesis in Lung Fibroblasts
Am. J. Respir. Cell Mol. Biol., July 1, 2004; 31(1): 92 - 99.
[Abstract] [Full Text] [PDF]

Home page
 ChestHome page
S. Berg, V. Hoffstein, and T. Gislason
Acidification of Distal Esophagus and Sleep-Related Breathing Disturbances
Chest, June 1, 2004; 125(6): 2101 - 2106.
[Abstract] [Full Text] [PDF]

Home page
 ChestHome page
S. Teramoto, H. Yamamoto, Y. Yamaguchi, Y. Ouchi, and T. Matsuse
A Novel Diagnostic Test for the Risk of Aspiration Pneumonia in the Elderly
Chest, February 1, 2004; 125(2): 801 - 802.
[Full Text] [PDF]

Home page
 Dentomaxillofac RadiolHome page
E Levring Jaghagen, K. Franklin, and A Isberg
Snoring, sleep apnoea and swallowing dysfunction: a videoradiographic study
Dentomaxillofac. Radiol., September 1, 2003; 32(5): 311 - 316.
[Abstract] [Full Text] [PDF]

Home page
 ChestHome page
S. Teramoto, H. Yamamoto, Y. Ouchi, A. Valipour, and S. G. Spiro
Gastroesophageal Reflux Common in Patients With Sleep Apnea Rather Than Snorers Without Sleep Apnea
Chest, August 1, 2003; 124(2): 767 - 768.
[Full Text] [PDF]

Home page
 Am. J. Respir. Cell Mol. Bio.Home page
J. J. Atkinson and R. M. Senior
Matrix Metalloproteinase-9 in Lung Remodeling
Am. J. Respir. Cell Mol. Biol., January 1, 2003; 28(1): 12 - 24.
[Abstract] [Full Text] [PDF]

Home page
 ChestHome page
S. Teramoto, H. Kume, Y. Ouchi, C. Janson, and T. Gislason
Nocturnal Gastroesophageal Reflux: Symptom of Obstructive Sleep Apnea Syndrome in Association With Impaired Swallowing
Chest, December 1, 2002; 122(6): 2266 - 2267.
[Full Text] [PDF]

Home page
 ChestHome page
S. Teramoto, H. Kume, Y. Ouchi, and B. Mokhlesi
Altered Swallowing Physiology and Aspiration in COPD
Chest, September 1, 2002; 122(3): 1104 - 1105.
[Full Text] [PDF]

Home page
 ChestHome page
J. Herr, S. Teramoto, T. Ishii, and T. Matsuse
Chronic Cough, Sleep Apnea, and Gastroesophageal Reflux Disease
Chest, September 1, 2001; 120(3): 1036 - 1037.
[Full Text] [PDF]

Home page
 ChestHome page
S. Teramoto and Y. Ouchi
A Possible Pathologic Link Between Chronic Cough and Sleep Apnea Syndrome Through Gastroesophageal Reflux Disease in Older People
Chest, April 1, 2000; 117(4): 1215 - 1216.
[Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (29)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Teramoto, S.
Right arrow Articles by Fukuchi, Y.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Teramoto, S.
Right arrow Articles by Fukuchi, Y.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS