Correlation between respiratory muscle strength and arm muscle strength of the unaffected side in patients with sub-acute stroke

Abstract

[Purpose] To prospectively examine the relationship between respiratory muscle strength and proximal and distal arm muscle strength on the unaffected side in patients with sub-acute stroke during rehabilitation. [Participants and Methods] Twenty patients with hemiplegic stroke admitted to a post-acute rehabilitation unit were included. Maximal inspiratory pressure (MIP), maximal expiratory pressure (MEP), shoulder flexion strength (index of the proximal portion), and handgrip strength (index of the distal portion) were measured bilaterally on admission and at one month and two months post-admission. [Results] MIP and MEP were significantly increased two months post-admission, particularly MEP. Bilateral arm muscle strength significantly increased in the proximal and distal portions during intensive rehabilitation. On the unaffected side, the strength of the proximal portion was lower than that of the distal portion. Positive correlations were observed between MIP and MEP, and arm muscle strength on the unaffected side, at each time point. Notably, the correlation coefficient tended to be higher with MEP than with MIP. [Conclusion] MIP and MEP correlated with arm muscle strength on the unaffected side during sub-acute rehabilitation.

INTRODUCTION

Stroke is a disorder of the central nervous system that leads to a spectrum of impairments, such as hemiplegia, sensory disorders, pain, aphasia, depression, and pulmonary dysfunction¹⁾. Pulmonary dysfunction can cause atelectasis, pneumonia, and other respiratory complications, often attributed to weakened respiratory muscles. Respiratory muscle strength is thought to be related to the strength of trunk muscles, including the erector spinae and transverse abdominal muscles (TrA). Thus, trunk motor dysfunction due to stroke can influence the trunk muscles, resulting in decreased respiratory muscle strength. Patients with stroke have a lower TrA-to-diaphragm thickness ratio²⁾. Maximal inspiratory pressure (MIP) and maximal expiratory pressure (MEP) were employed to assess respiratory muscle strength. MIP serves as a primary indicator of diaphragmatic muscle strength, while low MIP and MEP are indicative of overall skeletal muscle weakness³⁾.

For two decades, numerous studies have investigated respiratory muscle strength in patients with stroke. Previous studies have shown that MIP and MEP were decreased in patients with stroke even in the chronic stage compared with healthy controls^{4, 5)}. In terms of trunk function or control after stroke, previous studies have shown a positive correlation between trunk function and respiratory muscle strength^{2, 6, 7)}. Recent studies have shed light on the beneficial effects of respiratory muscle training based on muscle strength, such as decreased pulmonary complications and/or increased walking ability in patients with stroke^8,9,10,11).

However, there are very few studies examining the respiratory muscle strength in patients with subacute stroke, and the recovery process of respiratory muscle strength remains poorly understood.

In addition, the correlation between respiratory muscle strength and arm muscle strength of the unaffected side in patients with stroke remains unclear due to the limited studies on this topic; however, some studies have suggested a positive correlation between MIP and handgrip strength in healthy controls^{3, 12, 13)}. Kim reported that MEP showed a positive correlation with handgrip strength of the unaffected side in patients with chronic stroke¹⁴⁾. However, these studies were cross-sectional, and handgrip strength was adopted for assessing distal muscle strength of the arm regardless of whether the participants were patients with stroke or healthy controls. The relationship between proximal muscle strength on the unaffected side and respiratory muscle strength has not yet been explored. Therefore, we focused on examining the proximal muscle strength in addition to the distal muscle strength of the arm muscle of the unaffected side in a prospective study. Hence, it is important to assess the changes in the respiratory and arm muscle strength on the unaffected side in patients undergoing rehabilitation for subacute stroke to elucidate the actual process of muscle strength recovery after stroke.

The current study aimed to investigate the correlation between respiratory muscle strength and proximal and distal arm muscle strength on the unaffected side and examine the changes in respiratory muscle strength and arm muscle strength in patients with subacute stroke during rehabilitation. We also aimed to compare the respiratory and arm muscle strength in patients with subacute stroke with those in healthy controls matched by sex and age.

PARTICIPANTS AND METHODS

This prospective observational study was conducted at our rehabilitation facility from August 2018 to November 2020. This study followed the ethical standards of the Declaration of Helsinki and was approved by the Research Ethics Committee (approval number: 2018C0004). Written informed consent was obtained from each participant prior to the performance of all procedures.

Twenty patients with stroke admitted to the post-acute rehabilitation unit participated in this study. For the control group, 25 healthy sex- and age-matched individuals were recruited. Patients with hemiplegia who had suffered their first-ever stroke and who were able to sit in a wheelchair were included. Conversely, individuals with ability to walk independently were excluded because they had only minor functional impairments due to stroke. Also, individuals with cardiopulmonary diseases, such as chronic obstructive pulmonary disease, interstitial pneumonia, and heart failure; and individuals with ataxia or tetraplegia; an inability to understand the study procedure due to cognitive dysfunction; attention disorder were excluded. Patients with stroke underwent a conventional rehabilitation program with a frequency of two sessions per day (60 minutes per session), seven days a week.

Respiratory muscle strength was assessed using a spirometer (Autospiro AS-507, Minato, Japan) with associated equipment (ASS, Minato, Japan) to measure the MIP and MEP. These measurements were performed in accordance with the American Thoracic Society/European Respiratory Society guidelines¹⁵⁾. Measurements were conducted with the participants sitting on a chair or wheelchair, the trunk positioned at a 90° angle to the hips, and the feet resting on the ground. A clip was attached to the nose, and a mouthpiece was placed rigidly between the lips. The MIP was acquired by measuring the pressure generated during maximal inspiratory effort from the residual volume. The MEP was acquired by measuring the pressure generated during maximal expiratory effort from the total lung capacity. Inspiratory and expiratory efforts were performed for at least 1.5 s, and measurements were taken three times, with a repose period of 30 s between executions. The highest values obtained from the three MIP and MEP attempts were used for the statistical analysis.

Shoulder flexion strength was determined by assessing the proximal arm muscle strength using a hand-held dynamometer (HHD) (μ-Tas F-1, ANIMA Co., Ltd., Japan). Measurements were conducted with the participants sitting on a chair or wheelchair, the trunk positioned at a 90° angle to the hips, the feet resting on the ground, and the upper limb placed at a 90° angle to the trunk. The HHD was attached to the proximal portion of the lateral epicondyle of the humerus. Following the examiner’s instructions, the participants exerted an isometric maximum voluntary contraction against the HHD. When a clear compensatory movement was observed, such as elbow flexion or trunk extension, the measurements were repeated. Measurements were taken twice with a repose period of 30 s between measurements bilaterally. The highest values obtained from the two attempts were used for statistical analyses.

Handgrip strength was determined by assessing the distal arm muscle strength using a Smedley-type hand dynamometer (TKK5001; Takei Scientific Instruments Co., Ltd., Japan). Measurements were conducted with the participants sitting on a chair or a wheelchair, according to standard procedures. Measurements were taken twice with a repose period of 30 s between measurements bilaterally. The highest values obtained from the two attempts were used for statistical analyses.

The functional independence measure motor items (mFIM) were used to assess the participant’s level of independence in performing the activities of daily living (ADL)¹⁶⁾.

These measurements were examined three times concomitantly at admission, 1 month after admission, and 2 months after admission in patients with stroke; however, the respiratory muscle strength and unilateral arm muscle strength (the side was chosen at random) were measured once in healthy controls.

Unpaired t-tests and χ² tests were used to compare the participant’s characteristics. The arm and respiratory muscle strengths between patients with stroke and healthy controls were analyzed using an unpaired t-test or a Mann–Whitney U test. Repeated one-way analysis of variance was used to compare changes in handgrip strength at admission, 1 month later, and 2 months after. Friedman’s test was used to compare the changes in respiratory muscle strength, shoulder flexion strength, and mFIM at admission, 1 month after admission, and 2 months after admission. The Bonferroni post-hoc test was used to determine significant differences. The Spearman’s rank correlation coefficient was used to compute the relationship between respiratory muscle strength and the variables at admission, 1 month after admission, and 2 months after admission.

A p-value of <0.05 was considered significant. Statistical analyses were performed using the IBM SPSS statistics version 27.0 (IBM corporation, Armonk, NY, USA).

RESULTS

The demographic characteristics of the patients with stroke and healthy controls are shown in Table 1. No significant differences were found in the demographic and clinical characteristics between patients with stroke and healthy controls (p>0.05). The degree of paresis in the upper and lower extremities was evaluated using the Brunnstrom recovery stage (BRS) and classified as severe (BRS I and II), moderate (BRS III and IV), or mild (BRS V and VI)¹⁷⁾.

Table 1. Demographic characteristics.

	Patients with stroke (n=20)	Healthy controls (n=25)
Age (years)	67.1 ± 11.2	71.0 ± 3.0
Sex (female), n (%)	10/10	12/13
Height (cm)	160.6 ± 8.0	157.7 ± 7.2
Weight (kg)	56.3 ± 14.7	56.3 ± 8.5
Body mass index (kg/m2)	21.7 ± 4.7	22.6 ± 2.6
Type of stroke, n (%)
Cerebral infarction	14 (70)
Intracerebral hemorrhage	6 (30)
Affected side, n (%)
Right	11 (55)
Left	9 (45)
Degree of paralysis
Upper limb, n (%)
Severe	9 (45)
Moderate	4 (20)
Mild	7 (35)
Degree of paralysis
Lower limb, n (%)
Severe	6 (30)
Moderate	5 (25)
Mild	9 (45)
Days from stroke onset	33.7 ± 18.8

Unpaired t-test and χ² test for sex distribution were used to compare the characteristics between patients with stroke and healthy controls.

No significance was found between the two groups.

Values were expressed as the mean ± standard deviation or number (percentage).

Table 2 presents a comparison of the respiratory and arm muscle strengths on the unaffected side between patients with stroke at admission and healthy controls. The MIP and MEP were significantly lower in patients with stroke less than half in healthy controls (p<0.001). The shoulder flexion strength and handgrip strength of the unaffected side were significantly lower in patients with stroke than in healthy controls (p<0.001 and p<0.019, respectively). Upon examining the strength of the unaffected side in patients with stroke, the results indicated that the proximal muscle strength (58.6%) was lower than the distal muscle strength (75.6%) when compared to healthy controls.

Table 2. MIP, MEP, and arm muscle strength in the unaffected side at admission.

	Patients with stroke	Healthy controls
MIP (cmH2O)	23.3 ± 14.8	62.3 ± 21.2**
MEP (cmH2O)	28.0 ± 17.7	66.2 ± 29.0**
US shoulder flexion strength (kgf)	8.4 ± 4.2	14.0 ± 4.7**
US handgrip strength (kg)	22.0 ± 10.8	29.1 ± 7.7*

Unpaired t-test and Mann–Whitney U test were used to compare those items between the two groups.

All variables showed a significant difference.

Values were expressed as the mean ± standard deviation.

^*p<0.05, ^**p<0.01.

MIP: maximal inspiratory pressure; MEP: maximal expiratory pressure; US: unaffected side.

Table 3 shows the changes in respiratory muscle strength, arm muscle strength on both sides, and mFIM at each time point. The MIP and MEP significantly increased at 1 and 2 months after admission (p<0.01). The MEP was greater than MIP at each time point.

Table 3. Changes in the MIP, MEP, bilateral arm muscle strength, and mFIM in patients with stroke.

	Admission	1 month	2 months
MIP (cmH2O)	23.3 ± 14.8	29.7 ± 14.9**	30.0 ± 15.5##
MEP (cmH2O)	28.0 ± 17.7	35.3 ± 19.1**	39.2 ± 18.4##
ΔMIP (cmH2O)	-	6.3 ± 7.3	8.4 ± 8.4
ΔMEP (cmH2O)	-	7.3 ± 7.6	13.0 ± 8.3‡
US shoulder flexion strength (kgf)	8.4 ± 4.2	9.7 ± 4.7	10.5 ± 5.7##
US handgrip strength (kg)	22.0 ± 10.8	23.6 ± 10.8	25.2 ± 10.5##
AS shoulder flexion strength (kgf)	2.1 ± 3.3	3.2 ± 4.0	4.3 ± 4.7##
AS handgrip strength (kg)	5.5 ± 6.4	7.6 ± 7.9	8.1 ± 8.1##
mFIM (points)	32.1 ± 19.6	44.8 ± 23.6**	57.6 ± 21.2##‡‡

Repeated one-way analysis of variance and Friedman’s test were used to compare those changes.

Values were expressed as the mean ± standard deviation.

^*p<0.05 admission vs. 1 month, ^**p<0.01 admission vs. 1 month.

^#p<0.05 admission vs. 2 months, ^##p<0.01 admission vs. 2 months.

^‡p<0.05 1 month vs. 2 months, ^‡‡p<0.01 1 month vs. 2 months.

Δ represents the change relative to admission.

MIP: maximal inspiratory pressure; MEP: maximal expiratory pressure; US: unaffected side; AS: affected side; mFIM: functional independence measure motor items.

The parameters of bilateral arm muscle strength significantly increased after at 2 months compared with those at admission, regardless of whether the side was affected or unaffected (p<0.01). On the unaffected side, the shoulder flexion strength increased compared with the handgrip strength gained from admission (25% and 14.5%, respectively). The mFIM scores significantly increased at each time point.

Table 4 shows a comparison of Spearman’s rank correlation coefficients between the respiratory and bilateral arm muscle strength in the proximal and distal portions and mFIM. Both MIP and MEP were significantly correlated with shoulder flexion and handgrip strength at each time point (ρ=0.450–757, less than p<0.05).

Table 4. Correlations between the MIP, MEP, and bilateral arm muscle strength.

			US shoulder flexion strength	US handgrip strength	AS shoulder flexion strength	AS handgrip strength	mFIM
MIP	Admission	ρ	0.636**	0.757**	0.090	0.236	0.234
	1 month	ρ	0.591**	0.473*	0.350	0.350	0.110
	2 months	ρ	0.476*	0.450*	0.221	0.109	0.389
MEP	Admission	ρ	0.480*	0.746**	−0.086	0.182	0.106
	1 month	ρ	0.685**	0.661**	0.186	0.367	0.171
	2 months	ρ	0.682**	0.662**	0.304	0.325	0.439

Spearman’s rank correlation coefficient (ρ) was computed for those variables.

*p<0.05, **p<0.01.

MIP: maximal inspiratory pressure, MEP: maximal expiratory pressure; US: unaffected side, AS: affected side; mFIM: functional independence measure motor items.

DISCUSSION

To the best of our knowledge, this study is the first to prospectively investigate the association among respiratory muscle strength, shoulder flexion strength, and handgrip strength in patients with subacute stroke. Consequently, MIP and MEP were significantly lower in patients with stroke than in healthy controls at the time of admission, with a mean of 33.7 days from stroke onset. The shoulder flexion strength and handgrip strength on the unaffected side were also significantly lower in patients with stroke; however, these patients showed relatively lower strength in the proximal portion than in the distal portion. The MIP and MEP were significantly increased at 1 month and 2 months after admission; however, the MEP increased compared with the MIP. Additionally, other measurements showed that bilateral arm muscle strength significantly increased at 2 months after admission compared with that at admission. Positive correlations were found between the MIP, MEP, and muscle strength of the distal and proximal portions of the unaffected side, in addition to their stronger correlation with MEP than with MIP. Conversely, no significant correlations were found between the respiratory muscle strength and arm muscle strength of the affected side and mFIM at each time point; meanwhile, the muscle strength in the proximal and distal portions and mFIM increased at 2 months after admission.

The MIP and MEP unexpectedly decreased in patients with stroke at admission compared with that in healthy controls. Some previous studies have reported lower MIP and MEP values in patients with subacute stroke than in healthy controls^{7, 18)}. They were thought to be significantly decreased in chronic patients after more than six months post stroke onset^{4, 5)}. The MIP and MEP values in this study were considerably lower than those reported in previous studies. First, this difference may stem from the pronounced impairment of physical abilities, such as trunk dysfunction, and severity of paresis. Second, it may be attributed to the exclusion criteria applied to patients with subacute stroke during recruitment. The present study excluded participants capable of walking independently, resulting in a relatively low mFIM score of 32.1 points at admission. When interpreting the respiratory muscle strength in patients with stroke, careful consideration should be given to the stratification of patients. Trunk function or control is thought to be impaired to varying degrees in patients with stroke¹⁹⁾. Many previous studies have established a positive correlation between impaired trunk function and control and respiratory muscle strength^{2, 6, 7)}. Karatas et al. observed significant muscle weakness in trunk flexion and extension in hemiplegic patients compared with healthy controls, impacting balance and stability²⁰⁾. Consequently, we assume that trunk muscle weakness may negatively affect respiratory muscle strength after stroke; however, no study has reported the relationship between these two strengths.

In general, the muscle strength of the arm or leg on the unaffected side after stroke is not thought to be normal. Our findings support this notion, revealing that the shoulder flexion strength and handgrip strength of the unaffected side were significantly reduced compared with the healthy controls (58.6% and 75.6%, respectively). The potential causes of this reduction include disuse atrophy, the lack of concentration or consciousness, disorders of trunk function or control, and impaired trunk muscle strength. A previous study reported that handgrip strength was decreased in patients with chronic stroke compared with healthy controls²¹⁾; however, no study has investigated the relationship between arm strength of the proximal and distal portions and respiratory muscle strength. Our findings confirm those of Andrew and Bohannon²²⁾, who reported that the shoulder abduction strength and wrist extension strength of the unaffected side in patients with stroke were 66.3% and 78.7% of the average rate for healthy controls, indicating weakness in the strength of the proximal portion, similar to our findings. Consequently, we assume that decreased respiratory muscle strength contributes to trunk instability, which may adversely affect muscle force generation in the arm, particularly in the proximal portion. Given that this study focused on isometric contractions, it emphasizes the need for increased trunk stability during arm muscle contraction.

The current study observed a significant increase in the MIP and MEP after 2 months of rehabilitation. However, the values did not reach the levels observed in healthy controls. Specifically, our results indicated an average ΔMIP (gains) of 8.4 cmH₂O and an average ΔMEP (gains) of 13.0 cmH₂O throughout the prospective study period. Previous studies employing rehabilitative interventions reported that the MIP and MIP at 2 and 3 months were greater than the values reported in the present study^{18, 23)}. This discrepancy can be attributed to the greater severity of the stroke in our cohort study. Furthermore, the recovery pattern of respiratory muscle strength differed, with the ΔMEP (gains) being greater than the ΔMIP (gains). This aligns with the findings reported by Kubo et al¹⁸⁾.

Positive correlations were found between respiratory muscle strength, shoulder flexion strength, and handgrip strength on the unaffected side at each time point. Overall, the Spearman’s rank correlation coefficient was stronger for MEP than for MIP, especially at 1 month and 2 months after admission, regardless of whether the arm muscle was in the proximal or distal portion. Kim reported that the MEP was weakly correlated with handgrip strength in patients with chronic stroke (r=0.348, p<0.05), while the MIP was not significantly correlated with handgrip strength¹⁴⁾. MIP is mainly considered the index of diaphragmatic muscle strength; meanwhile, MEP is used to assess the strength of other respiratory muscles³⁾. Hence, it was considered to affect trunk stabilization, resulting in a correlation with arm muscle strength.

This study has some limitations. First, the number of participants was relatively small; hence, increasing the number of samples can strengthen the findings. Additionally, owing to the small number of participants, we were unable to perform an analysis of subgroups based on factors such as the degree of limb paresis, age, and sex. Therefore, future research may need to estimate an appropriate sample size and ensure sufficient statistical power, as well as consider conducting multi-center collaborative studies. Second, it is imperative to unveil the mechanisms underlying the decline in respiratory muscle strength after stroke and establish causal relationships by conducting imaging or physiological evaluations in future studies.

Our findings suggest that healthcare professionals including physiatrists, physiotherapists, and occupational therapists, should focus on the decline in respiratory muscle strength and arm muscle strength on the unaffected side in patients with stroke, in the context of stroke rehabilitation.

Funding

This study received no external funding.

Conflict of interest

The authors declare that they have no conflict of interest.