ABSTRACT
Objective
The aim of this study was to evaluate the respiratory‐swallow coordination (RSC) in healthy, dysphagic, and subjects with blocked, unblocked or without tracheostomy cannula (TC) over 2 h with focus on unintended deglutition.
Methods
In a single center (cross‐sectional) observational study, a total of 65 subjects were included. Swallowing processes were recorded using RehaIngest (Hasomed GmbH, Magdeburg, Germany), combining electromyography (EMG) and bioimpedance (BI) inputs. Group differences were calculated using non‐parametric tests, the influences of age and gender were evaluated using regression analysis.
Results
Respiratory patterns from 3761 swallows were evaluated. Nineteen healthy and 46 dysphagic subjects, including 15 without TC, 15 with blocked TC and 16 with unblocked TC, were recorded. In the dysphagia cohort unblocked and without TC demonstrated increased post‐deglutitive expiration (p = 0.012, p = 0.001) and a decrease in post‐deglutitive inspiration (p = 0.028, p = 0.013) compared with healthy probands. In addition, a higher proportion of subjects demonstrating post‐deglutitive expiration was recorded amongst probands with unblocked TC compared to blocked TC (p = 0.012). Neither age nor gender significantly impacted the aforementioned outcomes.
Conclusion
Our novel cross‐sectional study shows that the RSC adapts in a compensatory fashion in the acquired dysphagia cohort. The adaptation depends on the occurrence of dysphagia and the type of TC. If the TC cuff is blocked, patients likely have an inadequate adaptation of the RSC, mainly because of the absence of a transglottic air flow. These findings indicate that RSC and TC care should be closely incorporated into clinical routine to improve dysphagia therapy.
Level of Evidence
1
Keywords: dysphagia/swallowing, respiratory‐swallow coordination, swallow therapy
The aim of this study was to evaluate the respiratory‐swallow coordination (RSC) in healthy, dysphagic, and subjects with blocked, unblocked, or without tracheostomy cannula (TC) over 2 h with a novel focus on unintended deglutition. Sixty‐five subjects were included, respiratory patterns from 3761 swallows were evaluated, in which we could show an adaptation of the RSC in the acquired dysphagia cohort, which depends on the occurrence of dysphagia and the type of TC. This information indicates that TC care should be incorporated into daily therapy and clinical routines to restore respiratory function.
1. Introduction
The understanding of the complex processes and the significance of respiratory‐swallow coordination (RSC) has been the subject of ongoing investigation in recent years. Previous studies focused on intentional swallows being triggered within examination conditions using liquid or solid food boluses. Evaluation took place using videofluoroscopic or endoscopic assessment paired with respiratory cycle detection [1, 2, 3, 4, 5, 6, 7, 8]. An uniform pattern of RSC could not be found, several studies showed a high degree of variability between healthy subjects [2, 9, 10, 11, 12, 13, 14]. Nevertheless, the most common pattern reported was expiration before and after swallowing, which was interpreted as being physiological [2, 6, 8, 12, 15]. It has been hypothesized that peri‐deglutitive expiration serves a protective function due to increased subglottic pressure during swallowing and generating a countercurrent that prevents aspiration [9, 16].
Uncued swallows, which are primarily responsible for the gastric deposition of saliva, account for the largest proportion of daily swallows [17]. The investigation of the RSC of these is yet to be conclusively researched due to shortcomings in examination modalities. The RehaIngest (Hasomed, Magdeburg) is a novel mobile device that can reliably detect and record swallowing processes based on EMG signals and changes in bioimpedance in the pharynx while simultaneously recording respiratory excursions [18]. Thus measurement data can be collected unobserved over several hours and extracted for analysis.
The aim of the present study was to continuously record the RSC of uncued swallows in healthy subjects and patients with a swallowing disorder with blocked, unblocked and without a tracheostomy cannula (TC) over a period of at least 2 h.
2. Material and Methods
2.1. Study Design
This cross‐sectional single‐center study was approved by the Institutional Review Board of the Charité Berlin Ethics Committee (EA 1/068/19) and registered in the German Clinical Study Register (DRKS00016952). Sixty‐five adult subjects were included in this study between September 2019 and February 2020.
2.2. Data Collection Device
The measurement data were collected using the RehaIngest device (Hasomed GmbH, Magdeburg, Germany) to identify swallowing processes in combination with abdominal and chest respiratory belts to evaluate corresponding breathing patterns.
2.3. Data Collection, Inclusion Criteria
Adult patients with diagnosed dysphagia were selected on an interdisciplinary basis in consultation with colleagues from the speech therapy department. Healthy subjects were examined after a swallowing disorder was ruled out. Data collection was carried out, the demographic data and the corresponding grouping took place before the respective measurements. Healthy subjects (n = 19) and dysphagic subjects with blocked (n = 15), unblocked (n = 15), and without (n = 16) TC were studied. Exclusion criteria were a reduction in vigilance, clinical or laboratory signs of an infection, age under 18 years, lack of consent and pregnancy.
2.4. Data Acquisition and Statistical Analysis
Patients were informed in detail about the examination and signed a written consent form. Data collection with RehaIngest was carried out using BI and EMG with a high sensitivity and specificity for identification of swallowing processes [18]. Therefore, cervical electrodes were placed according to the positioning pattern described by Schultheiss et al. [18]. Measurement took place over at least 2 h to detect spontaneous swallows with simultaneous evaluation of the respiratory maneuvers using chest and abdominal belts. No speech therapy or therapeutic intervention was performed during recording. The participants were allowed to move according to their abilities.
After the data were exported from the measuring device, swallows and corresponding breathing maneuvers were marked on a graphical plot [18]. For the description of RSC, six breathing patterns were defined from pre‐ or post‐deglutitive breathing activity with inspiration, expiration, and apnea. The data were statistically evaluated using SPSS Statistics (IBM SPSS Statistics 25, 2021). Demographic data were described as mean ± standard errors. Categorical and continuous variables were described as median ± standard error and analyzed using Mann–Whitney U tests. The impact of age and gender on the corresponding group differences was evaluated using regression analysis. All p variables were two‐tailed with a significance level of p < 0.05.
3. Results
Between September 2019 and February 2020, 65 patients were enrolled in the study, 68% of them male (n = 44), and 32% female (n = 21). In addition to 19 healthy people, 22 subjects with neurological diseases, 12 with cervical spinal cord injuries, 2 patients from the ENT department and some others for example after prolonged mechanical ventilation were included. The median age was 64.0 (IQR: 52.0–76.0) years ranging from 29 to 85. A total of 3761 swallows within 12,003 min and corresponding breathing patterns were evaluated, the median swallowing frequency in all groups was 1.12 swallows per 5 min. The median recording time was 180 min (IQR: 130–240) min per subject, with a minimum of 120 min and a maximum of 270 min (Table 1).
TABLE 1.
Parameters of the groups.
| Groups | Mean age in years (IQR) | Gender female/male n (%) | Mean number of swallows (IQR) | Swallowing frequency, mean swallows/5 min (IQR) | Mean recording time in minutes (IQR) |
|---|---|---|---|---|---|
|
Healthy |
50.0 | 12 (63.0)/ | 41.0 | 1.33 | 180 |
|
n = 19 | |||||
| (34.0–65.0) | 7 (37.0) | (29.0–78.0) | (0.85–2.18) | (125–180) | |
|
Without TC |
64.0 | 4 (25.0)/ | 40.0 | 1.11 | 180 |
|
n = 16 | |||||
| (64.0–76.0) | 12 (75.0) | (33.0–80.0) | (0.93–2.54) | (130–224) | |
|
TC blocked n = 15 |
79.0 | 4 (26.7)/ | 41.5 | 1.01 | 240 |
| (71.3–80.5) | 11 (73.3) | (30.0–78.8) | (0.83–1.01) | (170–240) | |
|
TC unblocked |
64.0 | 2 (13.3)/ | 35.0 | 0,87 | 208 |
|
n = 15 | |||||
| (62.0–68.0) | 13 (86.7) | (23.0–85.0) | (0.58–2.23) | (125–240) | |
|
Total n = 65 |
64.0 | 21 (32.3)/ | 40.0 | 1.12 | 180 |
| (52.0–76.0) | 44 (67.7) | (29.0–79.0) | (0.78–2.18) | (130–240) |
In healthy individuals (n = 19), the breathing pattern of pre‐ and post‐deglutitive inspiration (IN/IN) was shown to be the most common with 31.4% (IQR: 25.0–36.0), followed by EX/EX with 20.0% (IQR: 15.0–29.2) and EX/IN with 12.2% (IQR: 6.2–22.9). In dysphagic subjects without TC, the IN/IN breathing pattern was also the most frequent one at 23.7% (IQR: 11.5–37.5). This was followed by EX/EX with 24.6% (IQR: 12.5–27.6) and IN/EX with 15.1% (IQR: 11 0.1–29.7). Amongst dysphagic subjects with a blocked TC, the breathing patterns IN/IN, EX/IN, IN/EX, and EX/EX were found with 23.9% (IQR: 15.9–27.7), 17.6% (IQR: 9.4–25.1), 17.4% (IQR: 5.2–23.6), and 15.4% (IQR: 11.7–19.4). Amongst dysphagic subjects with an unblocked TC, the breathing patterns EX/EX, IN/IN, and IN/EX represented 24.3% (IQR: 22.2–28.6), 23.6% (IQR: 13.8–30.0), and 16.4% (IQR: 10.0–26.3), respectively.
In a separate analysis, the aforementioned clinical groups, healthy, dysphagic with blocked, unblocked and without TC, were then stratified according to their respective pre‐ and post‐ deglutition breathing phases (Table 2). Again, inspiration was found to be the most common breathing pattern in healthy subjects at 44% before and 50% after swallowing, followed by expiration at 40% and 37%. In contrast, the proportion of post‐deglutitive expiration significantly increased in subjects with dysphagia without (p = 0.028) and with unblocked TC (p = 0.007) compared to healthy subjects (Table 3). In addition, post‐deglutitive expiration was found to occur more frequent in patients with unblocked TC than with a blocked TC (p = 0.021) (Figure 1). In contrast to this, post‐deglutitive inspiration showed a significant decrease in patients with dysphagia without and with unblocked TC (p = 0.037 vs. p = 0.022) compared to healthy subjects (Figure 2). This difference could not be demonstrated in patients with blocked TC (p = 0.389). Furthermore, no differences between the pre‐deglutitive respiratory groups could be found. An impact of age and gender on the group differences was evaluated using regression analysis and could not be shown.
TABLE 2.
Composition of the respiratory groups.
| Respiratory groups | Biphasic breathing pattern | |
|---|---|---|
| Post‐deglutitive | Inspiration | IN/IN, EX/IN, AP/IN |
| Expiration | IN/EX, EX/EX, AP/EX | |
| Apnea | IN/AP, EX/AP, AP/AP | |
| Pre‐deglutitive | Inspiration | IN/IN, IN/EX, IN/AP |
| Expiration | EX/IN, EX/EX, EX/AP | |
| Apnea | AP/IN, AP/EX, AP/AP | |
TABLE 3.
Pre‐ and post‐deglutitive respiratory groups.
| Groups | Respiratory groups in %, median (IQR) | |||||
|---|---|---|---|---|---|---|
| Pre‐deglutitive | Post‐deglutitive | |||||
| Inspiration | Expiration | Apnea | Inspiration | Expiration | Apnea | |
|
Healthy n = 19 |
44.0 (34.5–51.4) |
40.0 (34.6–42.9) |
13.5 (5.7–23.3) |
50.0 (42.3–58.4) |
37.1 (24.4–40.0) |
13.9 (8.0–23.6) |
|
Without TC n = 16 |
48,7 (36.9–55.4) |
39.5 (35,1–43.5) |
13.0 (9.2–23.1) |
39.5 (34.5–50.0)* |
44.8 (37.0‐52.2)* |
13,2 (8.1‐22.8) |
|
TC blocked n = 15 |
45.3 (29.4–49.5) |
39.0 (34.9–48.8) |
18.5 (9.9–26.6) |
44.1 (33.8–63.6) |
34.7 (19.4–45.0)** |
14.3 (5.9‐27.9) |
|
TC unblocked n = 15 |
44.4 (38.1–48.6) |
41.4 (36.4–50.0) |
11.1 (3.7–17.5) |
40.0 (26.3–50.0)* |
48.2 (35.0‐62.1)* |
10.5 (7.4‐16.7) |
|
Total n = 65 |
45.2 (35.9–51.4) |
40.0 (35.3–46.0) |
13.5 (8.0–22.0) |
44.4 (35.3–54.0) |
40.0 (26.1–50.3) |
13,8 (7.7–23.2) |
Significant differences within the respiratory group compared to healthy subjects (Mann–Whitney U test), each p < 0.05.
Significant differences compared to patients with unblocked TC (Mann–Whitney U test), p = 0.021.
FIGURE 1.
Post‐deglutitive expiration of groups.
FIGURE 2.
Post‐deglutitive inspiration of groups.
4. Discussion
Research into RSC continues to be a complex topic in current research. To our knowledge, this is the first study, that evaluates RSC of spontaneous, unobserved swallows in healthy individuals and patients with dysphagia, tracheotomized as well as non‐tracheotomized, over a longer period of time. For data collection, RehaIngest was used, a validated measuring device to detect swallowing processes using EMG and bioimpedance. In combination with a breathing belt, recording of the corresponding breathing maneuvers was possible [19]. In healthy individuals, the pattern of pre‐ and post‐deglutitive inspiration was shown to be the most common. Previous literature has identified pre‐ and post‐deglutitive expiration as the most common respiratory pattern in cued swallows [2, 6, 8, 13, 15]. To date, pre‐ and post‐deglutitive inspiration has been associated with an increased risk of aspiration [12, 20]. Smith et al. were able to demonstrate an increased proportion of inspiration during oral intake compared to the rest phase [21]. This has also been shown in patients with COPD when ingesting larger boluses of food [22]. Martin‐Harris et al. reported increased post‐deglutitive inspiration with increasing age in healthy subjects as a reason for increased aspiration risk [6]. This is thought to be due to negative endotracheal pressure and the resulting drag effect [20]. In addition, post‐deglutitive expiration enables an adequate cough in terms of aspiration prophylaxis. If the respiratory volume is missing due to exhalation before swallowing, coughing is only possible to a limited extent [14]. In our study, we found a high variability of the RSC in pre‐ and post‐deglutitive inspiration and expiration amongst healthy controls. In these, the RSC seems to play a minor role in minimizing aspiration risk due to a well‐developed protective system. According to Martin‐Harris et al., the focus is primarily on four functional units during a physiological swallowing process by which an aspiration protection is usually provided [6, 23]. Additionally, the possibility of developing a profound post‐deglutitive cough is crucial and could be significantly reduced in patients with dysphagia [6, 10, 14, 24, 25].
Differences of breath patterns between the groups occurred in the post‐deglutitive phase only. Expiration was the most common post‐deglutitive breathing pattern in people with dysphagia with unblocked or without TC. Compared with healthy subjects, there was a significantly higher rate of expiration and a reduced rate of inspiration after swallowing (Figure 1). In subjects with blocked TC, the post‐deglutitive breathing patterns were comparable to those of healthy subjects, with a predominance of post‐deglutitive inspiration (Figure 2). This behavior differs significantly from the post‐deglutitive behavior of subjects with an unblocked cannula, in whom expiration predominates.
These results show for the first time, that the RSC automatically adapts to the sensory information, resulting in an increase in protective expiration in dysphagia. A subglottic pressure build‐up, which is generated based on a positive residual expiratory lung volume during swallowing, plays a key role in terms of aspiration protection [2, 6, 10, 16]. This is increasingly present at the beginning of the swallowing process and can be demonstrated to be persistently increased over the course of the swallowing process [26]. Martin‐Harris et al. were able to show that the breathing maneuver is resumed before the swallowing process is completed [6]. In this way, food components that are still in the area of the hypopharynx and laryngeal vestibule can be removed by the expiratory airflow [6, 10, 15, 24, 27]. Adjustment of the RSC during dysphagia appears to be a result of neurophysiological control of the RSC. Vovka et al. were able to show an influence on the RSC by stimulation of the swallowing centers in the brainstem during the pharyngeal phase, which increased post‐deglutitive expiration [28].
Post‐deglutitive inspiration was found less frequently in subjects at risk of aspiration with dysphagia without and with unblocked TC than in healthy subjects. Here, too, an adjustment of the RSC can be assumed due to a reduced post‐deglutitive inspiration rate, which leads to a lower risk of aspiration [14, 24, 29].
Furthermore, breathing pattern of subjects with blocked TC was different to subjects with a unblocked or without TC and comparable to heathy controls. Due to the blocked cuff in the trachea, the airflow occurs exclusively via the TC, bypassing the larynx. As a result, there is a reduction in sensitivity in the larynx and pharynx with reduced perception of saliva and food [30, 31, 32]. This seems to be an aspect of a lack of adaptation of the RSC. In addition, there is no subglottic pressure build‐up to produce a proper cough due to the blocked TC, resulting in less frequent post‐deglutitive expiration.
The present results show, that TC management is of great importance in the context of dysphagia therapy. The aim of dysphagia therapy is to restore a safe swallowing process. This can only be learned if sufficient sensory information is available, that is, there is an air flow passing the larynx, which is not possible with an inserted blocked TC [33, 34, 35, 36].
Limitations of our study are the single center design and the resulting restrictions. In contrast to our study, previous studies have focused on initiated swallowing processes after the application of liquids, semi‐solid or solid food [4]. In our study, we continuously evaluated spontaneous, unobserved swallows over a period of at least 2 h without any patient interaction or observation. Therefore, comparability of the data with regard to the current literature must be seen critically and evaluated on larger amounts of data. Furthermore, in an average of 20.3% of the swallows of the respective subjects, the appropriate respiratory pattern could not be reliably assigned due to insufficient signal recording. Therefore, these specific swallows were excluded from the calculation. In these, no significant differences in the percentage of undetected signals could be found between the groups. However, this proportion could possibly have been reduced by measuring nasal airflow [37], which could not be combined with RehaIngest for technical reasons. Irrespective of this, this would only be practicable to a limited extent in subjects with blocked TC, since a corresponding flow measurement would have to be carried out directly around the TC. Finally, we must admit the relatively small size of the study population, especially after grouping. In this context, the collection of data with larger study populations and meta‐analyses is required.
5. Conclusion
To our knowledge, this study is the first to measure the RSC of uncued swallows for over 2 h. In patients with dysphagia and increased risk of aspiration, post‐deglutitive expiration was shown to be the dominant RSC pattern. In healthy individuals, the RSC is thought to play a minor role concerning risk of aspiration due to unaffected sensory and muscle coordination. In subjects with a blocked TC, the pattern of RSC seems to be maladaptive due to a lack of sensory feedback. Our data should provide an incentive for future clinical studies. Given its importance for preventing aspiration, we support the implementation of routine RSC analysis into clinical routine, particularly amongst dysphagic patients and TC use in dysphagia therapy. Correct TC selection during therapy may help restore protective RSC.
Conflicts of Interest
The authors declare no conflicts of interest.
Funding: The authors received no specific funding for this work.
References
- 1. Preiksaitis H. G. and Mills C. A., “Coordination of Breathing and Swallowing: Effects of Bolus Consistency and Presentation in Normal Adults,” Journal of Applied Physiology 81, no. 4 (1996): 1707–1714. [DOI] [PubMed] [Google Scholar]
- 2. Hårdemark Cedborg A. I., Bodén K., Witt Hedström H., Kuylenstierna R., Ekberg O., and Eriksson L. I., “Breathing and Swallowing in Normal Man—Effects of Changes in Body Position, Bolus Types, and Respiratory Drive,” Neurogastroenterology and Motility 22, no. 11 (2010): 1201‐e316, 10.1111/j.1365-2982.2010.01551.x. [DOI] [PubMed] [Google Scholar]
- 3. Wang C., Chen J., Chuang C., Tseng W., Wong A. M., and Pei Y., “Aging‐Related Changes in Swallowing, and in the Coordination of Swallowing and Respiration Determined by Novel Non‐Invasive Measurement Techniques,” Geriatrics & Gerontology International 15, no. 6 (2015): 736–744. [DOI] [PubMed] [Google Scholar]
- 4. Schultheiss C., Nusser‐Müller‐Busch R., and Seidl R. O., “The Semisolid Bolus Swallow Test for Clinical Diagnosis of Oropharyngeal Dysphagia: A Prospective Randomised Study,” European Archives of Oto‐Rhino‐Laryngology 268 (2011): 1837–1844. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. Boden K., Cedborg A. I. H., Eriksson L. I., Hedström H. W., Kuylenstierna R., and Sundman E., “Swallowing and Respiratory Pattern in Young Healthy Individuals Recorded With High Temporal Resolution,” Neurogastroenterology and Motility 21, no. 11 (November 2009): 1163‐e101. [DOI] [PubMed] [Google Scholar]
- 6. Martin‐Harris B., Brodsky M. B., Michel Y., Ford C. L., Walters B., and Heffner J., “Breathing and Swallowing Dynamics Across the Adult Lifespan,” Archives of Otolaryngology‐Head & Neck Surgery 131, no. 9 (2005): 762, 10.1001/archotol.131.9.762. [DOI] [PubMed] [Google Scholar]
- 7. Preiksaitis H. G., Mayrand S., Robins K., and Diamant N. E., “Coordination of Respiration and Swallowing: Effect of Bolus Volume in Normal Adults,” American Journal of Physiology‐Regulatory, Integrative and Comparative Physiology 263, no. 3 (September 1992): R624–R630. [DOI] [PubMed] [Google Scholar]
- 8. McFarland D. H. and Lund J. P., “Modification of Mastication and Respiration During Swallowing in the Adult Human,” Journal of Neurophysiology 74, no. 4 (1995): 1509–1517, 10.1152/jn.1995.74.4.1509. [DOI] [PubMed] [Google Scholar]
- 9. Charbonneau I., Lund J. P., and McFarland D. H., “Persistence of Respiratory‐Swallowing Coordination After Laryngectomy,” Journal of Speech, Language, and Hearing Research 48, no. 1 (2005): 34–44, 10.1044/1092-4388(2005/004). [DOI] [PubMed] [Google Scholar]
- 10. Gross R. D., Steinhauer K. M., Zajac D. J., and Weissler M. C., “Direct Measurement of Subglottic Air Pressure While Swallowing,” Laryngoscope 116 (2006): 753–761. [DOI] [PubMed] [Google Scholar]
- 11. Kelly B. N., Huckabee M. L., Jones R. D., and Carroll G. J., “The Influence of Volition on Breathing‐Swallowing Coordination in Healthy Adults,” Behavioral Neuroscience 121 (2007): 1174–1179. [DOI] [PubMed] [Google Scholar]
- 12. Dozier T. S., Brodsky M. B., Michel Y., Walters B. C., and Martin‐Harris B., “Coordination of Swallowing and Respiration in Normal Sequential Cup Swallows,” Laryngoscope 116, no. 8 (2006): 1489–1493, 10.1097/01.mlg.0000227724.61801.b4. [DOI] [PubMed] [Google Scholar]
- 13. Hirst L. J., Ford G. A., Gibson G. J., and Wilson J. A., “Swallow‐Induced Alterations in Breathing in Normal Older People,” Dysphagia 17, no. 2 (2002): 152–161, 10.1007/s00455-001-0115-3. [DOI] [PubMed] [Google Scholar]
- 14. McFarland D. H., Martin‐Harris B., Fortin A. J., Humphries K., Hill E., and Armeson K., “Respiratory‐Swallowing Coordination in Normal Subjects: Lung Volume at Swallowing Initiation,” Respiratory Physiology and Neurobiology 234 (2016): 89–96, 10.1016/j.resp.2016.09.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Hopkins‐Rossabi T., Curtis P., Temenak M., Miller C., and Martin‐Harris B., “Respiratory Phase and Lung Volume Patterns During Swallowing in Healthy Adults: A Systematic Review and meta‐Analysis,” Journal of Speech, Language, and Hearing Research 62 (2019): 868–882. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Gross R. D., Carrau R. L., Slivka W. A., Gisser R. G., Smith L. J., and Zajac D. J., “Deglutitive Subglottic Air Pressure and Respiratory System Recoil,” Dysphagia 27 (2012): 452–459. [DOI] [PubMed] [Google Scholar]
- 17. Bulmer J. M., Ewers C., Drinnan M. J., and Ewan V. C., “Evaluation of Spontaneous Swallow Frequency in Healthy People and Those With, or at Risk of Developing, Dysphagia: A Systematic Review and Meta‐Analysis,” [Internet]. In Review; 2021 Jan [zitiert 3. Februar 2021]. Verfügbar unter, https://www.researchsquare.com/article/rs‐153473/v1. [DOI] [PMC free article] [PubMed]
- 18. Schultheiss C., Schauer T., Nahrstaedt H., and Seidl R. O., “Evaluation of an EMG Bioimpedance Measurement System for Recording and Analysing the Pharyngeal Phase of Swallowing,” European Archives of Oto‐Rhino‐Laryngology 270 (2013): 2149–2156. [DOI] [PubMed] [Google Scholar]
- 19. Nahrstaedt H., Schultheiss C., Seidl R. O., and Schauer T., “Swallow Detection Algorithm Based on Bioimpedance and EMG Measurements,” in IFAC Proceedings Volumes (IFAC‐PapersOnline) (2012).
- 20. Kawasaki M., Ogura J. H., and Takenouchi S., “Neurophysiologic Observations of Normal Deglutition. I. Its Relationship to the Respiratory Cycle,” Laryngoscope 74, no. 12 (December 1964): 1747–1765. [DOI] [PubMed] [Google Scholar]
- 21. Smith J., Wolkove N., Colacone A., and Kreisman H., “Coordination of Eating, Drinking and Breathing in Adults,” Chest 96, no. 3 (1989): 578–582. [DOI] [PubMed] [Google Scholar]
- 22. Cvejic L., Harding R., Churchward T., Turton A., Finlay P., and Massey D., “Laryngeal Penetration and Aspiration in Individuals With Stable COPD: Aspiration in COPD,” Respirology 16, no. 2 (February 2011): 269–275. [DOI] [PubMed] [Google Scholar]
- 23. Jacob P., Kahrilas P. J., Logemann J. A., Shah V., and Ha T., “Upper Esophageal Sphincter Opening and Modulation During Swallowing,” Gastroenterology 97, no. 6 (December 1989): 1469–1478. [DOI] [PubMed] [Google Scholar]
- 24. Martin B. J., Logemann J. A., Shaker R., and Dodds W. J., “Coordination Between Respiration and Swallowing: Respiratory Phase Relationships and Temporal Integration,” Journal of Applied Physiology 76, no. 2 (February 1994): 714–723. [DOI] [PubMed] [Google Scholar]
- 25. Shaker R., “Airway Protective Mechanisms: Current Concepts,” Dysphagia 10 (1995): 216–226. [DOI] [PubMed] [Google Scholar]
- 26. Shaker R., Dua K. S., Ren J., Xie P., Funahashi A., and Schapira R. M., “Vocal Cord Closure Pressure During Volitional Swallow and Other Voluntary Tasks,” Dysphagia 17, no. 1 (January 2002): 13–18. [DOI] [PubMed] [Google Scholar]
- 27. Curtis J. A. and Troche M. S., “Effects of Verbal Cueing on Respiratory‐Swallow Patterning, Lung Volume Initiation, and Swallow Apnea Duration in Parkinson's Disease,” Dysphagia 35, no. 3 (June 2020): 460–470. [DOI] [PubMed] [Google Scholar]
- 28. Vovka A., Davenport P. W., Wheeler‐Hegland K., Morris K. F., Sapienza C. M., and Bolser D. C., “Swallow Pattern Generator Reconfiguration of the Respiratory Neural Network,” Perspectives on Swallowing and Swallowing Disorders (Dysphagia) 18, no. 1 (2009): 3–12. [Google Scholar]
- 29. Martin‐Harris B., Brodsky M. B., Price C. C., Michel Y., and Walters B., “Temporal Coordination of Pharyngeal and Laryngeal Dynamics With Breathing During Swallowing: Single Liquid Swallows,” Journal of Applied Physiology 94, no. 5 (2003): 1735–1743. [DOI] [PubMed] [Google Scholar]
- 30. Bogdanov V., Reinhard J., McGlone F., Haehner A., Simons C. T., and Hummel T., “Oral Somatosensory Sensitivity in Patients With Taste Disturbance,” Laryngoscope 131, no. 11 (August 2021): 2572–2577. [DOI] [PubMed] [Google Scholar]
- 31. Seidl R. O., Nusser‐Müller‐Busch R., and Ernst A., “The Influence of Tracheotomy Tubes on the Swallowing Frequency in Neurogenic Dysphagia,” Otolaryngology‐Head and Neck Surgery 132 (2005): 484–486. [DOI] [PubMed] [Google Scholar]
- 32. Tomsen N., Ortega O., Nascimento W., Carrión S., and Clavé P., “Oropharyngeal Dysphagia in Older People Is Associated With Reduced Pharyngeal Sensitivity and Low Substance P and CGRP Concentration in Saliva,” Dysphagia 37, no. 1 (February 2022): 48–57. [DOI] [PubMed] [Google Scholar]
- 33. Tran T. T. A., Harris M. B., and Pearson W. G., “Improvements Resulting From Respiratory‐Swallow Phase Training Visualized in Patient‐Specific Computational Analysis of Swallowing Mechanics,” Computer Methods in Biomechanics and Biomedical Engineering: Imaging and Visualization 6, no. 5 (2018): 532–538. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34. Jakobsen D., Poulsen I., Schultheiss C., Riberholt C. G., Curtis D. J., and Petersen T. H., “The Effect of Intensified Nonverbal Facilitation of Swallowing on Dysphagia After Severe Acquired Brain Injury: A Randomised Controlled Pilot Study,” NeuroRehabilitation 45, no. 4 (2019): 525–536, 10.3233/NRE-192901. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35. Martin‐Harris B., McFarland D., Hill E. G., Strange C. B., Focht K. L., and Wan Z., “Respiratory‐Swallow Training in Patients With Head and Neck Cancer,” Archives of Physical Medicine and Rehabilitation 96, no. 5 (2015): 885–893. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36. McFarland D. H., Harris B. M., and Fortin A. J., “Enhancing Swallowing‐Respiration Coordination,” Current Physical Medicine and Rehabilitation Reports 6, no. 4 (2018): 239–244, 10.1007/s40141-018-0202-0. [DOI] [Google Scholar]
- 37. Montazeri K., Jonsson S. A., Agustsson J. S., Serwatko M., Gislason T., and Arnardottir E. S., “The Design of RIP Belts Impacts the Reliability and Quality of the Measured Respiratory Signals,” Sleep & Breathing 25, no. 3 (2021): 1535–1541. [DOI] [PMC free article] [PubMed] [Google Scholar]