Effects of resistance expiratory muscle strength training in elderly patients with dysphagic stroke

Abstract

BACKGROUND:

Recently, resistance expiratory muscle strength training (EMST) has been reported as a remedial treatment for dysphagia.

OBJECTIVE:

To investigate the effect of resistance EMST on the swallowing function in stroke patients with oropharyngeal dysphagia.

METHODS:

Forty-two stroke patients with dysphagia were randomly assigned to two groups: an experimental group (n = 13) and a placebo group (n = 13). The experimental group performed EMST using a portable EMST device, while the placebo group performed EMST using a sham EMST device with no loading. The intervention was performed 5 days per week for 4weeks, in five sets of 5 breaths through the device for a total of 25 breaths per day. Both groups underwent conventional dysphagia treatment for 30 minutes/day, 5 days/week, for 4 weeks. Videofluoroscopic dysphagia scale (VDS) and penetration-aspiration scale (PAS) based on a videofluoroscopic swallowing study (VFSS) were assessed to analyze the oropharyngeal swallowing function.

RESULTS:

The experimental group showed more improvement in pharyngeal phase of the VDS (p = 0.018 and 0.006, respectively) and PAS compared to the placebo group (p = 0.014).

CONCLUSIONS:

We suggest that EMST could improve the effects of dysphagia observed in post-stroke elderly patients based on swallowing function.

Keywords

Aspiration dysphagia expiratory muscle strength training subacute stroke

1 Introduction

Expiratory muscle strength training (EMST) has been reported as a novel remedial strategy for dysphagia (Park, Oh, Chang, & Kim, 2016; Pitts, Bolser, Rosenbek, Troche, Okun, & Sapienza, 2009). EMST contributes to both ventilatory and non-ventilatory functions, such as coughing, speaking, and swallowing (Kim & Sapienza, 2005). The respiratory system and the swallowing process share various anatomical structures and are both responsible for airway protection (Pitts, Morris, Lindsey, Davenport, Poliacek, & Bolser, 2012). Several studies reported that among the muscles involved in swallowing, the suprahyoid muscles are activated during EMST, and this activation is potentially effective for improving the swallowing function through directed application (Reyes, Cruickshank, Thompson, Ziman, & Nosaka, 2014; Wheeler, Chiara, & Sapienza, 2007).

Recently, some studies have demonstrated the effects of EMST on dysphagia in various neurologic conditions. Troche and colleagues performed 4weeks of EMST in patients with Parkinson’s disease, resulting in improved hyolaryngeal movement and decreased aspiration (Troche et al., 2008). Park and colleagues reported that EMST effectively activated the suprahyoid muscles and strengthened the oral facial muscles in the healthy elderly population (Park et al., 2016). It also demonstrated helpfulness in reducing aspiration in patients with dysphagia.

However, most previous studies analyzed dysphagia in patients with Parkinson’s disease, Huntington’s disease, and multiple sclerosis (Chiara, Martin, Davenport, & Bolser, 2006; Pitts et al., 2009; Reyes, Cruickshank, Nosaka, & Ziman, 2015). For these reasons, studies on elderly patients with dysphagia caused by a stroke are lacking, and clinical evidence of the effect of EMST for dysphagic patients is unclear. Therefore, we investigated the effect of 4-week EMST application on oropharyngeal swallowing function and airway aspiration/penetration in elderly patients with dysphagia caused by a stroke.

2 Methods

2.1 Participants

In total, 30 patients were randomly allocated into either the experimental (n = 15) or the placebo group (n = 15) by blocked randomization to ensure equal number of participants in both groups. The inclusion criteria for participation were as follows: (1) having dysphagia caused by a stroke, confirmed by a videofluoroscopic swallowing study (VFSS), (2) age >65, (3) onset duration of <3 months, (4) a score of ≥ 24 on the Mini-Mental State Examination. Exclusion criteria were the following: (1) presence of severe orofacial pain including trigeminal neuropathy, (2) significant malocclusion or facial asymmetry, (3) unstable breathing and pulse, (4) tracheostomy, (5) communication disorder like severe aphasia and apraxia (6) inadequate lip closure. All participants provided written informed consent, and this study protocol was approved by the university Institution Review Board.

2.2 Sample size calculation

Sample size was calculated using the G-power 3.1 software (University of Dusseldorf, Dusseldorf, Germany). The power and the alpha levels were set at 0.60 and 0.05, respectively, and the effective size was set at 0.8. According to a prior analysis, each group required at least 12 subjects. Therefore, this study included 15 subject in the experimental group and 15 in the placebo group in preparation for drop-out cases.

2.3 Procedure

We measured maximal expiratory pressure (MEP) to determine the EMST threshold value of patients, using a respiratory pressure meter (Micro RPM, Micro Medical-Care Fusion, Kent, UK). Measurement of MEP was done based on the protocols of a previous study (Wheeler et al., 2007). Patients were instructed to maintain upright position on a flat chair and block their noses slightly using a noseclip. Then, measurement was taken by blocking airflow through the nasal cavity. Patients were asked to hold a disposable mouthpiece in their mouth in the state of maximum inhalation and exhale strongly and rapidly. Each participant repeated the maneuver until three trials were achieved within 5% ± of each other.

Participants in the experimental group used a portal Expiratory Muscle Trainer (EMST150. Aspire Products, LLC) and threshold value was set at the 70% range of MEP. For training, patients were asked to open their mouth after inhalation and locate the EMST mouthpiece between the lips before closing mouth. Then, they were instructed to blow strongly and rapidly until the pressure release valve within the EMST device opens. The pressure release valve was set to open if expiratory pressure exceeded targeted pressure set for the device. Evaluators confirmed whether it was successful by listening to the sound of air rushing. Intervention was performed 5 days per week/4weeks, in five sets of 5 breaths through the device for a total of 25 breaths per day. During training, less than a 1 minute break was provided after each session, considering muscle fatigue and dizziness. The placebo group was trained by using a sham EMST device with no loading device. Its exterior is the same as that of an EMST device for the experiment group, but it is a nonfunctional device with little effect of physiologic load on targeted muscles. VFSS was completed before and after the intervention by an experienced physician and occupational therapist blinded to the subjects’ group allocation.

2.4 Outcome measures

The Videofluoroscopic Dysphagia Scale (VDS) is an oropharyngeal swallowing assessment based on the VFSS findings. The VDS is divided into the oral stage (7 items: lip closure, bolus formation, tongue-to-palate contact, mastication, apraxia, premature bolus loss, and oral transit time) and the pharyngeal stage (7 items: pharyngeal triggering, vallecular residues, pyriform sinus residues, laryngeal elevation, pharyngeal wall coating, pharyngeal transit time, and aspiration) (Han, Paik, & Park, 2001).

The Penetration-Aspiration Scale (PAS) is a standard tool that reflects laryngeal penetration and aspiration. Laryngeal penetration is defined as passage of material into the larynx, which does not pass below the vocal folds, and aspiration refers to the action of material penetrating the larynx and entering the airway below the true vocal folds. The scale is broken down into 8 different levels based on the depth of material invasion into the airway and whether the material entering the airway is expelled; higher levels indicate higher aspiration severity (Rosenbek, Robbins, Roecker, Coyle, & Wood, 1996).

2.5 Data analysis

Participant characteristics were analyzed using a statistical software program (SPSS Statistics 20), and descriptive statistics are presented as mean±SD. The Shapiro-Wilk test was used to check normality of the outcome variables. To evaluate the intervention effects, the Wilcoxon signed-rank test was used to compare measures pre- and post-intervention in each group. The Mann-Whitney U-test was used to compare the intergroup changes in outcome measures. Significance level was set at p < 0.05. Effect sizes (Cohen d) of changed scores comparing experimental and placebo group were calculated. Effect size of 0.2, 0.5 and 0.8 represent a small, moderate or large effect respectively.

3 Results

Of the original 33 subjects, 7 subjects (experimental group [n = 3] and placebo group [n = 4]) dropped out before the post-test owing to a hospital transfer or discharge. Therefore, 13 subjects each in the experimental group and placebo group completed this experiment. General characteristics of the participants are described in Table 1. There were no significant differences between groups in the baseline characteristics.

Table 1
Characteristics of participants

Characteristics Experimental group (n = 13) Placebo group (n = 13)

Age (year), mean±SD 69.2±4.1 70.2±3.6

Gender, male/female 5/8 6/7

Site of stroke lesion (number)

Middle cerebral artery 9 9

Basal ganglia 0 1

Midbrain 1 0

Frontal lobe 1 1

Internal capsule 1 1

Pons 1 1

Characteristics	Experimental group (n = 13)	Placebo group (n = 13)
Age (year), mean±SD	69.2±4.1	70.2±3.6
Gender, male/female	5/8	6/7
Site of stroke lesion (number)
Middle cerebral artery	9	9
Basal ganglia	0	1
Midbrain	1	0
Frontal lobe	1	1
Internal capsule	1	1
Pons	1	1

SD, standard deviation.

Both groups showed significant improvement in both oral and pharyngeal phases of VDS (all p < 0.05). However, in comparison with the placebo group, the experimental group showed more improvement in the oral and pharyngeal phases of VDS (p = 0.042, 0.047, respectively) (Table 2), with the differences between the groups being statistically significant (p = 0.003, 0.038, respectively) (Table 3). Effect sizes were observed for the oral phase (0.8), and pharyngeal phase of VDS (1.09).

Table 2

Changes in parameters before and after treatment

	Experimental group			Placebo group			Between groups P-values
	Before treatment	After treatment	P- value	Before treatment	After treatment	P- value
VDS
Oral phase	15.92±5.18	11±3.69	0.003^**^†	15±5.95	13.96±5.58	0.043^*^†	0.042^*^††
Pharyngeal phase	42.04±5.99	31.27±7.73	0.001^**^†	40.04±5.16	35.81±2.98	0.031^*^†	0.047^*^††
Total score	57.96±9.39	42.27±8.67	0.001^**^†	55.04±9.38	49.77±6.95	0.016^*^†	0.018^*^††
PAS	5.08±0.76	3.77±0.93	0.007^**^†	4.92±0.64	4.62±0.77	0.102	0.027^*^††

^*P-value <0.05; ^**P-value <0.01. ^†Wilcoxon signed-rank test, ^††Mann-Whitney U-test. The values are mean±standard deviation, VDS, Videofluoroscopic Dysphagia Scale; PAS, Penetration-Aspiration Scale.

Table 3

Comparison of variations before/after intervention

	Experimental group	Placebo group	Between groups P-values
VDS
Oral phase	4.92±3.08	1.04±1.78	0.003^**^†^†
Pharyngeal phase	10.77±7.79	4.23±5.83	0.038^*^††
Total score	15.69±7.97	5.27±6.16	0.002^**^††
PAS	1.31±1.25	0.31±0.63	0.027^*^††

^*P-value <0.05; ^**P-value <0.01. ^††Mann-Whitney U-test. The values are mean±standard deviation, VDS, Videofluoroscopic Dysphagia Scale; PAS, Penetration-Aspiration Scale.

Further, only the experimental group showed significant improvement in PAS (p = 0.007, 0.102, respectively). The experimental group also showed more improvement in the PAS, compared with the placebo group (p = 0.027) (Table 2), and the difference between the groups was statistically significant (p = 0.027) (Table 3). Effect sizes were observed for the PAS (1.13).

4 Discussion

This study investigated the effects of EMST on oropharyngeal swallowing function and aspiration to provide clinical evidence of the usefulness of EMST for treating the elderly population with dysphagia after stroke.

This study assessed VDS based on VFSS to evaluate the oropharyngeal swallowing function. As a result, we demonstrated that EMST improves oropharyngeal swallowing function in older patients with dysphagia after a stroke. Based on these results, the improvement in the oropharyngeal swallowing function after EMST can be mainly explained by several reasons such as muscular and neural effects.

First, EMST is an oral exercise in which patients are encouraged to exhaleforcefully through a mouthpiece, using strength exerted by their orofacial muscles (e.g., orbicularis oris, buccinators and genioglossus muscle) during the oral phase. Orofacial muscles are considered essential factors that directly and indirectly affect oral structures and functions, such as lip closing, mastication, and bolus formation. A previous study reported a significant improvement in the strength of lip and cheek muscles in healthy elderly subjects after a 4-week EMST program (Park, Oh, & Chang, 2017; Yanagisawa, Matsuo, Shuntoh, & Horiuchi, 2014), and this finding is similar with our results.

Second, EMST promotes the activation of suprahyoid muscles, which play a major role in swallowing in the anterior neck, suggesting the possibility of improving muscle strength through repeated EMST. During swallowing, strong contraction of the suprahyoid muscles directly affects the superior and anterior movements of the hyoid bone and the larynx (Pearson, Langmore, Yu, & Zumwalt, 2012). This mechanism is also known to have direct effects on various functions during the pharyngeal phase, in particular, aspiration, pharyngeal residue, and UES opening (Park, Oh, Hwang, & Lee, 2016). Therefore, we believe that EMST may have positively influenced oropharyngeal swallowing through resistance training of orofacial and suprahyoid muscles.

Another possible mechanism for improvement in the oropharyngeal swallowing function would be related to central nervous system. A high expiratory flow is required for oropharynx during EMST. At this time, sensory receptors of the tongue and oropharynx increase in various afferent stimuli, and this stimulation activates the swallowing center located in the medulla oblongata of the brainstem (Doty, Richmond, & Storey, 1967). Consequently, the efferent information from the swallow center is delivered to motor units participating in the oropharyngeal swallowing function (Kim & Sapienza, 2005). This study suggests that repeated EMST stimulates the swallowing center in the brainstem and contributes positively to the central effect.

In this study, PAS was used to assess the degrees of aspiration and penetration more sensitively. As a result, this study revealed that EMST is effective in decreasing the degrees of penetration and aspiration. The superior movement of the hyoid bone is associated with airway closure, which prevents aspiration (Jacob, Kahrilas, Logemann, Shah, & Ha, 1989; Logemann et al., 1992). In other words, the movement of the hyoid bone through suprahyoid muscle contraction is closely related to decreased aspiration, and therefore, an important factor in the airway protection mechanism. The load training of the suprahyoid muscle through EMST in this study seemed to contribute to safer swallowing and decreased aspiration. PAS assessed the degrees of penetration and aspiration, but also considered the possibility of foreign materials ejecting above the vocal fold while coughing, as well as when airway penetration or aspiration occurs. Strong voluntary coughing can reduce penetration and aspiration by removing foreign materials, even after food enters the airway, which can lower the incidence of aspiration (Kanai et al., 2009; Smith Hammond, Goldstein, Zajac, Gray, Davenport, & Bolser, 2001). According to a previous study, voluntary coughing is closely related to aspiration in terms of the airway protection mechanism in swallowing (Lee, Lee, Kim, Lee, & Park, 2015). Additionally, cough intensity and the risk of airway aspiration are correlated (Widdicombe, Addington, Fontana, & Stephens, 2011). That is, EMST can enhance coughing ability through forced expiration. Previous studies that reported EMST to be effective for airway aspiration prevention support the results of this study.

This study has some limitations. First, the sample size may have influenced the results, therefore, these results cannot be generalized. Second, this study was conducted in subacute patients, in whom the effects of natural recovery by neuroplasticity, considering the rapid nature of neurological recovery, cannot be excluded. Third, because there was follow-up after the end of intervention, the durability of effects could not be determined. Further studies, including a larger sample size and long-term follow-up assessment, are needed in order to evaluate the long-term effects of EMST.

5 Conclusion

In conclusion, the results of this study suggest that EMST can improve the effects of dysphagia after stroke in elderly patients based on swallowing function.

Conflict of interest

This research was carried out without funding. No conflicts of interest have been declared.

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