Rationale: During deglutition, a strongly preferred exhale–swallow–exhale pattern has been shown in healthy adults. Disruption of this pattern can provoke prandial aspiration. Impaired coordination of breathing and swallowing has been measured in patients with chronic obstructive pulmonary disease (COPD) during the exacerbated state, but no reports describe the coordination of breathing and swallowing in stable patients with COPD during oral intake.
Objectives: To test the hypothesis that persons with moderate to severe COPD would show disordered coordination of breathing and swallowing during oral intake when compared with a matched, healthy control group.
Methods: This study used a prospective, repeated measures design using 25 subjects with COPD and 25 control subjects. Respiratory inductance plethysmography and nasal thermistry were used simultaneously to track respiratory signals. Submental surface EMG was used to mark the presence of each swallow within the respiratory cycle. Data were recorded while participants randomly and spontaneously swallowed solids and semi-solids.
Measurements and Main Results: Logistic regression showed that participants with COPD swallowed solid food during inhalation more frequently than normal subjects (P = 0.002) and had a significantly higher rate of inhaling after swallowing semi-solid material (P < 0.001). Subjects with COPD also swallowed pudding at low Vt significantly more often than they did the cookie (P = 0.006). Conversely, the control subjects swallowed cookie at low Vt significantly more often than pudding (P = 0.034). Significant differences in deglutitive apnea durations were also found.
Conclusions: Patients with COPD exhibit disrupted coordination of the respiratory cycle with deglutition. Disrupted breathing–swallowing coordination could increase the risk of aspiration in patients with advanced COPD and may contribute to exacerbations.
During deglutition, a strongly preferred exhale–swallow–exhale pattern has been observed. Disruption of this pattern can provoke prandial aspiration. Abnormal coordination of breathing and swallowing has not been described in stable patients with COPD.
This study documents several abnormal aspects of respiratory timing during swallowing in patients with COPD and demonstrates that stable patients with COPD swallow at points during the respiratory cycle that can promote prandial aspiration.
During deglutition, a strongly preferred exhale–swallow–exhale pattern has been found in healthy adults (7–10). A disruption of the normal breathing–swallowing pattern, such as inhaling after the swallow, could put patients at increased risk for aspiration because the negative pressure of inhalation has the potential to draw food and liquid residue toward the lungs (8, 11). In addition, swallowing during early inhalation, late exhalation, or at the transition from exhalation to inhalation results in decreased subglottic air pressure during the swallow (12). The presence of subglottic mechanoreceptors has been established; however, a clear role for them in laryngeal or respiratory control has not been demonstrated (13). The primary function for these receptors seems to be in relation to the swallowing. Accordingly, low or absent deglutitive subglottic pressure at the time of the swallow has been shown to change physiology by prolonging pharyngeal contraction duration in healthy adults (6) and slowing bolus transit time or increasing amounts of pharyngeal residue and aspiration frequency in patients undergoing tracheostomy (5, 14, 15). Breathing and swallowing coordination may be particularly important to patients with chronic obstructive pulmonary disease (COPD) because prandial aspiration may be a factor that sets off an exacerbation of COPD. Conversely, an exacerbation of COPD may promote aspiration, thereby increasing the severity (16, 17).
Preiksaitis and colleagues (7) suggested that patients with COPD may be prone to disrupted breathing and swallowing patterning because of the combined effects of deglutitive apnea and reduced ventilatory capacity. Shaker and colleagues compared breathing and swallowing coordination of spontaneous saliva swallows in 10 patients with COPD at their basal state and during exacerbation. They reported that spontaneous swallowing interrupted the inhalatory phase and was followed by inspiration significantly more frequently during exacerbation when compared with the patients' basal state (17). Their work serves as a basis from which additional exploration into relationships between pulmonary status at the time of the swallow, coordination of the upper airway with deglutition, and exacerbation can be explored. The purpose of this investigation was to further elucidate the relationships between breathing and swallowing in patients with COPD during deglutition. Portions of this work and preliminary data were presented in a poster at the annual meeting of the American Thoracic Society (18).
This study was approved by the Pittsburgh VA subcommittee for the protection of human subjects, and all volunteers provided written informed consent before participation.
Participants with COPD were recruited from the home oxygen program at the VA Pittsburgh University Drive location. Spirometry was completed in the preceding 30 days before data collection to confirm moderate or severe COPD. Moderate COPD was defined FEV1/FVC <70% and FEV1 64 to 50% predicted. Severe COPD was defined as FEV1/FVC <70% and FEV1 <50% predicted (19). Exclusion criteria for the COPD group was the presence of an indwelling tracheostomy tube and/or naso-gastric feeding tube, history of stroke or Parkinson's disease, active pulmonary infection, fever, exacerbated COPD, cardiac ischemia or congestive heart failure, and severe metabolic derangements. A total of 25 male patients with COPD with a mean age of 69 years (SD, 8; range, 52–87 yr) participated. Nineteen out of twenty-five participants were classified as severe COPD with a mean FEV1 of 35% predicted (range, 14–49% predicted), and 6 out of 25 were classified as moderate COPD (mean FEV1, 59%).
Family members of the patients with COPD, staff, and visitors to the medical center were recruited for the healthy control group. Control subjects had no history of oropharyngeal dysphagia or complaints about swallowing function, no history of neurologic disease, no history of oral or pharyngeal cancer, and no history of COPD. Spirometric testing was completed to verify a FEV1/FVC ratio greater than 70% predicted. All potential participants completed a screening questionnaire that consisted of questions that are routinely used to identify dysphagic symptoms and risk factors for dysphagia during clinical evaluation. Any verbal or written description of dysphagic symptoms provided by the potential participant, such as coughing, choking, or the feeling of food sticking in their throat, or a positive response to any of the questions on any portion of the questionnaire excluded the participant from the study. A total of 25 healthy control subjects with a mean age of 64 years (SD 9, range 51–81) participated. There were 12 male and 13 female subjects.
For both groups, the use of medications at the time of the study that may have an effect on swallowing function, such as psychotropic drugs and barbiturates, excluded potential subjects from participation. To rule out dementia, a delayed/immediate recall ratio < 95% on the Story Retelling-Immediate/Story Retelling-Delayed subtests of the Arizona Battery for Communicative Disorders of Dementia excluded enrollment (20).
The KayPentax Swallowing Station and Swallowing Signals Lab (KayPentax, Lincoln, NJ) enabled the acquisition and recording of simultaneous respiratory and surface electromyographic (SEMG) measurements. Two auxiliary ports enabled respiratory signals to be displayed from an uncalibrated respiratory inductance plethysmograph (Respitrace; Ambulatory Monitoring Inc., Ardsley, NY) that measured changes in cross-sectional area of the rib cage and abdomen, allowing for the determination of direction of motion (inhalation or exhalation). The software takes the combined movement of chest and abdomen and calculates a summed output that is reflective of changes in Vt. Chest motion was displayed in one port, and a summed output of chest and abdominal motion (Vt) was displayed in the second port. Combined sum was used during data analysis to assure that the chest and nasal signals were pulmonary related and not artifact. Respiratory data were also obtained from the Signals Lab's calibrated nasal cannula (Micro Switch AWM200 Microbridge Mass Airflow sensor; Honeywell, Morristown, NJ) that displayed the direction, level, and duration of airflow. For the SEMG, two Ag/AgCl electrodes and a reference electrode contained in a single cohesive housing designed to detect the occurrence of the swallow were affixed under the patient's chin behind the mental symphysis according to the manufacturer's instructions. This muscle group includes the mylohyoid, anterior belly of the digastrics, and geniohyoid (21). The electrode placement and muscle group have been shown to be valid and reliable indicators of the pharyngeal swallow (22). The swallowing station software provided a rectified, integrated, and smoothed EMG signal so that a distinctive peak at the height of laryngeal elevation occurring during each swallow was clearly displayed and time-locked to the other respiratory signals. The occurrence of each swallow was determined by the simultaneous appearance of deglutitive apnea where the flow at the nasal cannula ceases and a black, flat line is visualized and electromyographically using SEMG. Figures 1 and 2 show examples of the raw data.
Data were recorded while participants randomly and spontaneously swallowed a total of nine 2.5-g solid (vanilla wafer cookie) portions that were placed on a plate and 10 5-ml semi-solid (vanilla pudding) boluses that were measured out onto individual teaspoons. To simulate as natural an eating environment as possible, each subject was seated comfortably at a table as they self-fed without cueing.
Food boluses that were not swallowed entirely on the first swallow were not analyzed because bolus volume was controlled in this experiment. Any discrepancy between nasal and plethysmography signals, such as those that can occur when the nasal cannula becomes occluded and the signal lost or when the respitrace signal exhibited electrical artifact, were excluded from the final analysis. Both groups swallowed a total of 250 pudding swallows, from which 230 of the control group (92%) and 238 (95%) from the COPD group were acceptable for analysis. From a total of 225 cookie swallows, 214 (95%) were suitable for analysis from the healthy control group and 219 (97%) from the COPD group.
Each swallow was noted by the simultaneous appearance of deglutitive apnea where nasal airflow ceases while the airway is closed and a peak in the SEMG signal when swallowing muscles are activated. These combined signals were also used to distinguish periods of breath holding and mouth breathing from deglutitive apnea because only bolus swallows gave a time-linked apnea/SEMG signal. Respiratory phase in which the swallow occurred and postswallow airflow direction (negative or inhalation vs. positive or exhalation) were determined using the combined nasal airflow and plethysmographic signals. When mouth breathing resulted in a temporary loss of nasal airflow, the signal from plethysmography was used to determine respiratory phase so long as there had been good correlation between nasal and plethysmography traces.
Swallows that occur at or near end-exhalation or the transition between exhalation and inhalation are associated with lower lung volumes. Swallows that occur at the transition between inhalation and exhalation or near end-inhalation are associated with higher Vt. Because lung volume at the time of the swallow is directly related to the amount of subglottic pressure generated during the swallow (12), the frequency of high versus low Vt was examined. To estimate Vt at the time of the swallow (high vs. low), the duration of the exhalation or inhalation portion of the respiratory phase was determined in milliseconds using the Swallowing Signals Lab software. This value was divided into four quadrants. The first and last quadrants were used to classify swallows into early or late inhalation or exhalation.
The duration of deglutitive apnea (DDA) was defined as the length of time that the nasal signal returned to baseline (zero flow), indicating central inhibition of respiratory musculature and airway closure associated with swallowing (23). The brief negative, nonrespiratory deflection that commonly appears as the pharynx begins to open postswallow was not included in DDA.
Blinding procedures were used for all measurements. Twenty percent of the data was randomly selected for reliability purposes. Intrarater agreement for dichotomous determinations (respiratory phase) ranged from a Kappa value of 0.685 to 0.739. Interrater reliability ranged from 0.648 to 0.771. For the continuous variable (DDA) intraclass correlation was 0.80 for intrarater and 0.6 for interrater measurements. Logistic regression was used to analyze breathing–swallowing data. Apnea data were not normally distributed; therefore, the nonparametric generalized linear model was used for the analysis. Statistical significance was set at P < 0.05 before data analysis. All analyses were performed with SAS version 8 software (SAS Institute Inc., Cary, NC).
Logistic regression analysis showed that participants with COPD swallowed the solid bolus (cookie) during inhalation significantly more often than normal subjects (P = 0.002). When comparing food types within each group (cookie vs. pudding), the percentage of swallows that occurred during inhalation was not significantly different in the COPD group (P = 0.277). However, healthy subjects swallowed significantly less often during inhalation when eating the cookie (P = 0.001). Table 1 is a statistical table, and Figure 3 is a graphic representation of percentages.
Odds Ratio (95% CI)
|Control vs. COPD|
|Pudding vs. cookie|
| COPD||Pudding||28/238||0.737 (0.424–1.282)||0.277|
Postswallow inhalation occurred significantly more often in the COPD group with the semi-solid (pudding) when compared with control subjects (P < 0.001). Figure 4 shows a graphic representation of the percentages. Within the COPD group, postswallow inhalation also occurred significantly more often with pudding when compared with cookie (P = 0.001). There was no difference in the rate of postswallow inhalation when pudding and cookie were compared within the control group (P = 0.457). Table 2 displays the statistical table.
Odds Ratio (95% CI)
|Control vs. COPD|
|Pudding vs. cookie|
| COPD||Pudding||44/238||0.422 (0.249–0.716)||0.001|
Between-group comparisons found that the normal and COPD participants swallowed the cookie at high Vt with the same frequency (P = 0.36). However, subjects with COPD swallowed pudding at low Vt significantly more often than the normal control subjects (P < 0.001). Within-group comparison of food types revealed that the subjects with COPD also swallowed pudding at low Vt significantly more often than cookie (P = 0.006). Conversely, the control subjects swallowed cookie at low Vt significantly more often than pudding (P = 0.034). Table 3 is the statistical table, and Figure 5 shows a graphic representation of between group comparisons. Correspondingly, there were significant interactions between food and group for swallows occurring during inhalation (P = 0.030), for postswallow inhalation (P = 0.007), and for low Vt swallows (P = 0.001).
Odds Ratio (95% CI)
|Control vs. COPD|
|Pudding vs. cookie|
| COPD||Pudding||45/250||0.519 (0.319–0.843)||0.006|
There was no difference in DDA between the groups for either consistency. In addition, there were no significant differences between the consistencies within the control group (P = 0.589). However, the DDA for pudding in the COPD group was significantly shorter than the DDA for cookie (P = 0.03).
Because swallowing during inhalation and postswallow inhalation are thought to be risk factors for aspiration, within-group comparisons of DDA between inhalation versus exhalation were made for each food type.
When the food types were combined, DDA was longer in both groups for swallows that occurred during the inhalation phase. The median DDA for control subjects was 670 milliseconds during exhalation and 801 milliseconds during inhalation (P = 0.025). The median DDA in the COPD group was 624 milliseconds during exhalation and 736 milliseconds during inhalation (P = 0.001). In the control group, the DDA for pudding swallows that occurred during inhalation were significantly longer than those that occurred during exhalation (P = 0.018). There was no difference in DDA between inhalation and exhalation for cookie (P = 0.868). In the COPD group, the DDA of swallows that occurred during the inhalation phase were significantly longer for both food types (P = 0.011 for cookie and 0.002 for pudding). Table 4 is a statistical table of these data.
|n||Mean (SD)||Median||n||Mean (SD)||Median||P Value|
|Cookie||176||694 (147)||687||4||760 (142)||775||0.868|
|Pudding||171||675 (117)||664||22||910 (288)||805||0.018|
|Cookie||149||681 (151)||641||16||760 (158)||26||0.011|
| Pudding||149||634 (120)||613||26||763 (137)||750||0.002|
In the control group, the DDA was not significantly different for cookie or pudding swallows when inhalation followed (P = 0.244 for cookie and P = 0.276 for pudding). However, in the COPD group, the DDA of pudding swallows that were followed by inhalation was significantly shorter in duration (P = 0.0411).
When compared with control subjects, patients with COPD showed three patterns of impaired breathing and swallowing coordination: First, when eating a bolus that required mastication, the frequency with which swallows occurred during inhalation was significantly greater. Second, the semi-solid pudding was followed by inhalation with significantly increased frequency. Third, COPD participants swallowed at low Vt at a significantly higher rate than the healthy volunteers. The abnormal timing of swallows within the respiratory cycle that we measured can help to explain the relationship between pulmonary disease and dysphagia.
The breathing and swallowing coordination of our control group was consistent with the majority of other published studies where, regardless of food consistency, the preponderance of spontaneous swallows occurred during exhalation (94%) (8, 10, 11, 24–29). Our control subjects also most frequently timed swallows to occur at higher Vt, such as at early to mid-exhalation, at late inspiration, or at the transition between inhalation to exhalation. This finding is consistent with several other reports (8, 11, 25, 30, 31). The postswallow breathing cycle observed in our healthy control subjects also correlated with reports in the literature where > 90% of swallows were followed by exhalation (8, 10, 24, 26, 32, 33).
Solid food was used in this investigation because mastication has been shown to affect the respiratory rhythm by causing the breathing cycle to become irregular (3, 29) and increasing respiratory rate (34). Thus, our results are consistent with and build upon those of Shaker and colleagues, who studied nonnutritive swallows and reported disordered breathing and swallowing patterns when respiratory rate and rhythm were altered by COPD exacerbation.
The presence of lung disease may be an important factor in a person's ability to coordinate breathing and swallowing adequately. A test of this hypothesis was performed by Kijima and colleagues (35). As expected, in the control condition, water swallows of healthy, young subjects were observed primarily to occur during exhalation. The experimental condition of elastic loading shifted 50% of their swallows to the exhale to inhale interval and was also associated with “laryngeal irritation” indicated by coughing. The exhalation to inhalation transition point is essentially end-exhalation and consistent with a low Vt. The coughing that occurred when the subjects swallowed at the low Vt strongly implies that aspiration occurred as a result of swallowing at end-exhalation. Their findings also support the suggestion by Shaker and colleagues that disrupted breathing and swallowing patterns might increase the risk of aspiration and the sequelae that can ensue (17).
The preferred pattern of timing swallows with higher lung volumes may reflect the situation in which it is most easy to generate subglottic air pressure during the swallow (deglutitive subglottic pressure [DPsub]). There is a direct relationship between lung volume and the amount and polarity of DPsub. Lung–thoracic unit recoil is likely responsible for the generation of DPsub because respiratory muscles are centrally inhibited during the swallow (12). Therefore, recoil potential may need to be considered as a variable related to swallowing function. As such, other conditions associated with hyperinflation, such as bronchiectasis, those that restrict lung expansion, and extrinsic restrictive disorders (e.g., kyphoscoliosis), could reduce DPsub and affect swallowing function. Although the exact relationship between the amount of DPsub and swallowing integrity is still being investigated, the fact that our breathing–swallowing pattern is not random signifies that this pattern serves a purpose. Considering the intimate anatomic and neuroanatomic relationships of the upper airway, the most likely purpose would be optimization of swallowing function (36).
A few investigations have concluded that normal swallows most often occur at end-exhalation (3, 37). The theory is that the position of the larynx would be higher at end-exhalation and thus at a mechanical advantage because rapid laryngeal elevation occurs during swallowing. Mitchinson and Yoffey disproved this assumption when they X-rayed 23 subjects in extremes of inhalation and exhalation and showed that deep inspiration did not result in a corresponding descent of the larynx (38). They postulated that contraction of suprahyoid and infrahyoid musculature serves to stabilize the hyoid and larynx as the distal trachea descends with the traction force of the diaphragm. Andrew later verified their hypothesis in an animal model (39). Swallows occurring at end-exhalation are more likely to be followed by inhalation, as our data have shown. Inhalation after swallowing may increase the frequency of prandial aspiration (17, 40–42).
Additional evidence linking pulmonary compromise with disruptions in breathing and swallowing coordination can be found in the DDA values. Deglutitive apnea occurs involuntarily during each swallow when the respiratory muscles are centrally inhibited and the airway closes. DDA is most often cited to range from approximately 0.5 to 1.0 seconds (8, 10, 26, 28, 43–45). The overall mean apnea that we measured in both groups was consistent with other reports (654.00 ms in the control group and 641.00 ms in the COPD group). DDA has also been examined as a function of age, bolus volume, and gender; however, our study is the first to examine DDA in the context of respiratory phase relationships (inhalation vs. exhalation). Participants with COPD showed longer DDA for both materials when swallows occurred during inhalation, whereas the control subjects prolonged DDA with the pudding only. Prolongation of DDA could indicate the presence of a compensatory mechanism, such as providing more time for recoil forces to generate higher DPsub or more time for the bolus to traverse the pharynx and enter the esophagus. Spontaneous swallowing compensations occurring in patients with COPD were previously reported by Mokhlesi and colleagues (46).
There was no effect of DDA in the control subjects on the postswallow respiratory phase; however, a shorter DDA was measured in the subjects with COPD for pudding. This finding, when combined with the increased frequency with which these subjects swallowed at low Vt and inhaled after swallowing pudding, seems to suggest that ventilatory drive or “air hunger” can take precedence over deglutition when necessary. The increased frequency of postswallow inhalation of saliva during exacerbation reported by Shaker and colleagues demonstrates this point.
We set our inclusion/exclusion criteria so that we would capture subjects who were homogenous in terms of clinical severity. However, a limitation of our study is that we are unable to determine if disrupted breathing and swallowing patterns vary as a function of the severity of obstructive disease. A larger study that stratifies patients with COPD by severity level could address this issue. Another limitation of our study is that swallowing function was not measured. Additional study of the potential physiologic swallowing alterations that may occur at different points within the respiratory cycle or at known lung volumes may further explain the interplay of respiratory and deglutitive functions.
The study of swallowing and breathing relationships is important because oropharyngeal dysphagia is an underdiagnosed comorbidity in patients with COPD (47–49). Indeed, the presence of COPD was shown to be the most significant risk factor for aspiration pneumonia in nursing home patients (50). The direct observation of swallowing physiology in patients with COPD under fluoroscopy has revealed findings that are consistent with dysphagia, such as delayed pharyngeal response, decreased base of tongue retraction, and reduced laryngeal elevation (46). Suggested causes for oropharyngeal dysphagia in COPD are muscle fatigue of the upper aerodigestive tract, alterations in airway protective mechanisms, and anxiousness (16). A lack of reciprocity between respiration and deglutition has been suggested as one of the mechanisms that can induce swallowing impairments in patients with COPD (47, 48).
In summary, when compared with healthy control subjects, patients with COPD were more likely to swallow a bolus that required mastication during inhalation and were more likely to swallow a semisolid at a low Vt and with a shortened DDA and subsequent inhalation after the swallow. The observed impaired breathing and swallowing patterns in the patients with COPD suggests a possible explanation for the presence of dysphagia in persons who do not have neurologic illness. Unrecognized prandial aspiration before or during COPD exacerbation may also contribute to the severity of the exacerbations.
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