Ⅰ Introduction
Stroke patients have weakened muscles overall, and approximately 55% to 70% of stroke patients develop a chronic dysfunction (Duncan et al., 2002; Sutbeyaz et al., 2010). Further, stroke patients have muscles of their body weakened as a consequence of various prognostic symptoms of stroke and weakened respiratory function due to diaphragm, intercostal muscle (IC), and abdominal muscle paralysis (Britto et al., 2011; Lima et al., 2014; Messaggi-Sartor et al., 2015). Hemiplegia caused by stroke can lead to an impairment of posture, muscle tone, and motor control by impairing coordination between voluntary motor function and muscle (de Almeida et al., 2011), and a disturbance of motor control impairs the ability to control respiratory muscle coordination (Britto et al., 2011) while increasing the asymmetry of diaphragm contraction in the paretic and non-paretic sides (Kim & Jung, 2013).
Inspiratory muscle training using a device has been widely used in previous studies as a type of respiratory muscle training to improve respiratory function in stroke patients. It improves muscle strength and endurance by straining the diaphragm and inspiratory muscles (Britto et al., 2011; Moodie, Reeve, & Elkins, 2011; Sutbeyaz et al., 2010; Xiao et al., 2012), and enhances ventilation capacity of patients with inspiratory muscle impairment regardless of whether the disorder is neurological or non-neurological (Petrovic et al., 2009). Meanwhile, a previous study showed that a strong relation exists between increased maximal inspiratory pressure (MIP) and activation of the sternocleidomastoid (SCM) and scalene muscle (Yokoba et al., 2003). Moreover, activation of the diaphragm (DI) and intercostal (IC) muscles increased during inspiratory muscle loading, as assessed by a threshold inspiratory loading device (Hawkes, Nowicky, & McConnell, 2007). A recent study has shown that an excessive load during inspiratory muscle training can lead to overactivation of the secondary inspiratory muscle (Jung & Kim, 2016). Therefore, therapists are recommended to minimize compensation by providing proper training methods (Jung & Kim, 2016).
Posture change alters spontaneous breathing by causing kinematic changes of the chest wall and abdomen, while also altering the relative contributions of the chest wall and abdomen to lung function and ventilation (Romei et al., 2010), affect the shape of the chest wall and the movement of the chest wall compartment (Lee et al., 2010). Based on these considerations, previous studies have investigated the effects of posture change during spontaneous breathing and deep breathing on right and left chest wall volume in normal adults (Aliverti et al., 2000), and have also confirmed that posture change is strongly correlated with changes in lung volume and spontaneous breathing (Verschakelen & Demedts, 1995).
In clinical practice, thoracic rotation and lateral flexion posture is applied to the trunk during breathing training for pulmonary disease patients, to promote the partial expansion of the chest wall and chest wall mobilization exercise (Kisner & Colby, 2007; Leelarungrayub, 2012). This posture may improve the mobility and respiratory function of the chest wall by inducing expansion in a specific region of it (Kisner & Colby, 2007).
Despite the varying effects of posture on respiratory function however, studies comparing the effects of different training postures during respiratory muscle training are lacking.
The current study aimed to investigate changes in muscle activation in respiratory muscles and subsequently identify the most efficient respiratory muscle training posture for stroke patients, by comparing a neutral posture (NP) that equally trains the respiratory muscles of both the paretic and non-paretic sides, a sidebending posture (SP) that extends the respiratory muscle of the paretic side, and a habitual posture (HP).
Ⅱ Methods
1 Subjects
Subjects in the present study were patients who had been diagnosed with stroke via computed tomography, and had exhibited disease for at least 6 months. Selection criteria for the subjects in this study were identical to those described in previous research (Britto et al., 2011; Sutbeyaz et al., 2010).
The subjects had a full understanding of the study, and voluntarily consented to participate in it. This study was approved by the university institutional review board (IRB No. CUPIRB-2015-008).
A total of 39 patients agreed to participate in the study and gave informed consent. Patients were allocated to either the NP (n = 13), SP (n = 13), or HP groups (n = 13). However, there were three dropouts, two from the SP group (lack of time) and one from the HP group (high blood pressure). Thus, 36 subjects completed all training among the NP (n = 13), SP (n = 11) and HP groups (n = 12).
To randomize the group, we used three cards, each of which was marked with one of the postures. Each subject was asked to select a card from an envelope containing each of the three postures.
2 Measurement and Procedure
A spirometer (Pony Fx, Cosmed, Italy) was used to measure pulmonary function parameters including forced vital capacity (FVC), forced expiratory volume in the first second (FEV1), FEV1/FVC, and peak expiratory flow before applying an intervention in each group (Jung et al., 2014; Jung & Kim, 2015).
This test was used to recruit subjects with a restricted lung disease type whose FEV1/FVC value was > 70% of the predicted value and whose FVC value was < 80% of the predicted value.
Surface electromyography (sEMG) was used to measure respiratory muscle function during induction of in a sitting posture with 90ﾟ hip flexion and 90ﾟ knee flexion. The electrodes for sEMG were attached to the external muscles (de Andrade et al., 2005; Hawkes, Nowicky, & McConnell, 2007).
To minimize skin resistance, the skin was cleaned and swabbed with alcohol-soaked cotton before the electrodes were placed. Each EMG probe was attached to two superficial reusable bipolar electrodes consisting of Ag/AgCl material and a conductive hydrogel adhesive. The electrodes were placed 2 cm apart (Hawkes, Nowicky, & McConnell, 2007; Jung & Kim, 2016) on the external IC muscles, in the fifth IC space at the posterior axillary line (Hawkes, Nowicky, & McConnell, 2007); the SCM electrode was placed on the muscle body, 5 cm from the mastoid process (de Andrade et al., 2005; Jung & Kim, 2016).
The sEMG responses were amplified (gain × 3000) (FreeEMG 300, BTS Bioengineering, Italy), and the band-pass was filtered between 20 and 500 Hz and digitized at a sampling rate of 3000 Hz via an analogue -to-digital converter and the root-means-square (RMS) (Hawkes, Nowicky, & McConnell, 2007). The acquired data were subsequently analyzed using commercially available software (SMART, BTS Bioengineering, Italy). The activation of the respiratory muscle was computed with the equation used in a previous study to compute a standardized value (de Andrade et al., 2005; Jung & Kim, 2016). Respiratory muscle activity was calculated as RMS values at maximum inspiratory pressure (MIP) (μV)/ RMS values at rest (μV) (de Andrade et al., 2005).
For respiratory muscle training, a threshold inspiratory muscle trainer (POWER breathe Medic, POWER breathe International Ltd., UK) was employed using a method modified from that used in previous studies (Sutbeyaz et al., 2010). Each group began receiving training with the MIP at 30%, and exercise intensity was gradually increased by 10 cmH2O in each session. Training was ended at an MIP of 60% (Jung & Kim, 2015; Sutbeyaz et al., 2010). Each intervention was conducted for sessions of 30 minutes, three times per week, for 6 weeks.
All groups participated in a conventional stroke rehabilitation program, 5 days per week for 6 weeks.
Respiratory muscle training postures were set to neutral posture, side-bending posture, and habitual posture with reference to a previous study (Lee et al., 2010), and respiratory muscle training was performed in each training posture.
Neutral posture refers to the “ideal” and “reference” postures. The subjects were asked to maintain thoracic kyphosis and lumbar lordosis. Side bending posture refers to a lateral shifting posture to the non-paretic side.
The subject was asked to “let the non-paretic side shoulder drop towards the non-paretic hip” while the examiner provided tactile facilitation at the level of the 8th rib, in order to encourage lateral translation and side-bending apex at that level (Lee et al., 2010). For the habitual posture, the subjects were asked to “sit comfortably in an upright position the way you would usually sit” (Figure 1).
3 Data analysis
The data collected were analyzed using PASW Statistics for Windows (ver. 18.0). A paired t-test was conducted to verify changes within each group, and one-way analysis of variance was used to examine differences between the three groups. Bonferroni post-hoc analysis was employed. Statistical significance was set at p < .05.
All experimental measurements with the sEMG test demonstrated intra-rater reliability as follows: ICC (3,1) 0.69 (95%CI, 0.09-0.91); the spirometer test demonstrated intra-rater reliability as follows: ICC (3,1) 0.96 (95%CI 0.89-0.98).
Ⅲ Results
1 Participants characteristics
The homogeneity analysis among the three groups were conducted prior to the experiment, and the result revealed that there was no significant difference in age, height, weight, and time since stroke values (Table 1).
2 Respiratory muscle activation
The effects of the interventions over time within each group is shown in Table 2, and the results of comparisons between the groups after a 6-week intervention period are shown in Table 3.
Ⅳ Discussion
Stroke patients use the chest wall and abdominal muscles asymmetrically, which causes trunk flexion and rotation, making postural maintenance difficult and altering respiratory muscle functions (Jandt, et al.,, 2011). In addition, a previous study showed that changes in thorax alignment affect the movement and shape of the chest wall during breathing (Gandevia et al., 2002; Hodges & Gandevia, 2000). To address these problems, respiratory muscle training (RMT) is practiced in the clinic; among the different types of RMT, inspiratory muscle training (IMT) has been effective for improving pulmonary function (Britto et al., 2011; Sutbeyaz et al., 2010).
The inspiratory muscle training used in the present study has been widely applied to patients with neurological problems, in order to improve inspiratory muscle strength and endurance, exercise capacity, and dyspnea (Britto et al., 2011; Jung & Kim, 2015; Sutbeyaz et al., 2010). In addition, previous study results showed that inspiratory muscle training methods could improve the diaphragm thickness asymmetry ratio and diaphragm contraction (Jung & Kim, 2015). Such results were obtained because the principle of “overload” (i.e., maximal training load should be applied to stimulate optimal physiologic adaptation within the skeletal muscle) was applied appropriately (Britto et al., 2011; Sutbeyaz et al., 2010).
Therefore, based on the hypothesis that posture during respiratory muscle training would affect the expansion of the paretic side chest wall in stroke patients, we aimed to identify the most effective respiratory muscle training posture by investigating the effects of neutral posture, side bending posture, and habitual posture on respiratory muscle activity in stroke patients.
Previous studies have reported that sEMG shows the degree of spasticity and ability to coordinate and control extremity muscles in stroke patients (Kuriki et al., 2010), and that the decline of spasticity of the paretic side can be confirmed with a reduction of muscle activation (Albani et al., 2010). In the current study, the activity of the paretic side external IC muscle was decreased by 48.5% in the NP group and by 21.0% in the SP group, but increased by 64.6% in the HP group, and there was a significant difference between the groups. These results suggest that respiratory muscle training in a neutral posture improves the ability to control the trunk muscle by controlling the muscle spasticity of the paretic side, but that a habitual posture does not effectively train respiratory muscles through the same mechanism. Furthermore, the activity of the external IC muscle in the nonparetic side was significantly reduced by 28% in the NP group and increased by 46% in the HP group. These results show that applying appropriate training of the respiratory muscles for 6 weeks in the NP group improved the efficiency of the respiratory muscles. Furthermore, the results in the HP group show that focusing the training on the non-paretic side muscle hinders efficient training of the respiratory muscles.
Previous studies have reported that a continuous increase in SCM muscle activation causes a defect in the respiratory mechanism (Costa et al., 1994; de Andrade et al., 2005). In the current study, the NP group showed a symmetrical reduction of SCM activity of 23% in the paretic and non-paretic sides. In contrast, the HP group showed a 23% reduction in the paretic side with a 122% increase in the nonparetic side, while the SP group showed a 23% increase in the paretic side with a 30% reduction in the non-paretic side, constituting asymmetrical SCM muscle activation. These results are attributable to the fact that the side bending posture and habitual posture altered the length of respiratory muscles by inducing asymmetrical lateral flexion of the cervical spine by extending the upper cervical spine, including the atlantooccipital joint, and flexing the lower cervical spine (Lee et al., 2010). Such changes in muscle length are speculated to have affected chest wall movement.
Limitations of this study included its relatively small sample size and the inherent difficulty in assessing respiratory muscle activation among the various clinical symptoms of subjects. Therefore, a standard scale that can efficiently measure respiratory muscle activity in stroke patients is necessary; notably, this requires further studies with larger numbers of subjects.
Ⅴ Conclusions
The findings of the current study demonstrated that applying respiratory muscle training in a neutral posture leads to the most efficient training, with symmetrical contraction of respiratory muscles in the paretic and non-paretic sides. Conversely, the side bending posture and habitual posture lower the effects of respiratory muscle training by inducing asymmetrical contraction of respiratory muscles and causing overactivation of respiratory accessory muscles.
