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(Chest. 2002;121:361-369.)
© 2002 American College of Chest Physicians

Oropharyngeal Deglutition in Stable COPD*

Babak Mokhlesi, MD; Jeri A. Logemann, PhD; Alfred W. Rademaker, PhD; Carrie A. Stangl, MS and Thomas C. Corbridge, MD, FCCP

* From the Division of Pulmonary and Critical Care (Drs. Mokhlesi and Corbridge), Speech Pathology (Dr. Logemann and Ms. Stangl), and Preventive Medicine (Dr. Rademaker) of the Northwestern University Medical School and the Veterans Administration Chicago Healthcare System-Lakeside Division.

Correspondence to: Babak Mokhlesi, MD, Division of Pulmonary and Critical Care Medicine, Cook County Hospital/Rush Medical College, 1900 West Polk St, Room 914, Chicago, IL 60612; e-mail: Babak_Mokhlesi{at}rush.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: The aim of this study was to examine deglutition in stable patients with COPD and lung hyperinflation.

Design: Twenty consecutive, eligible COPD patients with an FEV1 <= 65% of predicted and a total lung capacity >= 120% of predicted were enrolled prospectively.

Intervention: Patients received a detailed videofluoroscopic evaluation of oropharyngeal swallowing and were compared to 20 age-matched and sex-matched historical control subjects.

Setting: An outpatient pulmonary clinic at a Veterans Affairs Medical Center.

Measurements and results: The mean total lung capacity, functional residual capacity, and residual volume for the patients were 128% of predicted, 168% of predicted, and 218% of predicted, respectively. The mean FEV1 was 39% of predicted. There was no evidence of tracheal aspiration in either group. The laryngeal position at rest measured relative to the cervical vertebrae was not different between groups. The maximal laryngeal elevation during swallowing was significantly lower in patients with COPD (p < 0.001). Patients with COPD exhibited more frequent use of spontaneous protective swallowing maneuvers such as longer duration of airway closure and earlier laryngeal closure relative to the cricopharyngeal opening than did control subjects (p < 0.05).

Conclusions: We conclude that hyperinflated patients with COPD have an altered swallowing physiology. We suspect that the protective alterations in swallowing physiology (swallow maneuvers) may reduce the risk of aspiration. However, these swallowing maneuvers may not be useful during an exacerbation and may require further research.

Key Words: aspiration • COPD • oropharyngeal swallow • swallow maneuvers • videofluoroscopy


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Swallowing is a complex process that separates the tracheobronchial tree from the GI tract. These two systems share intimate anatomic and develop-mental relationships.1 Both swallowing and breathing consist of complex interactions between various muscles and nerves, including a voluntary and involuntary pattern of control. The swallowing process can be severely impaired in certain conditions.

COPD affects > 14 million people in the United States. There are approximately 10 to 15 million exacerbations per year, leading to 2 million hospitalizations.2 Often, the etiology of the COPD exacerbation is unclear. Aspiration has been suggested to be a cause in some patients, but there are few data supporting this relationship.2 Since there is a complex anatomic and functional relationship between swallowing and respiration, it is reasonable to question whether this relationship is disrupted when pulmonary function is compromised. Therefore, we studied 20 patients with COPD to determine whether this condition is an independent risk factor for aspiration. We were also interested in studying the effects of hyperinflation on laryngeal position and swallowing function. Our hypotheses were that hyperinflated patients with COPD have a lower laryngeal resting position, a decreased laryngeal elevation, and an increased risk of aspiration.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
All patients attended the outpatient pulmonary clinic at the Veterans Administration Chicago Healthcare System-Lakeside Division between September 1998 and March 1999. Twenty patients were selected in a consecutive manner. The inclusion criteria were the following: (1) >= 55 years of age; (2) a smoking history >= 30 pack-years; and (3) a history, physical examination findings, chest radiograph findings, and pulmonary function test (PFT) results that are compatible with COPD, as defined by the American Thoracic Society.2 Pulmonary function criteria included the following: FEV1, <= 65% of predicted; FEV1/FVC ratio, <= 70% of predicted; and total lung capacity, functional residual capacity, and residual volume by body plethysmography, >= 120% of predicted. We excluded patients with respiratory disorders other than COPD, patients who had undergone endotracheal intubation within the previous 3 months, those who had a previous or current tracheostomy, patients with head and neck cancer or head and neck surgery, and patients with CNS muscle pathology, muscle disease, or esophageal disease, including cancer, achalasia, and stricture. One patient had a history of elective intubation for anesthesia 5 years earlier. We also excluded patients with other conditions that may affect swallowing such as current abuse of alcohol (ie, more than one drink per day) and type 1 or 2 diabetes mellitus with > 20 years of insulin use.3 Smoking was not a confounding variable since only two of the patients were currently smoking. Only one patient was receiving oral steroid therapy, while 11 patients were receiving inhaled steroid therapy. We did not exclude patients who had gastroesophageal reflux disease (GERD) since our focus was on the pharynx, not the esophagus. However, a history of GERD was noted. Only one COPD patient had significant GERD symptoms. Significant GERD symptoms were defined as heartburn and/or regurgitation once or more per week.4 None of the healthy subjects had GERD symptoms. Twenty healthy historical control subjects who volunteered to complete a radiographic study of swallowing and who were matched for age and gender to COPD subjects also were studied. These individuals had no history of any disorder that might affect oropharyngeal swallowing, including intubations, CNS disease, gastroesophageal disease, COPD, and swallowing complaints, and had no history of smoking or of respiratory symptoms.

After obtaining informed consent, patients underwent a complete history and physical examination, and were asked to complete a dysphagia questionnaire. All patients had a chest radiograph and PFTs within 3 months of evaluation. Patients received a detailed videofluoroscopic evaluation of oropharyngeal swallowing in a standardized fashion.3 5 Control subjects had received the same oropharyngeal swallow evaluation previously. The protocol consisted of swallowing two boluses each of 3 mL and 5 mL barium liquid, cup drinking of barium liquid, and swallowing 3 mL barium paste. Individuals were seated and were viewed in the lateral plane during the radiographic study. The fluoroscopic tube was focused on the lips anteriorly, the cervical vertebrae posteriorly, the soft palate superiorly, and the cervical esophagus inferiorly. Studies were recorded on a VHS recorder for later slow motion and frame-by-frame analysis enabling the definition of the following: (1) swallowing disorders in oral preparation, oral, and pharyngeal stages of deglutition; (2) the duration of bolus movement through the oral cavity and pharynx (ie, transit times); and (3) the duration of physiologic swallow events such as airway closure and upper esophageal sphincter opening.

The laryngeal position at rest and at maximum elevation during swallowing were measured relative to the cervical vertebrae. Patients with COPD were monitored continuously with pulse oximetry. Patient and control subject videofluoroscopic studies were randomly analyzed by a speech language pathologist who was blinded to subject status (COPD vs control subject) and was not involved in performing the swallowing study. The interjudge and intrajudge reliability of judgments ranged from 0.81 to 0.99 and 0.85 to 1.00, respectively.

The study was approved by the Institutional Review Board of Northwestern University and by the Veterans Administration Chicago Healthcare System-Lakeside Division.

Data Reduction and Statistical Methods
Motility disorders were identified by reviewing the videotape of each swallow in slow motion. Temporal measures of the critical physiologic events in the oropharyngeal swallow such as airway closure, upper esophageal sphincter opening, and tongue base movement were recorded. In addition, other observations completed for each swallow were the following:

  1. Oral transit time: the time interval (in seconds) from the onset of tongue movement propelling the bolus posteriorly until the bolus head passes the ramus of the mandible;
  2. Pharyngeal transit time: the time interval (in seconds) from the bolus head passing through the ramus of the mandible until the bolus tail passes through the cricopharyngeal (CP) sphincter;
  3. Pharyngeal delay time: the time interval (in seconds) from the bolus head passing the ramus of the mandible until the onset of laryngeal elevation;
  4. Pharyngeal response time: the time interval (in seconds) from the onset of laryngeal elevation until the bolus tail passes through the CP sphincter;
  5. Duration of tongue base movement to the posterior pharyngeal wall: the first onset of posterior motion of the tongue base until first contact with the posterior pharyngeal wall during the swallow;
  6. Duration of tongue base contact to the pharyngeal wall at the level of the middle portion of the second cervical vertebrae (C2): first until last contact of the tongue base (mid-C2 level) to the posterior pharyngeal wall during the swallow;
  7. Duration of tongue base contact to the posterior pharyngeal wall at the inferior C2 level: first until last contact of the tongue base (inferior C2 level) to the posterior pharyngeal wall during the swallow;
  8. Duration of tongue base contact with the posterior pharyngeal wall at the superior C3 level: first until last contact of the tongue base (superior C3 level) to the posterior pharyngeal wall during the swallow;
  9. The time interval (in seconds) between the first laryngeal entrance closure and the first CP opening;
  10. Duration of velopharyngeal (VP) closure: the time interval (in seconds) from the first to the last contact of the soft palate with the posterior pharyngeal wall;
  11. Duration of laryngeal closure: the length of time (in seconds) that the laryngeal entrance between the arytenoid and the base of the epiglottis was closed in the lateral plane during the swallow;
  12. Duration of CP opening: the length of time (in seconds) that the CP region was open during each swallow;
  13. Duration of hyoid movement: the time interval (in seconds) between the start of movement and the return to the rest of the hyoid bone; and
  14. Duration of laryngeal elevation (in seconds): the time interval (in seconds) between the beginning of laryngeal elevation and the laryngeal return to rest.

In addition to these measures, observations were made regarding the presence or absence of aspiration (defined as food entering the trachea below the vocal folds), the approximate percentage of the bolus remaining in the oral cavity (ie, oral cavity residue) after the swallow, and the approximate percentage of residue remaining in the pharynx (pharyngeal residue) after each swallow.

Oropharyngeal swallow efficiency (OPSE)6 was calculated for each swallow as follows:

where ORES is the percentage of oral residue, PRES is the percentage of pharyngeal residue, ASPB is aspiration before the swallow, ASPD is aspiration during the swallow, OTT is oral transit time, and PTT is pharyngeal transit time.

The laryngeal position at rest and during the swallow were determined by defining the position of the undersurface of the vocal folds relative to the cervical vertebrae (upper edge and mid-lower edge). While evaluating the videofluoroscopic studies, the speech language pathologists noted that some patients swallowed both with and without spontaneous airway protective swallowing maneuvers. On this basis, the following three groups of swallows were identified for the analysis of swallowing data: (1) swallows from control subjects; (2) patient swallows in which no protective maneuvers were performed; and (3) patient swallows in which a protective maneuver was performed. A single patient could have had swallows with and without maneuvers. Nine of 20 patients performed swallows with and without protective maneuvers. Since for any bolus type, the number of patients having swallows both with and without maneuvers was minimal (at most four), the groups were considered to be independent. Swallowing measures were compared among groups using mixed-model analysis of variance in which multiple swallows within a person at any bolus were kept distinct in the analysis. If the p value comparing groups was statistically significant (p < 0.05), then pairwise comparisons were performed among the groups, with each having p < 0.05 as the criterion for significance. If the p value comparing the groups was not significant, then no pairwise comparisons were performed. Laryngeal position was compared among groups using Fisher’s Exact Test. Pearson correlation coefficients were calculated among 9 respiratory measures (ie, respiratory rate, pulse oximetry, and seven PFT parameters) and 18 swallowing measures at each of four bolus types (total, 648 correlations).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
There were 20 participants with COPD in this study, and 19 were men. Sixteen participants had an FEV1 < 50% of predicted. Nine participants were receiving home oxygen therapy. The demographics and PFT characteristics of these patients are shown in Table 1 . Four patients (20%) reported mild and intermittent dysphagia. None of these four patients had complained of these symptoms prior to completing the dysphagia questionnaire. For all patients, respiratory rate and pulse oximetry remained unchanged during the swallowing study. The two groups, control subjects and patients with COPD, were compared on the following five levels of data: (1) frequency of swallowing disorders; (2) frequency of voluntary changes during swallowing; (3) temporal measures of swallowing; (4) laryngeal position at rest and at mid-swallow; and (5) correlations among respiratory parameters and swallowing measures.


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  		Table 1. Demographics of the 20 Patients With COPD

 
Swallowing Disorders
Control subjects did not exhibit any abnormalities of swallowing during the study. Patients with COPD exhibited a number of swallowing disorders, as shown in Table 2 . Patients did not exhibit any of the following disorders: reduced lip closure; tongue thrust; apraxia of swallow; absent pharyngeal swallow; reduced VP closure; incomplete closure of the laryngeal vestibule; reduced glottic closure; unilateral or bilateral pharyngeal weakness; reduced CP opening; or aspiration. Despite recognizable swallowing disorders, almost all patients had functional swallows, that is, they were not aspirating and were eating an entirely oral diet.


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  		Table 2. Frequency of Occurrence of Swallowing Disorders in COPD Patients*

 
Frequency of Voluntary Changes During Swallowing
During the slow-motion analysis of each swallow for the presence of abnormalities, the frequency of voluntary changes in swallowing was noted. Control subjects did not use voluntary maneuvers during swallowing. Nine of the 20 patients with COPD (45%) were spontaneously utilizing voluntary prolonged closure of the airway entrance on at least some bolus types. This level of airway closure is illustrated in Figure 1 .



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  		Figure 1. Lateral drawing of the neck demonstrating the airway entrance closure maneuver used by some patients with COPD.

 
Temporal Measures of Swallow
Because of the number of COPD patients using an airway closure maneuver, the statistical analysis of the temporal measures was completed by dividing all patient swallows into the following two groups: those swallows with spontaneous maneuvers and those without maneuvers, as shown in Figures 2 -4 and Tables 3 -6 . Figure 2 shows the differences in the duration of airway entrance closure for the three subject groups for all four bolus types. These differences were statistically significant for patients with spontaneous protective maneuvers compared to others receiving 5 mL liquids and those performing paste swallows. As shown in Figure 3 , patients using protective maneuvers closed their airways early, well before the CP opening. These differences were statistically significant (p < 0.05) only for patients using protective maneuvers compared to patients in other groups performing paste swallows. The control subjects exhibited closure of the airway entrance within 0.06 s of the opening of the CP (upper esophageal) sphincter, a relationship that has been documented previously.7 8 Differences in delay in the triggering of pharyngeal swallowing are shown in Figure 4 . Both patient groups typically exhibited longer pharyngeal delays (but not significantly so) than control subjects except during paste swallows in which the patients not using protective maneuvers had significantly longer delays than did control subjects or patients using protective maneuvers.



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  		Figure 2. The duration of airway entrance closure (mean and SE) by bolus type for control subjects (open bars), patient swallows using protective maneuvers (shaded bars), and patient swallows not using protective maneuvers (hatched bars). * = p < 0.05 compared with patients using protective maneuvers.

 

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  		Table 3. Oropharyngeal Swallowing Measures for the Three Subject Groups Performing 3-mL Liquid Swallows*

 


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  		Figure 3. Laryngeal closure to CP opening (mean and SE) by bolus type for control subjects (open bars), patient swallows using protective maneuvers (shaded bars), and patient swallows not using protective maneuvers (hatched bars). * = p < 0.05 compared with patients using protective maneuvers.

 


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  		Figure 4. Duration of pharyngeal delay (mean and SE) by bolus type for control subjects (open bars), patient swallows using protective maneuvers (shaded bars), and patient swallows not using protective maneuvers (hatched bars). * = p < 0.05 compared with patients not using protective maneuvers.

 
Tables 3 4 5 6 present the remainder of the temporal data for the three subject groups performing swallows with 3 mL (Table 3) and 5 mL (Table 4 ) liquid, cup-drinking swallows (Table 5 ), and paste swallows (Table 6 ).


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  		Table 4. Oropharyngeal Swallowing Measures for the Three Subject Groups Performing 5-mL Liquid Swallows*

 

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  		Table 5. Oropharyngeal Swallowing Measures for the Three Subject Groups Performing 1-Cup Liquid Swallows*

 

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  		Table 6. Oropharyngeal Swallowing Measures for the Three Subject Groups Performing Paste Swallows*

 
Laryngeal Position
There was a trend toward lower laryngeal position at rest in patients with COPD, but the difference did not reach statistical significance. Laryngeal position at mid-swallow was significantly lower in COPD patients (with and without maneuvers) than in control subjects (p < 0.001).

Correlations Between Respiratory Parameters and Swallowing Measures
Pearson correlation coefficients were used to examine whether swallow variables correlated with respiratory variables. The number of significant correlations did not exceed the number expected by chance (significant correlations, 27; total correlations, 648).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Our study is the first clinical study providing detailed analysis of swallowing in stable hyperinflated patients with COPD. The data demonstrate that COPD is associated with abnormal swallowing physiology. Abnormalities consisted of frequent spontaneous and protective maneuvers and decreased laryngeal elevation during swallowing. We suspect that protective swallowing maneuvers explain the absence of aspiration in this study.

There are limited data correlating COPD with aspiration. Cohello9 found aspiration in three of his COPD patients. However, his patient population was heterogeneous relative to pulmonary status. Thirteen of the 14 patients had tracheostomy tubes, and 5 patients were ventilator-dependent, which is a very different population than that assessed in this article.9

Other studies have examined the risk of aspiration during COPD exacerbation. Shaker et al10 have demonstrated that tachypnea, aging, bolus volume, and COPD modify the close coordination between deglutition and respiration. They found that patients experiencing COPD exacerbations swallowed significantly more often by interrupting the inspiratory phase and resumed their respiration significantly more with inspiration. Stein et al11 studied 25 patients with severe COPD who experienced frequent exacerbations. CP dysfunction was diagnosed in 17 of these patients. The majority had dysphagia, and eight patients who underwent a CP myotomy had significant improvement in swallowing and a decrease in respiratory exacerbations. Mokhlesi et al4 have reported a higher prevalence of dysphagia in patients with COPD when compared with control subjects (17% vs 4%, respectively). In our patient population, 20% of patients (4 of 20 patients) reported dysphagia.

Our patients exhibited a shorter duration of CP opening on three of the four bolus types, but these differences were not statistically significant. Other studies12 13 14 15 16 are available examining the coordination of breathing and airway protection during deglutition, however, these studies did not evaluate patients with COPD. Active smoking also can affect swallowing,17 18 however, smoking was not a confounding variable since only two of the patients were currently smoking.

In summary, we conclude that stable hyperinflated patients with COPD frequently exhibit abnormal swallowing physiology. Patients exhibit protective swallowing maneuvers that appear to improve airway protection. Additional studies should be performed to determine whether patients with less severe COPD exhibit any protective maneuvers or aspiration. The relationships among swallowing difficulty, aspiration, and exacerbation of COPD remains to be elucidated. Further research is needed to evaluate occult aspiration as a cause of (and/or contributing factor to) COPD exacerbation and whether patients in exacerbation are at even greater risk of aspiration.


   Footnotes
 
Abbreviations: CP = cricopharyngeal; GERD = gastroesophageal reflux disease; PFT = pulmonary function test; VP = velopharyngeal

This research was supported by grant P01 CA 40007 from the National Cancer Institute of the National Institutes of Health.

Received for publication January 19, 2001. Accepted for publication August 27, 2001.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. deMello, DE, Reid, LM (1995) Developmental anatomy of the proximal gastrointestinal tract and lungs. Semin Respir Crit Care Med 16,439-447
  2. Celli, BR, Snider, GL, Heffner, JE (1995) American Thoracic Society statement: standards for the diagnosis and care of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 152,S77-S120
  3. Logemann, JA (1988) Evaluation and treatment of swallowing disorders 2nd ed. ,313 Pro-Ed Austin, TX.
  4. Mokhlesi, B, Morris, AL, Huang, CF, et al (2001) Increased prevalence of gastroesophageal symptoms in patients with COPD. Chest 119,1043-1048[Abstract/Free Full Text]
  5. Logemann, JA (1993) A manual for videofluoroscopic evaluation of swallowing 2nd ed. Pro-Ed Austin, TX.
  6. Rademaker, AW, Pauloski, BR, Logemann, JA, et al (1995) Oropharyngeal swallow efficiency as a representative measure of swallowing function. J Speech Hear Res 37,314-325
  7. Rademaker, AW, Pauloski, BR, Colangelo, LA, et al (1998) Age and volume effects on liquid swallowing function in normal women. J Speech Hear Res 41,275-284
  8. Logemann, JA, Pauloski, BR, Rademaker, AW, et al (2000) Temporal and biomechanical characteristics of oropharyngeal swallow in younger and older men. J Speech Lang Hear Res 43,1264-1274[Abstract/Free Full Text]
  9. Cohello, CA (1987) Preliminary findings on the nature of dysphagia in patients with chronic obstructive pulmonary disease. Dysphagia 2,28-31[CrossRef][Medline]
  10. Shaker, R, Townsend, WF, Dodds, WJ, et al (1992) Coordination of deglutition and phases of respiration: effect of aging, tachypnea, bolus volume, and chronic obstructive pulmonary disease. Am J Physiol 263,G750-G755[Abstract/Free Full Text]
  11. Stein, M, Williams, AJ, Grossman, F (1990) Cricopharyngeal dysfunction in chronic obstructive pulmonary disease. Chest 97,347-352[Abstract/Free Full Text]
  12. Martin, BJW, Logemann, JA, Shaker, R, et al (1994) The coordination between respiration and swallow: respiratory phase relationships and temporal integration. J Appl Physiol 72,714-723
  13. Shaker, R, Dodds, WJ, Dantas, RO, et al (1990) Coordination of deglutitive glottic closure with oropharyngeal swallowing. Gastroenterology 98,1478-1484[ISI][Medline]
  14. Martin, BJW, Robbins, J (1995) Physiology of swallowing: protection of the airway. Semin Respir Crit Care Med 16,448-458
  15. Shaker, R (1995) Airway protective mechanisms: current concepts. Dysphagia 10,216-227[CrossRef][ISI][Medline]
  16. Gilbert, RJ, Daftary, S, Woo, P, et al (1996) Echoplanar magnetic resonance imaging of deglutitive vocal fold closure: normal and pathologic patterns of displacement. Laryngoscope 106,568-572[CrossRef][ISI][Medline]
  17. Kahrilas, PJ, Gupta, RR (1989) The effect of cigarette smoking on salivation and esophageal acid clearance. J Lab Clin Med 114,431-438[ISI][Medline]
  18. Dua, K, Bardan, E, Ren, J, et al (1998) Effect of chronic and acute cigarette smoking on the pharyngo-upper oesophageal sphincter contractile reflex and reflexive pharyngeal swallow. Gut 43,537-541[Abstract/Free Full Text]



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S. Teramoto, H. Kume, Y. Ouchi, and B. Mokhlesi
Altered Swallowing Physiology and Aspiration in COPD
Chest, September 1, 2002; 122(3): 1104 - 1105.
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