Rationale: Malnutrition and aspiration are major problems in patients with neuromuscular disease. Because impaired swallowing contributes to malnutrition, means of improving swallowing are needed.
Objectives: To investigate interactions between breathing and swallowing in neuromuscular disorders and to evaluate the impact of mechanical ventilation (MV) on swallowing in tracheostomized patients.
Methods: We studied 10 healthy individuals and 29 patients with neuromuscular disease and chronic respiratory failure (including 19 with tracheostomy). The tracheostomized patients who could breathe spontaneously were recorded during spontaneous breathing (SB) and with MV, in random order.
Measurements and Main Results: Breathing–swallowing interactions were investigated by chin electromyography and inductive respiratory plethysmography, using three water-bolus sizes (5, 10, and 15 ml) in random order. In contrast to healthy individuals, neuromuscular patients showed piecemeal deglutition with several swallows over several breathing cycles for each bolus. The percentage of swallows followed by expiration was about 50% in the patients compared with nearly 100% in the control subjects. The number of swallows and total swallowing time per bolus correlated significantly to maximal inspiratory pressure. In the 10 tracheostomized patients who were recorded both in SB and MV, the number of swallows and total swallowing time per bolus were significantly reduced during MV compared with SB.
Conclusion: Neuromuscular patients showed abnormal breathing–swallowing interactions, which correlated to maximal inspiratory pressure. Moreover, MV improved the swallowing parameters in tracheostomized patients who were able to breathe spontaneously.
Malnutrition is common in patients with neuromuscular disease. Impaired swallowing jeopardizes the patient's ability to meet intake needs.
In neuromuscular patients, deglutition is fragmented in several swallows over several breathing cycles. Swallowing parameters are better in tracheostomized patients when they are under mechanical ventilation than in spontaneous breathing.
Little is known about interactions between swallowing and breathing in patients with neuromuscular disorders (4). Swallowing–breathing interactions must be evaluated in each of the breathing conditions encountered in patients with neuromuscular disease, as follows: spontaneous breathing (SB) (5), noninvasive MV (NIV) (6–9), tracheostomy with SB (10, 11), and tracheostomy with MV (10, 12, 13). Few data are available on swallowing in neuromuscular patients who breathe spontaneously or use NIV. NIV is generally used only during sleep, so that patients in this group usually eat without ventilatory assistance (1). Whether tracheostomized patients should use the ventilator during meals remains controversial. Patients who are not completely dependent on MV may prefer to be off their machine during meals, for social reasons or to continue their pretracheostomy habits. Tracheostomized patients on an assist-control mode of MV cannot prolong their expiratory period, and during meals the ventilator determines whether expiration or inspiration occurs after swallowing. Swallowing in normal individuals is nearly always followed by expiration (14–16), a pattern that may contribute to prevention of aspiration.
The main objective of our study was to evaluate swallowing–breathing interactions in a population of neuromuscular patients who exhibited different degrees of disability. Our secondary objective was to assess the influence of MV during swallowing in tracheostomized patients who were incompletely dependent on MV.
Details on methods are available in the online supplement.
We studied 10 healthy volunteers and 29 consecutive patients who had neuromuscular disorders responsible for respiratory muscle weakness with a vital capacity (VC) less than 60% but no episodes of acute respiratory failure within the last 2 mo. Patients were recruited during routine follow-up visits at the Raymond Poincaré teaching hospital, whereas healthy volunteers were recruited among hospital staff members. The healthy volunteers had no history of dysphagia or pulmonary disease. All study participants provided informed consent. The study was approved by the relevant ethics committee (Hôpital Ambroise Paré, Paris, France).
Dysphagia was graded into three clinical grades (17). Locomotor function was evaluated using the Hauser Ambulatory Index (18). Spirometry was performed in the sitting position in all study participants and in the supine position in a subset of the patients (19). Maximal inspiratory pressure (MIP), maximal expiratory pressure (MEP) (20), and arterial blood gas levels were measured in all study participants. Several clinical and laboratory parameters reflecting nutritional status were collected. An otolaryngologist examined all the study participants.
For respiratory parameter measurements, thoracic and abdominal movements were monitored using respiratory inductive plethysmography (Respitrace; Ambulatory Monitoring, Ardsley, NY), as described in detail in the online supplement. Swallowing was monitored noninvasively, using electromyography (EMG) to detect submental muscle activity via skin-surface electrodes on the chin and a piezoelectric sensor placed between the cricoid and thyroid cartilages on the midline to detect laryngeal motion (21). All signals were digitized and recorded directly on a personal computer equipped with the MP 100 data-acquisition system (Biopac Systems, Goleta, CA). The system software (AcqKnowledge) was configured so that EMG signals, laryngeal movements, and thoracic and abdominal movements were displayed simultaneously on separate channels.
The study participant was seated comfortably, and the experiment was started after a period of quiet breathing. The head was maintained in the neutral position to avoid bias due to effects of position on swallowing (22). Water boluses were placed in the mouth using a syringe. Three bolus sizes were used (5, 10, and 15 ml), in random order. Four sets of three boluses were studied, taking care not to use the same bolus size twice consecutively. The study participants were blinded to bolus size. They were instructed to swallow normally while trying to be as efficient as possible. In the 10 tracheostomized patients who could breathe spontaneously, swallowing was tested during SB and MV, in random order. SB was tested with the patient's usual uncuffed tube (see Table E1 of the online supplement) and a one-way valve (Rusch 506500; Willy Rusch AG, Kermen, Germany). In this subgroup of patients, the Borg scale score (23) was determined at the end of each condition to evaluate the influence of the breathing condition on dyspnea.
Swallowing onset was defined as the onset of phasic submental EMG activity and swallowing termination as the beginning of the downward laryngeal movement detected by the piezoelectric sensor (21). For each bolus size, we recorded the duration of swallowing, number of swallows, and number of ventilatory cycles. Respiratory movement direction (inspiration or expiration) immediately before and after each swallow was recorded, and for each patient the percentages of swallows preceded by expiration and swallows followed by expiration were computed.
For each subject and each bolus size, the mean value of the four trials was calculated. All results are reported as means ± SD in the tables and as means ± SEM in the figures. Statistical tests were run using the Stat View 5 package (SAS Institute, Grenoble, France).
Group comparisons were based on data obtained during SB (the most physiological condition), except in the eight tracheostomized patients who were completely dependent on the ventilator. Two-way (group effect and bolus-size effect) analysis of variance (ANOVA) with repeated measures on volume was used.
To determine the influence in the patients of each disability parameter (Hauser Ambulatory Index, MEP, MIP, VC, PaCO2, and dysphagia) and of tracheostomy on swallowing performance, least-squares linear regression analysis was performed between the disability parameters and the swallowing parameters with the largest bolus that all the patients were able to swallow (24). Univariate analysis was used to evaluate the independent contribution of each variable. Full-model, stepwise, multiple linear regression analysis was then performed to determine the influence of each variable (24).
In the tracheostomized patients who were recorded during both SB and MV, these two conditions were compared using two-way (ventilatory-condition effect and bolus-size effect) ANOVA with repeated measures (24). p values less than 0.05 were considered statistically significant.
Tables 1 and 2 report the characteristics of the 10 healthy volunteers and 29 neuromuscular patients included in the study (see also Table E1). No abnormal anatomic obstruction of the upper airway or severe maxillofacial deformity was observed. MV was consistently used in assist-control mode. All 19 tracheostomized patients used an uncuffed tracheostomy tube (see Table E1). At the beginning of MV, the tidal volume was set between 10 and 12 ml/kg and the backup respiratory rate was set two to three breaths per minute below the awake respiratory rate during SB, according to published recommendations (9, 25). Subsequently, tidal volume was adjusted to obtain normocapnia during MV.
Duration of Mechanical Ventilation (h/d)
VC, Sitting (%)
AI (out of 9)
Of the 19 tracheostomized patients, 11 were able to breathe spontaneously for at least 2 h/d. One patient who was able to breathe spontaneously refused to use MV during the trial. Therefore, 10 patients were investigated during both SB and MV. During meals, 4 of these 10 patients used MV, 4 breathed spontaneously, and 2 used MV or SB.
One tracheostomized patient who could breathe spontaneously and two tracheostomized patients who were completely dependent on the ventilator were unable to swallow the largest bolus (15 ml). Therefore, they could not be included in the ANOVA.
The healthy volunteers usually required a single swallow per bolus (see Figure 1A). In contrast, piecemeal deglutition occurred in the patients, with each bolus often requiring several swallows over several breathing cycles (see Figure 1B). The total bolus swallowing time was significantly shorter and the numbers of swallows and breathing cycles per bolus were significantly smaller in the healthy volunteers than in the patients (p < 0.0001, p = 0.0004, and p = 0.0007, respectively; ANOVA) (Figures 2A–2C). Increasing the size of the bolus significantly increased the duration of swallowing and the number of swallows but not the number of breathing cycles (p < 0.0001, p < 0.0001, and p = 0.98, respectively; ANOVA).
The percentage of swallows preceded by expiration was not different between the healthy control subjects and the patients (p = 0.18, ANOVA). The percentage of swallows followed by expiration differed between the healthy control subjects and patients (p < 0.0001, ANOVA) but was not significantly influenced by bolus size (p = 0.21, ANOVA) (Figure 2D). Expiration occurred after nearly all swallows in the healthy control subjects, compared with only about 50% of swallows in the patients.
The percentage of swallows followed by expiration was not correlated with any of the variables reflecting disability severity (all p values > 0.15). Correlations between other swallowing parameters and the disability variables are shown in Table 3. MIP and MEP correlated with the swallowing variables, but the dysphagia index and Hauser ambulatory index did not.
Duration of Swallowing
Number of Swallows
Number of Breathing Cycles
|Coefficient||R2||p Value||Coefficient||R2||p Value||Coefficient||R2||p Value|
The influence of tracheostomy on swallowing variables is reported in Table 4. Tracheostomy significantly affected the number of swallows per bolus (p = 0.022), the number of breathing cycles per bolus (p = 0.019), and the duration of swallowing (p = 0.048).
No Tracheostomy (n = 10)
Tracheostomy (n = 19)
|Duration of swallowing, s||3.1 ± 1.9||4.7 ± 2.0*|
|Number of swallows||1.7 ± 1.0||2.7 ± 1.0*|
|Number of breathing cycles||1.3 ± 0.4||2.0 ± 0.9*|
In a stepwise regression analysis using the variables that correlated significantly with the swallowing parameters, only MIP contributed to swallowing parameter variances (number of swallows: R2 = 0.309, p = 0.002; number of breathing cycles: R2 = 0.306, p = 0.002; and duration of swallowing: R2=0.223, p = 0.01).
In the 10 tracheostomized patients for whom recordings were obtained in both conditions, MV was consistently associated with shorter swallowing times per bolus and fewer swallows per bolus, compared with SB. Individual results with the largest bolus (15 ml) are shown in Figure 3. Interestingly, the patient who could not swallow the largest bolus while breathing spontaneously accomplished this task successfully while on MV (Figure 3). Figure 4A further illustrates the decrease in the number of swallows per bolus seen with MV compared with SB (p = 0.0007, ANOVA). This smaller number of swallows translated into a shorter swallowing time per bolus with MV than with SB (p= 0.0001, ANOVA) (Figure 4B). PaCO2 was lower with MV than with SB (p = 0.0079, ANOVA). The Borg scale score was significantly lower during MV than during SB (p = 0.0144, ANOVA) (Figure 3C).
Our physiological study showed differences in swallowing–breathing interactions between healthy volunteers and neuromuscular patients with chronic respiratory failure. In the patients, several swallows spread over several breathing cycles were needed for each water bolus. In addition, nearly half the swallows in the patients were followed by inspiration, a pattern that was extremely rare in the healthy volunteers. In the tracheostomized patients capable of breathing spontaneously, MV reduced both the swallowing time per bolus and the number of swallows per bolus. Before discussing these physiological results and their potential implications, we will address a number of methodologic issues.
We used a noninvasive method to explore swallowing. We did not use nasofibroscopy or needle-EMG of the cricopharyngeal muscle. A previous study established that the period between the two deflections of the laryngeal sensor corresponded to glottis closure as documented by invasive EMG of the thyroarytenoid muscle (26). In addition, the first deflection of the laryngeal sensor coincided with opening of the upper esophageal sphincter as detected by cricopharyngeal EMG relaxation, and this coordination was lost only in patients who had corticobulbar involvement (21, 27). None of our patients had corticobulbar disease. Moreover, our method did not require direct connection of measurement devices to the airway. Thus, the noninvasive method used in our study did not interfere with swallowing or with the swallowing–breathing interaction.
Because our objective was to obtain data relevant to meals, we evaluated volitional swallowing as opposed to spontaneous/automatic swallowing. Accordingly, the study participants chose when to initiate swallowing once the bolus of water was placed in the mouth. However, because in our physiological study the participants were investigated in the neutral position, we were unable to evaluate potential compensatory positions that might influence swallowing parameters.
Water was used in our study to investigate swallowing. This may explain why no correlation was found between the swallowing parameters and the dysphagia grade, as our patients tolerated water better than semisolid or solid foods. However, water was used in most of the previous studies (4, 14, 28, 29), which allowed us to compare our results with earlier data. Chewing, which influences nutrition in neuromuscular patients, did not occur in our study. Finally, our method did not ensure detection of aspiration. However, we used a previously described method for which normal values were available (30, 31). None of our patients had values within the normal range.
At our hospital, uncuffed tracheostomy is used in neuromuscular patients to improve comfort and speech (32). Our finding that tracheostomy influenced swallowing performance suggests an effect of the material conditions of tracheostomy on swallowing. We continued to use uncuffed tubes, because studies have shown no effect of cuff status on aspiration (33, 34). Moreover, because Suiter and colleagues (34) observed that cuff deflation using a one-way valve improved swallowing and reduced aspiration frequency, we added a one-way valve when patients were studied in SB.
Although DMD and Becker's muscular dystrophy predominated in our population (15 of 29 patients), a wide range of neuromuscular disorders was represented. However, none of our patients had cerebral or bulbar involvement and/or rapidly progressive diseases, such as myotonic dystrophy or amyotrophic lateral sclerosis.
Several studies focused on swallowing neurophysiology in normal individuals and in patients with neuromuscular disorders. Ertekin and colleagues (21, 27) showed that noninvasive evaluation of swallowing using submental EMG activity and laryngeal motion detection by a piezoelectric sensor was specific and sensitive for evaluating oropharyngeal dysphagia. With this method, Ertekin and Aydogdu (27) found that water boluses of 20 ml or less were never associated with piecemeal deglutition in normal individuals. In studies of the oropharyngeal phase of swallowing in 18 patients with myotonic dystrophy (31) and in 25 patients with myasthenia gravis (35), Ertekin and colleagues noted that impaired laryngeal elevation and bolus propulsion to the esophagus was often the main abnormality. In these patients, the pharyngeal phase was often prolonged. Similarly to Ertekin and colleagues (21), we noted piecemeal deglutition in our neuromuscular patients. In addition, swallowing was spread over several breathing cycles and nearly half the swallows were followed by inspiration, a pattern that was virtually nonexistent among healthy individuals (15, 29, 36–38).
The interaction between swallowing and breathing was evaluated by Paydarfar and coworkers in 30 healthy subjects (16) and Nishino and colleagues in 8 healthy subjects (14). The results showed that most swallows started during expiration and were followed by expiration, a pattern believed to contribute to airway protection during swallowing (4, 28). The mechanism involved in swallowing–breathing coordination is not fully understood. Nishino and colleagues showed that this coordination was partly maintained in unconscious patients, indicating a role for neural mechanisms in addition to behavioral factors (36). Furthermore, both the respiratory center and the central pattern of deglutition are located in the brainstem, where they share the same structures.
Our results are in agreement with a previous study (4) showing that swallows were more often followed by inspiration in patients with brain, spinal cord, and peripheral neurologic disorders. In healthy individuals, the occurrence of inspiration after swallows was increased by hypercapnia (39) or application of an inspiratory elastic load (28). In addition, laryngeal irritation was significantly more common with elastic loading compared with baseline, suggesting that inspiration after swallowing was associated with aspiration (28). Our patients with neuromuscular disorders had hypercapnia and probably an increased elastic load (40, 41), and about half their swallows were followed by inspiration. Conceivably, this abnormal swallowing–breathing pattern may be related to a respiratory drive increase in these patients with chronic respiratory failure, compared with healthy individuals.
In keeping with previous studies (14, 15, 37), we found that our healthy volunteers needed a single breathing cycle (and usually a single swallow) for water boluses smaller than 20 ml, whereas the patients needed several cycles. Although a larger number of respiratory cycles per bolus would be expected to increase the risk of aspiration, as the patient must take in air while holding material in the oropharyngeal cavity, we did not observe any correlation between the swallowing parameters and the dysphagia grade. In fact, most of our patients (n = 18) had no signs or symptoms of dysphagia. However, clinical evaluation of dysphagia may underestimate the frequency of aspiration as detected by an objective method (42). In addition, we investigated swallowing of water boluses, which are not as effective as solids for detecting dysphagia. The abnormalities detected in this physiological study probably explain the prolonged swallowing during meals described by neuromuscular patients, which is known to increase the risk of malnutrition (1, 2). Swallowing parameters correlated to respiratory muscle performance, suggesting that the swallowing abnormalities originated in upper airway muscle weakness. Weakness of the upper airway muscles may be similar to weakness of the respiratory muscles, as the main muscles involved in the oropharyngeal phase of swallowing share many physiological features with the inspiratory muscles (43). The other hypothesis is that the abnormal swallowing behavior described in this study is merely a direct consequence of respiratory failure and therefore could be improved by symptomatic treatment such as MV.
In the 10 tracheostomized patients who were studied during both SB and MV, MV decreased both the swallowing time per bolus and the number of swallows per bolus, compared with SB. These differences occurred regardless of the usual eating pattern (with MV, with SB, or with either MV or SB). Several hypotheses can be put forward to explain the improvements seen with MV. First, swallowing probably increased the work of the respiratory muscles, whereas MV had the opposite effect, allowing the upper airway muscles to serve only for swallowing. Second, some patients experience anxiety during SB. Alleviation of anxiety related to the use of MV may improve swallowing. Third, patients do not have to control their breathing while using MV and can therefore concentrate on swallowing, which may improve swallowing performance. Fourth, MV maintains a positive subglottic pressure throughout the breathing cycle, which reduces the risk of aspiration and may improve swallowing (44). Finally, hypercapnia may alter swallowing performance (39) and is corrected by MV.
Vitacca and colleagues (45) reported that tracheostomized patients who had severe obstructive pulmonary disease and MV weaning difficulties experienced dyspnea during SB and should therefore use MV during meals. Our patients were routinely asked about dyspnea during meals. None reported severe dyspnea, in keeping with the reported decrease in the perception of inspiratory difficulties by neuromuscular patients (46). However, the patients who were investigated both with SB and with MV had significantly lower Borg scale values during MV than during SB (Figure 3C). Finally, we agree with Vitacca and coworkers (45) that MV may be in order during swallowing in tracheostomized patients. SB could be used during more passive daytime periods.
In summary, patients with neuromuscular disorders exhibited piecemeal deglutition leading to an increase in the time needed to swallow a water bolus, as well as occurrence of inspiration after nearly half the swallows. These abnormalities, which correlated with the reduction in respiratory muscle performance, may explain feeding difficulties. In tracheostomized patients who could breathe spontaneously, piecemeal deglutition and swallowing time per bolus were diminished by the use of MV. Further clinical studies are needed to evaluate the impact of MV during an entire meal and to confirm the suggestion that MV should be recommended during meals.
The authors thank Line Falaize and Alain Louis for their skillful technical assistance.
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