Relation between hand grip strength, respiratory muscle strength and spirometric measures in male nursing home residents

Abstract

Adverse-outcomes related to sarcopenia are mostly mentioned as physical disability. As the other skeletal muscles, respiratory muscles may also be affected by sarcopenia. Respiratory muscle strength is known to affect pulmonary functions. Therefore, we aimed to investigate the relations between extremity muscle strength, respiratory muscle strengths and spirometric measures in a group of male nursing home residents. Among a total of 104 male residents, residents with obstructive measures were excluded and final study population was composed of 62 residents. Mean age was 70.5 ± 6.7 years, body mass index: 27.7 ± 5.3 kg/m² and dominant hand grip strength: 29.7 ± 6.5 kg. Hand grip strength was positively correlated with maximal inspiratory pressure (MIP) and maximal expiratory pressure (MEP) (r = 0.35, p < 0.01 and r = 0.26, p < 0.05, respectively). In regression analysis, the only factor related to MIP was hand grip strength; among spirometric measures only parameter significantly related to grip strength was peak cough flow (PCF). The association of PCF with grip strength disappeared when MIP alone or “MIP and MEP” were included in the regression analysis. In the latter case, PCF was significantly associated only with MIP. We found peripheric muscle strength be associated with MIP and PCF but not with MEP or any other spirometric parameters. The relation between peripheral muscle strength and PCF was mediated by MIP. Our findings suggest that sarcopenia may affect inspiratory muscle strength earlier or more than the expiratory muscle strength. Sarcopenia may cause decrease in PCF in the elderly, which may stand for some common adverse respiratory complications.

• Grip strength
• maximal inspiratory pressure
• muscle strength
• peak cough flow
• respiratory muscles
• sarcopenia

Introduction

Sarcopenia is a common problem in the elderly. It is a syndrome characterized by progressive and generalized loss of skeletal muscle mass and strength with a risk of adverse outcomes such as physical disability, poor quality of life and death [1,2]. Recently, the diagnostic criteria have been updated by the European Working Group on Sarcopenia in Older People (EWGSOP) [3]. It is concluded that decrease in muscle function (i.e. muscle strength or walking speed) should accompany the decrease in muscle mass to diagnose the sarcopenia. As a good and simple measure of muscle strength, the hand grip strength is recommended [3].

Although sarcopenia is not solely confined to peripheric skeletal muscles but rather generalized loss of skeletal muscle mass and strength, adverse outcomes related to sarcopenia are mostly mentioned as physical disability and related poor quality of life [1,2]. Age-associated alterations in skeletal muscles may also affect respiratory muscle function [4]. Although one cross-sectional study failed to demonstrate any relationship between age and maximal static respiratory pressures in old adults [5], larger studies documented an age-related decrease in respiratory muscle performance [6–9]. Moreover, maximal inspiratory pressure (MIP) and maximal expiratory pressure (MEP) in elderly subjects are reported to correlate with peripheral muscle strength [6], which suggests respiratory muscle strength and peripheric muscle strength is inter-related, i.e. originating from the same source – that is, sarcopenia.

Respiratory muscle strength is known to affect pulmonary functions. Therefore, it may be expected that the elderly with low peripheric muscle strength may have low respiratory muscle strengths and thereby have worse pulmonary functions. Accordingly, in their report, EWGSOP denoted also on peak expiratory flow (PEF) as an alternative measure of muscle strength. In people without lung disorders, PEF is determined by the strength of respiratory muscles. It is a cheap, simple and widely accessible technique that has prognostic value [10,11]. However, they concluded that research on the use of PEF as a measure of sarcopenia is limited, so PEF was not recommended as an isolated measure of muscle strength [3].

The impairment of the pulmonary function as a result of a weakness in the respiratory muscles may lead to atelectasis, an ineffective cough and other respiratory complications [12]. This scenario is a common cause of morbidity and mortality especially in nursing home residents [13]. Hence, it is important to understand the changes in the respiratory system in this population in order to minimize the number of respiratory complications. In this study, we aimed to investigate the relations between extremity muscle strength, respiratory muscle strengths and spirometric measures in a group of male nursing home residents.

Methods

Population and setting

Our study cohort was composed of the ≥ 60 years old male residents of a nursing home. The residents with past history of lung cancer and/or lung operation, mini mental state examination score < 24, significant chest wall deformity (kyphosis/scoliosis) had not given informed consent and who had been uncooperative to the measurements were excluded. History of cerebrovascular accident was asked to all participants as a factor that may affect grip strength, MIP or MEP.

Measurements

Cognitive status was screened by mini mental state examination and score < 24 was accepted as suggestive for cognitive problem [14]. The height was measured when the residents were at a stand-up position, and weights were measured with light clothes. Spirometric measurements were performed by portable spirometer (Spirolab II, MIR, Via del Maggiolino, 125-00155, Roma, Italy) cared for the American Thoracic Society criteria [15]. Three measurements were undertaken from each resident. Measurements were performed at any time of the day. We referred the Global Initiative for Chronic Obstructive Lung Disease spirometric obstruction criterion as forced expiratory volume in one second (FEV1)/forced vital capacity (FVC) < 0.7. Extremity muscle strength was evaluated by dominant hand grip strength via hydraulic hand dynamometer (Baseline® 3-piece Hand Evaluation Sets). The respiratory muscle strength was assessed by portable respiratory muscle strength measurement equipment including pressure sensitive transmission system (MICRO RPM – MIP/MEP equipment) giving the MIP and MEP in cm H₂O unit. MIP and MEP measurements were carried out as described by American Thoracic Society/European Respiratory Society (ATS/ERS) [16]. MIP and MEP were determined using the residual volume and the total lung capacity, respectively, with the subjects in a sitting position. The inspiratory and expiratory efforts were held for at least one second. Patients carried out at least three acceptable inspirations/expirations wearing a nose clip for determining the two reproducible inspirations/expirations. The highest values were used in the analysis. Peak cough flow (PCF) was measured by having the person cough as forcefully as possible through the peak flow meter after a maximum inspiration. This study was approved by the local medical ethical committee and conducted according to the guidelines laid down in the Declaration of Helsinki. Informed consent was obtained from all patients and/or their related conservators.

Statistical analysis

All data were entered into a database and were verified by a second independent person. Numerical variables were given as mean ± standard deviation. Correlations between numerical parameters were analyzed with Pearson correlation test. Linear regression analysis was used for multivariate analysis of numerical parameters. p Values less than 0.05 were accepted as significant. The statistical analysis was carried out with Statistical Package for Social Sciences for Windows ver. 15.0 (SPSS Inc., Chicago, IL).

Results

One-hundred four male residents were included. Among them, residents with obstructive pathology in spirometric measurements were excluded, so that final study population was composed of 62 male residents. Mean age was 70.5 ± 6.7 years. The mean values of the MIPs and the MEPs were 60.8 ± 25.6 cm H₂O and 100.9 ± 37.8 cm H₂O, respectively.

Characteristics of the study population regarding the age, body mass index, history of cerebrovascular accident, grip strength, respiratory muscle strengths and spirometric measures are listed in Table 1.

Table 1. Characteristics of the study population on demographics, medical history, dominant hand grip strength and pulmonary function tests (n = 62).

Age (years)	70.5 ± 6.7 (60–88)
Body mass index (kg/m2)	27.7 ± 5.3 (19.0–43.3)
History of cerebrovascular accident [n (%)]	9 (14.5%)
Dominant hand grip strength (kg)	29.7 ± 6.5 (18–44)
Pulmonary function tests
MIP (cm H2O)	60.8 ± 25.6 (17–131)
MEP (cm H2O)	100.9 ± 37.8 (18–228)
FVC predicted (%)	81.6 ± 22.5 (21–133)
FEV1 predicted (%)	84.8 ± 24.5 (27–137)
FEV1/FVC	80.3 ± 7.3 (70–100)
PEF predicted (%)	76.1 ± 24.6 (29–144)
PCF (l/min)	329.8 ± 105.9 (120–700)

Data are given as mean ± standard deviation (minimum – maximum).

MIP: maximal inspiratory pressure, MEP: maximal expiratory pressure, FEV1: forced expiratory volume in one second, FVC: forced vital capacity, PEF: peak expiratory flow, PCF: peak cough flow, ml: milliliter, s: second, l: liter and min: minute.

We first studied whether respiratory muscle strength, measured by MIP and MEP, were related to grip strength. Hand grip strength was positively correlated with MIP and MEP (r = 0.35, p < 0.01 and r = 0.26, p < 0.05, respectively). In regression analysis, including hand grip strength, age, BMI and history of cerebrovascular accident, the only factor related to MIP was hand grip strength (B: 1.27, SE: 0.53, p < 0.05). In this analysis, MIP was dependent variable, while hand grip strength, age, BMI and history of cerebrovascular accident were independent variables. On the other hand, in regression analysis, MEP was not related to any of the study parameters (p > 0.05). In this analysis, MEP was dependent variable, while hand grip strength, age, BMI and history of cerebrovascular accident were independent variables.

Second, we studied whether any spirometric measures were related to grip strength in accordance with our hypothesis. Hand grip strength was positively correlated with PCF (r = 0.34, p < 0.01) but not with FVC%, FEV%, FEV1/FVC or PEF%. In regression analysis including hand grip strength, age, BMI and history of cerebrovascular accident FVC%, FEV1%, FEV1/FVC and PEF% were not significantly related to grip strength, while PCF was significantly related to grip strength (B: 5.43, SE: 2.16, p < 0.05). In these analyses, FVC% or FEV1% or FEV1/FVC or PEF% or PCF was dependent variable, while hand grip strength, age, BMI and history of cerebrovascular accident were independent variables. As MIP was related to hand grip strength, another regression model was developed including MIP. In this analysis, PCF was the dependent variable, while hand grip strength, age, BMI, history of cerebrovascular accident and MIP were independent variables. The association of PCF with grip strength disappeared when MIP was included in the regression analysis. In the latter case, PCF was significantly associated only with MIP (B: 2.48, SE: 0.445, p < 0.001). We made one more regression analysis including MEP to the last regression. So, PCF was again the dependent variable, while hand grip strength, age, BMI, history of cerebrovascular accident, MIP and MEP were independent variables. Furthermore, in this analysis, PCF was significantly associated only with MIP (B: 1.80, SE: 0.61, p < 0.005).

Discussion

Sarcopenia has been extensively studied in the elderly with regard to limb function but less with regard to respiratory function [17]. Numerous reports have linked extremity muscle strength with mortality, but the mechanism underlying this association is not known. In a study that used data from 960 older persons, pulmonary function is suggested to partially account for the association of muscle strength and mortality [18]. However, sarcopenia of respiratory muscles, such as the diaphragm, have not been well characterized yet [19]. There is a reduction in respiratory muscle strength with the aging process [20–22]. Sedentary lifestyle combined with the aging process may exacerbate the reduction in both inspiratory and expiratory muscle strength [11]. This is most probably the respiratory translation of accentuated sarcopenia. However, the term “respiratory muscle sarcopenia” or “sarcopenia of the respiratory muscles” is uncommonly encountered, used only in few reports so far [11,17,19,23]. Most recently, sarcopenia of the diaphragm muscle in aging mice has been demonstrated [19]. So, sarcopenia may limit the ability of the diaphragm muscle to accomplish expulsive, non-ventilatory behaviors essential for airway clearance. Hence, sarcopenia of the respiratory muscles may contribute to respiratory complications with aging [19].

In previous studies, it is reported that physical activity has an important role for maintaining both inspiratory and expiratory muscle strength [21,22,24], and the active life style can positively affect the respiratory muscle strength. Furthermore, MIP and MEP in elderly subjects are reported to correlate with peripheral muscle strength [6], which suggests respiratory muscle strength and peripheric muscle strength are inter-related, i.e. originating from the same source – that is, sarcopenia. In our study, we found hand grip strength is associated with MIP but not with MEP in adjusted regression analyses. MIP and MEP measurements can localize respiratory muscle weakness. A low MIP and normal MEP suggests isolated inspiratory muscle weakness (usually diaphragmatic), while a low MIP and MEP suggests generalized skeletal muscle weakness. Isolated expiratory muscle weakness (normal MIP and low MEP) is rare. From a practical standpoint, this differentiation is of minimal diagnostic benefit because many of the causes of respiratory muscle weakness can cause either inspiratory muscle weakness or generalized skeletal muscle weakness [25]. To our knowledge, there is no study reporting the timing of inspiratory and expiratory muscle involvement with sarcopenia. Our finding suggests that the decrease in respiratory muscles’ strength may first and more commonly affect MIP, which is primarily the function of diaphragm muscle. This suggestion is in accordance with the – so far only demonstration of sarcopenia in the diaphragm muscle – rather than the muscles involved in maximal expiration – which are abdominal muscles and internal intercostal muscles.

In this study, we found hand grip strength be associated with PCF but not with any other spirometric parameters. The relation between hand grip strength and PCF was mediated by MIP since the association of hand grip strength and PCF disappeared when MIP was included in the regression analysis. For an effective cough, subjects initially inspire a large amount of air and apply an expiratory force against a closed glottis, generating a high thoraco-abdominal pressure. At this point, the glottis opens, resulting in strong expiratory flow [26,27]. As is known in the cough mechanism, the expiratory muscles play the most basic and important role in producing a functional cough flow. Therefore, associations of PCF with MIP but not with MEP were a somewhat unanticipated outcome of the study. However, it is known that although the expiratory muscle function plays an important role in an effective cough, the lung volume attained prior to a contraction of the expiratory muscle also plays an important role during cough [28,29]. The function of the inspiratory muscles is essential in the inspiratory phase of cough. Forced expiration during coughing normally begins with maximum inflation of the lungs, that is, greater expiratory pressures, and flows can be produced at high lung volumes by optimizing the length–tension relationship of the expiratory muscles [30]. As the strength of the inspiratory muscle declines, the patients lose their ability to take spontaneous periodic deep breaths, which normally stimulates surfactant production and distribution, and reopens the collapsed peripheral airways [31]. Without deep insufflations, these patients first develop micro-atelectasis, and a long-term inability to take deep breaths or chronic hypo-inflation results in a permanent pulmonary restriction. Therefore, decreased pulmonary compliance results initially in micro-atelectasis and ultimately in increased stiffness of the chest wall and the lung tissues themselves [32]. An effective cough relies on the generation of sufficient dynamic airway compression to produce a high airflow velocity. In contrast, the diminished lung compliance may limit the dynamic airway compression, which might be another factor that causes weak coughing [33]. These various factors are correlated with the MIP and can affect the cough capacity. Correlation between coughing and the inspiratory muscle strength has not been studied until a recent study [34]. In this report, the significance of the inspiratory muscle strength on the cough capacity were studied in patients with cervical spinal cord injury, and MIP showed a higher correlation with PCF than the MEP [34]. They discussed that it is possible that a stronger inspiratory muscle will result in a larger pre-cough inspiratory volume. This might explain why the MIP showed a more significant correlation with the PCF than the MEP, which also means that the inspiratory function had a more significant influence on the cough capacity in the patients with a motor complete cervical SCI than the expiratory function. It is known that the MIP is relatively preserved in patients with neuromuscular disease until they become old, and the MEP has been emphasized as a sensitive marker of the respiratory muscle deterioration in that patients [27]. However, these opinions are based on studies that were performed on patients with chronic progressive disease such as muscular dystrophy, spinal muscular atrophy, etc. Therefore, the authors suggested that the MEP might not be a more sensitive marker of the respiratory muscle deterioration in patients with a traumatic SCI in whom both the inspiratory and expiratory dysfunction develop simultaneously due to respiratory muscle paralysis injuries [34]. We suggest that this may also be valid in the elderly. There is no reason to suggest earlier involvement of expiratory muscles than the inspiratory ones in sarcopenia. In fact, the aforementioned result of our study – that is, association of grip strength with MIP but not with MEP – suggest that in sarcopenia, the inspiratory dysfunction may develop simultaneously with or earlier than the expiratory dysfunction. The MEP might not be a more sensitive marker of the respiratory muscle deterioration in elderly sarcopenic patients. The possible earlier or simultaneous involvement of inspiratory muscles than expiratory muscles may also explain the correlation of PCF with MIP but not with MEP in our study.

It is known that PCF is the most reliable way to evaluate cough strength [35]. Our findings suggest that regular physical activity may indirectly improve the airway defense mechanisms since gaining strength may contribute to increase the effectiveness of cough thereby decrease adverse respiratory complications of older people.

Some limitations of our study deserve consideration. The relatively small size of our sample might have masked or skewed some of the important statistical trends. Accordingly, a larger study will need to be performed in order to clarify the influence of sarcopenia on the respiratory muscle strengths and on the cough capacity of elderly. Second, factors not considered in this analyses (e.g. physical activity) might differently explain our findings. The cross-sectional design of the study does not allow establishing any cause-effect sequence among the studied relationships. Final limitation is that cough is commonly a reflex event; the best way to determine the effect of the respiratory muscle strength on it would be measuring their strength from a reflex cough [36].

Conclusion

In conclusion, we found peripheric muscle strength be associated with MIP and PCF but not with MEP or any other spirometric parameters. The relation between peripheral muscle strength and PCF was mediated through MIP. Our findings suggest that sarcopenia may affect inspiratory muscle strength earlier or more than the expiratory muscle strength. Modulated by its effect on inspiratory muscles, sarcopenia may cause decrease in PCF in the elderly, which may stand for some common adverse respiratory complications in this population.

Declaration of interest

None of the authors of this manuscript have any financial or personal relationships with other people or organizations that could inappropriately influence (bias) their work. None of the co-authors have direct or indirect conflicts of interest, financial or otherwise, relating to the subject of our report. There is no sponsorship. All authors have made substantial contributions to the design of the study, acquisition, analysis and interpretation of the data, drafting the article or revising and final approval of the version to be submitted. All authors have met the criteria for authorship stated in the Uniform Requirements for Manuscripts Submitted to Biomedical Journals. All authors have read and approved the final manuscript.

This work was supported by the Research Fund of The University of Istanbul, project number: 5146.