https://orcid.org/0000-0002-5948-6880
ABSTRACT
The aim of this study was to investigate if hand grip strength (HGS) is associated with: 1) fatigue, and specifically clinically relevant fatigue (CRF); 2) low physical activity; and 3) fatigue independent of physical activity level, among individuals with and without COPD. Data were collected from the Obstructive Lung Disease in Northern Sweden (OLIN) COPD-study in 2014. HGS was measured with a hand-grip dynamometer, fatigue and physical activity were assessed by questionnaires; FACIT-Fatigue respectively IPAQ. Among individuals with COPD (n = 389), but not without COPD (n = 442), HGS was lower among those with CRF than those without CRF, significantly so among men (p = 0.001) and close to among women (p = 0.051). HGS was not associated with physical activity levels within any of the groups. HGS was associated with fatigue among men, but not women, with COPD independent of physical activity level, age, height, and smoking habits (Beta = 0.190, 95% CI 0.061–0.319, respectively Beta = 0.048, 95% CI−0.056–0.152), while there were no corresponding significant findings among individuals without COPD. In summary, HGS was associated with CRF among individuals with COPD in this population-based study. Among men with COPD, HGS was associated with fatigue independent of physical activity level and common confounders.
Introduction
Chronic obstructive pulmonary disease (COPD) is estimated to affect over 8%–10% of all adults (Backman et al., Citation2016; Lamprecht et al., Citation2015), and the most well-known predictors are increasing age and smoking. The majority of all individuals with COPD have mild to moderate disease (Lindberg et al., Citation2006). However, merely a third of them are identified by health care (Lamprecht et al., Citation2015; Lindberg et al., Citation2006), and this under-diagnosis contributes to a lack of knowledge about COPD in the population. Cardiovascular comorbidities are common (Lindberg, Larsson, Ronmark, and Lundback, Citation2011), but skeletal muscle abnormalities such as muscle fiber atrophy, muscle fiber shift, weakness, and functional limitations are also frequent (Eisner et al., Citation2008; Maltais et al., Citation2014).
Hand grip strength (HGS) correlates strongly to muscle mass and strength in upper and lower extremities in individuals with COPD (Marino et al., Citation2010), and is also associated with exercise performance (da Silva et al., Citation2017; Rausch-Osthoff et al., Citation2014). There are a few studies of HGS in selected COPD samples, but with contradictory results; some found lower HGS in COPD than controls (Eisner et al., Citation2008), while others did not find any such differences (Gosselink, Troosters, and Decramer, Citation2000). Even though we found no difference in HGS when comparing individuals with and without COPD in a recently published population-based study, HGS was clearly associated with COPD severity (Strandkvist et al., Citation2016).
Physical activity is reduced among patients with moderate to very severe COPD compared to healthy controls (Pitta et al., Citation2005; Troosters et al., Citation2010). In a population-based study, the proportion with low physical activity was higher in moderate to severe COPD than in those without COPD (Andersson et al., Citation2015), and clinically relevant fatigue was associated with low physical activity (Andersson et al., Citation2015). Fatigue is associated with several chronic diseases (Swain, Citation2000), and is also common in COPD (Stridsman, Mullerova, Skar, and Lindberg, Citation2013). Among patients with COPD, fatigue seems to be associated with muscle strength (Calik-Kutukcu et al., Citation2014), and one strategy to gain control over fatigue is to continue with physical activity (Stridsman, Lindberg, and Skar, Citation2014).
Decreased HGS, increased fatigue and decreased level of physical activity are associated with the burden of COPD, and each of them is a possible target of rehabilitation interventions (Bolton et al., Citation2013). Still, most studies within this topic include small and selected COPD populations, and furthermore, the relationships between these factors have not been evaluated in the same study. Due to the under-diagnosis, population-based studies are needed to understand the true burden of and relationship between HGS, fatigue, and physical activity in COPD. An increased knowledge is of importance to identify individuals for rehabilitation interventions and also to individualize and monitor effects of rehabilitation efforts. Our hypothesis is that HGS is associated with fatigue and physical activity in individuals with, but not without COPD. The objective of this population-based study was to investigate if: 1) hand grip strength is associated to fatigue, and specifically clinically relevant fatigue, among individuals with and without COPD; 2) hand grip strength is associated to low physical activity among individuals with and without COPD; and 3) hand grip strength is associated to fatigue among individuals with and without COPD, independent of physical activity level.
Methods
Design
The cross-sectional data were collected from the population-based Obstructive Lung Disease in Northern Sweden (OLIN) longitudinal COPD study, and the study design has previously been described in detail (Lindberg and Lundback, Citation2008). The study was approved by the Regional Ethical Review Board at Umeå University, Sweden. All participants gave written informed consent before data collection.
Participants
All individuals with airway obstruction, FEV1/(F)VC < 0.70 (COPD, n = 993), were identified from four adult population-based adult cohorts during 2002–2004, together with a sex- and age-matched reference group without obstructive lung function impairment (non-COPD). The study population (n = 1 986; 902 women, 1,084 men) has been invited to annual examinations since 2005 with a basic program including spirometry and a structured interview (Lindberg and Lundback, Citation2008). The current study is based on data collected during 2014 when measurements of HGS as well as questionnaires for assessment of fatigue and physical activity were included in addition to the basic program. In total 831 individuals, whereof 389 with COPD participated ().
Figure 1. Flow chart, recruitment of study population.
Notes: aIndividuals who were unable to attend examination; bIndividuals who denied participation or could not be located; cIndividuals with complete data on FACIT-Fatigue; dIndividuals with complete data on HGS; eIndividuals with complete data on IPAQ; fIndividuals with complete data on HGS & FACIT-Fatigue; gIndividuals with complete data on HGS & IPAQ; hIndividuals with complete data on HGS, FACIT-Fatigue & IPAQ.
Outcome measures
HGS was measured by a hand-grip dynamometer, Jamar® (Mathiowetz, Weber, Volland, and Kashman, Citation1984), in kilogram (kg). The participants were instructed to sit down with their elbows flexed at an angle of 90 degrees, with the dynamometer held by the hand in a neutral position (Bohannon et al., Citation2006). Three attempts were performed with each hand, and the highest value was used for analysis.
Fatigue was assessed by the validated and symptom-specific questionnaire, the Functional Assessment of Chronic Therapy-Fatigue (FACIT-Fatigue) (Al-Shair et al., Citation2012; Cella et al., Citation2002). The scale has 13 items and measures the intensity of fatigue and its impact on daily life during the last week, with a higher score (0–52) indicating less fatigue. Clinically relevant fatigue (CRF) was defined as a FACIT-Fatigue score of ≤43 (Cella et al., Citation2002; Stridsman, Mullerova, Skar, and Lindberg, Citation2013).
Physical activity was assessed with the Swedish version of the International Physical Activity Questionnaire (IPAQ) short form modified for the elderly (Hurtig-Wennlof, Hagstromer, and Olsson, Citation2010), previously used in COPD research (Andersson et al., Citation2015; Todt et al., Citation2015). The total time is weighted by a metabolic equivalent of task, MET (1 MET = resting metabolic rate, 3.5 ml O2 kg−1∙min−1), resulting in a body weight-adjusted activity estimate, expressed as MET-minutes/week (min/w). Physical activity was categorized into three levels: 1) low; 2) moderate; and 3) high, based on reported time of walking, moderate and/or vigorous activity, in combination with a weighted factor for the different activities (International Physical Activity Questionnaire, Citation2005). Low activity was defined as not meeting the recommended minimum physical activity level defined as at least 30 min of moderate physical activity five days of the week (Garber et al., Citation2011; Nelson et al., Citation2007).
The spirometry was performed using a dry volume spirometer, Minhjard Vicatest, according to American Thoracic Society standards (American Thoracic Society, Citation1995) but with a repeatability criterion of 5%. COPD was defined as FEV1/best of VC or FVC <0.70, using the highest value pre- or post-bronchodilation, and severity-grading was based on FEV1% of predicted value according to the Global Initiative for Chronic Obstructive Lung Disease (GOLD) document, GOLD 1–4 (Vogelmeier et al., Citation2017). In 21 cases spirometry was missing, and in those cases the latest previous spirometry was used (2010–2013). The OLIN reference values based on healthy non-smokers were applied for FEV1 (Backman et al., Citation2015).
Data analysis
All analyses were stratified by sex. All individuals with complete data on spirometry and HGS, FACIT-Fatigue or IPAQ, respectively or combinations thereof, were included in the analysis (). Differences in proportions were analyzed with the Chi-2 test, and differences in mean values between groups were analyzed with the student’s t-test. The non-parametric Mann-Whitney u-test was used for non-normally distributed data. P-values < 0.05 were considered statistically significant. The relationships between HGS, fatigue, and physical activity among individuals with respectively without COPD were analyzed by multiple linear regression in three different models, I-III, including fatigue (I), low (II), or both (III). All models were adjusted for age, height, and smoking habits. Statistical analyses were performed with Statistical Package for the Social Sciences, Version 23 (IBM Corporation, Armonk, NY, USA).
Results
Basic characteristics of the study population are shown in . The COPD group included (n = women/men): GOLD 1; n = 87/96, GOLD 2; n = 72/107, and GOLD 3–4; n = 5/14. Respiratory symptoms and current smoking were more common among those with than without COPD. Mean HGS was significantly lower in COPD than non-COPD among both women and men ().
Table 1. Basic characteristics of individuals participating in clinical examination and measure of hand grip strength (HGS), comparing individuals with and without COPD, among women and men, respectively.
Fatigue in non-COPD and COPD by sex, and association with HGS
Among men, but not women, the median FACIT-Fatigue score was lower, and the proportion with clinically relevant fatigue (CRF) was higher in COPD than non-COPD (). Among individuals with COPD, those with CRF had lower mean HGS than those without CRF, significantly so among men (p = 0.001) and close to among women (p = 0.051), while in non-COPD corresponding comparisons were non-significant. Among men with CRF, those with COPD had lower HGS than those without ().
Table 2. Comparing A) fatigue assessed by the FACIT-fatigue questionnaire, and B) physical activity assessed by the IPAQ questionnaire, between individuals with and without COPD, among women and men, respectively.
Table 3. Comparing mean HGS (SD) among those with and without clinically relevant fatigue (CRF) in COPD and non-COPD, among women and men, respectively.
Physical activity in non-COPD and COPD by sex, and association with HGS
Among women, the distribution of the proportions with low, moderate and high physical activity level differed between COPD and non-COPD, and MET min/w was 33.5% lower among women with than without COPD (p = 0.002) (). Corresponding analyses among men revealed no significant differences. In both sexes, the proportion with low physical activity level was similar among those with and without COPD; among women 13.6% and 10.4% (p = 0.386), and among men 18.9% and 13.3% (p = 0.140). HGS was also similar among individuals with low physical activity and moderate-to-high activity in all groups (). Among men with low physical activity, HGS was lower among those with than without COPD, while corresponding findings were found among women with moderate-high physical activity ().
Table 4. Comparing mean HGS (SD) between those with a category of low and moderate/high physical activity level according to IPAQ, among women and men, respectively.
Associations between HGS, fatigue, and physical activity
Among men with COPD, HGS was associated with FACIT-fatigue score also when adjusted for age, smoking habits, and height (model I), and it was independent of physical activity level (model III) (). These associations remained significant also when COPD disease severity, assessed as FEV1% of predicted, was included in the models. Among women with COPD, as well as among men or women without COPD, the corresponding analyses yielded no significant results (). When substituting FACIT-Fatigue score with CRF in the models, the association with HGS among men with COPD in model I, but not in model III, remained significant (Beta = − 2.66, 95% CI −4.61 to −0.70).
Table 5. Multiple linear regression models analyzing the association between HGS, fatigue and low physical activity among A) women and B) men.
Discussion
To the best of our knowledge, this is the first study, which is also a population-based study, to investigate the relationship between hand grip strength, fatigue, and physical activity among men and women, with and without COPD. Among individuals with COPD, those with clinically relevant fatigue had lower mean HGS compared to those without, significantly so among men, and close to among women. There were no differences in HGS when comparing individuals with low physical activity and those with moderate-to-high physical activity in any of the groups. Among men, but not women with COPD, HGS was associated with fatigue also after adjustment for age, smoking habits, and height, and this association was independent of physical activity level as well as disease severity assessed as FEV1% of predicted. Corresponding analyses among individuals without COPD yielded no significant results.
In this report, based on data collected in 2014, mean HGS was lower among individuals with than without COPD, although no such difference was observed in the same cohort 5 years earlier (Strandkvist et al., Citation2016). Without a direct comparison between the groups over time, the differences are hard to evaluate. There may be differences in the process of aging among individuals with and without COPD (MacNee, Citation2016), but also differences regarding muscle strength associated with changes in physical activity over time. However, the observed increased fatigue and decreased physical activity level among individuals with COPD when compared to those without COPD is similar as previously found (Andersson et al., Citation2015; Stridsman, Mullerova, Skar, and Lindberg, Citation2013).
The current study indicates that there is an association between fatigue and HGS among individuals with COPD; those with CRF had lower HGS than those without. Our results correspond well with the findings in a previous study where quadriceps muscle strength predicted both physical and general fatigue among patients with COPD when assessed by the Multidimensional Fatigue Inventory questionnaire (Lewko, Bidgood, and Garrod, Citation2009). In our study, fatigue was associated with HGS independent of height, age, smoking habits, and low physical activity among men with COPD, while corresponding analyses among women yielded no significant results. However, we did no direct comparison between men and women. It has been reported that women with severe COPD suffer more from fatigue than men (Gift and Shepard, Citation1999), while another study concluded that there were no differences in fatigue, nor in functional limitations due to fatigue, when comparing women and men with COPD (Theander and Unosson, Citation2011). The referred studies include selected populations of more severe COPD than our population-based study, and further studies are needed to evaluate possible sex-related differences.
In a study comparing physical activity levels according to both IPAQ and objective accelerometer data, men reported almost 50% more moderate to vigorous physical activity than women, however, when analyzing activity data collected by accelerometer there were no sex differences (Dyrstad, Hansen, Holme, and Anderssen, Citation2014). Assuming that men also in our study over report their level of physical activity, the true proportion of men with low physical activity may be larger. However, we expect this phenomenon to be reasonably evenly distributed in COPD and non-COPD, and should therefore not affect the comparison between groups.
Muscle abnormalities in COPD may be related to inactivity and muscle disuse (Maltais et al., Citation2014). We hypothesized that HGS may be associated with physical activity, but it could not be confirmed, neither among individuals with nor without COPD. Previous studies are contradictory; some have shown associations between HGS and physical activity (Pitta et al., Citation2005), while others have not (van Gestel et al., Citation2012). There might be differences between healthy people and individuals with different diseases; HGS was associated with self-reported physical activity among healthy women, but not men, while the reverse was observed in hospitalized patients among whom HGS was associated with physical activity among men, but not women (Jakobsen, Rask, and Kondrup, Citation2010). A study evaluating the relationship between physical activity and muscle strength among healthy adults found no correlation between self-reported physical activity and HGS, but a significant correlation between accelerometer data and HGS, indicating that different methods of assessing physical activity may yield different results. (Leblanc et al., Citation2015). It is possible that the IPAQ questionnaire is not sensitive enough to differentiate between physical activity levels in this context. On the other hand, HGS might not be the most appropriate method to measure inactivity-related muscle dysfunction, where lower limb muscle strength has a higher prognostic and functional importance (Nyberg, Saey, and Maltais, Citation2015).
One of our hypotheses was confirmed; there was an association between HGS and fatigue among individuals with COPD, and to the best of our knowledge, this has not been shown in a population-based setting before. The relationships between HGS, fatigue and physical activity are complex, however, each of them is a possible target of rehabilitation intervention. A pulmonary rehabilitation program for individuals with COPD may improve muscle strength, fatigue as well as physical activity (Bolton et al., Citation2013). Individuals with COPD suffering from fatigue described that physical activity, such as walks or exercise, contributed to control their fatigue (Stridsman, Lindberg, and Skar, Citation2014). Exercise capacity and the experience of fatigue are associated among both men and women, and it has been suggested that endurance exercise training might have beneficial effects on fatigue (Todt et al., Citation2014). However, fatigue may also be an obstacle to COPD rehabilitation: among patients who chose not to participate or withdrew from the participation in a pulmonary rehabilitation program, lack of perceived benefit and being unwell were central themes contributing to non-participation. A minor theme was the subjective feeling of fatigue; some participants did not attend rehabilitation due to lack of required energy levels, and some felt too tired to complete the program (Keating, Lee, and Holland, Citation2011).
The strength of this epidemiological study is the large study population in which classification of COPD was based on post-bronchodilator spirometry. A majority of those with COPD had mild to moderate disease, GOLD 1 and 2, corresponding to what have been shown by other population-based studies (Lindberg et al., Citation2006). The population-based study design further means that the results will not be affected by the well-known under-diagnosis of COPD, and the results are considered generalizable to COPD in the general population. Another strength is that well-validated methods, measurement of HGS, and questionnaires for assessment of fatigue and physical activity, were used. Further, these three methods are simple, cheap, and easy to implement in clinical practice.
Despite the fact that this study presents new and original data regarding the relationships between HGS, fatigue and physical activity in a population-based setting, it is not possible to evaluate cause and effect due to the cross-sectional study design. Further, when assessing physical activity by a questionnaire, it is common that the study participants overestimate their physical activity, compared to when assessed by objective methods, such as accelerometers (Dyrstad, Hansen, Holme, and Anderssen, Citation2014). However, this bias is probably fairly evenly distributed, and may thus not affect the comparison between groups or the observed significant associations in the current study.
Conclusion
In this population-based study, individuals with COPD and clinically relevant fatigue had lower hand grip strength than those without clinically relevant fatigue, significantly so among men and close to among women. There was no clear association between hand grip strength and level of physical activity within any of the groups. Fatigue was associated with hand grip strength among men with COPD also when adjusted for age, smoking habits, and height, independent of physical activity level and disease severity assessed as FEV1% of predicted. No such associations were found in corresponding analyses among women with COPD or individuals without COPD. The relationships between hand grip strength, fatigue, and physical activity are complex, however, each of them is a possible target of interventions. We suggest further evaluation of these simple and cheap methods, easy to implement in clinical practice, as screening tools to identify individuals with COPD for rehabilitation and for follow-up during rehabilitation programs.
Declaration of interest
The authors declare no conflict of interest toward this study.
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