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Abstract
Background Grip strength is a well-established predictor of various chronic conditions and all-cause mortality. Body weight and physical activity (PA) are considered potential determinants of muscle strength. This study aimed to investigate gender-specific associations of baseline obesity and physical inactivity with long-term changes in grip strength among middle-aged and older European adults.
Methods Data from the Survey of Health, Ageing and Retirement in Europe 2004–2015 which was conducted in 12 countries were analysed. Grip strength was repeatedly measured at five follow-up visits with average 2-year intervals. Obesity and physical inactivity at baseline were primary exposures. Generalised estimated equations stratified by gender were fitted.
Results This study included 8616 males and 10 088 females with a median follow-up of 9.42 years. Significant interactions between obesity and time with grip strength were identified in both males (χ2 interaction=16.65, p = 0.002) and females (χ2 interaction=10.80, p = 0.029). No significant interaction between physical inactivity and time with grip strength was identified in males (χ2 interaction=9.42, p = 0.051) or females (χ2 interaction=5.62, p = 0.230). Those who were less physically active at baseline had weaker grip strength from the beginning at baseline (β = −2.753, p < 0.001 for males and β = −1.529, p < 0.001 for females) to Visit 6 (β = −2.794, p < 0.001 for males and β = −1.550, p < 0.001 for females). Further combined analysis suggested a trend that exposure to both obesity and physical inactivity was related to the fastest decline rate of grip strength.
Conclusions This study provides the additional evidence that PA and obesity prevention earlier in life play an important role in maintaining grip strength during ageing.
- obesity
- physical inactivity
- grip strength
- prospective study
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Introduction
Hand grip strength, a well-established indicator of overall muscle strength, has been associated with various chronic conditions including cardiovascular diseases, fasting insulin, falls, disability and cognitive decline, as well as all-cause mortality in community-dwelling populations.1–4 Grip strength declines with age from midlife onwards, but within age groups considerable heterogeneity in functions is evident.5 Understanding the determinants for age-related decline of grip strength is important to understand the mechanisms that lead to poor physical function in older adults and develop intervention strategies for active and healthy ageing.
Previous studies on the traditional determinants of muscle strength such as body mass index (BMI) and physical activity (PA) have drawn conflicting conclusions. Cross-sectional evaluations have consistently reported that higher BMI is associated with greater grip strength,6 7 while a retrospective cohort study identified the risk effect of long-term exposure to obesity on poor grip strength later in life.8 Meanwhile, longitudinal observations do not always find the positive associations between PA and muscle strength.9–11 In addition, there is growing appreciation that BMI and PA may have different relationships with grip strength in men and women.6 12
Here, we conducted a prospective study using a large, multiethnic cohort derived from ‘The Survey of Health, Ageing and Retirement in Europe (SHARE)’ 2004–2015 to (1) explore the gender-specific associations of baseline obesity and physical inactivity with long-term change of grip strength and (2) identify the combination effect of obesity and physical inactivity on trajectory of grip strength over time among middle-aged and older European adults.
Methods
Study population
The SHARE is a cross-national and longitudinal European cohort collecting data among adults aged 50 years and over and their partners, regardless of their age. The database contained information such as demographics, health, socioeconomic status as well as social and family networks. Details about the sampling procedure and information collection can be found in the official article.13 Up to now, SHARE 2004–2015 has collected five panel waves (Visit 1, 2, 4, 5 and 6) with average 2-year intervals and a retrospective life history wave (Visit 3). The data for this study were from the five panel waves.14–18 The ethics committee of University of Mannheim and the ethics council of the Max Planck Society reviewed and approved SHARE.
Baseline survey (Visit 1) was conducted in the 11 European countries (Austria, Germany, Sweden, Netherlands, Spain, Italy, France, Denmark, Greece, Switzerland and Belgium) in 2004 and Israel in 2005–2006.19 The average household response rate was 62% and a total of 30 434 people have taken this survey. In all, 5167 individuals were excluded because they did not participant in any of the follow-up visits after baseline. In all, 994 individuals were excluded because they were younger than 50 years at baseline. Those who had related diseases including cancer (n=2485), stroke (n=1784), Alzheimer’s disease (n=740), Parkinson (n=257) and underweight (n=205) at any visit were excluded because it is difficult for them to perform the grip strength test. Additionally, participants who resided in the same household as other SHARE participants were excluded (n=19 for men and n=79 for women) so that all the observations were unrelated. This yielded a total of 18 704 participants (n=8616, 46.1% for men and n=10 088, 53.9% for women) in this study (online supplementary file 1).
Supplemental material
Grip strength
In SHARE, the grip strength was measured using a handheld dynamometer (Smedley, S Dynamometer, 100 kg; TTM, Tokyo, Japan).20 21 Two alternate measures from their right and left hands were performed, expressing as kilogram.20 The highest value of four measures in each visit was used in this study.
Obesity and physical inactivity
Height and weight were self-reported. BMI (kg/m2) was calculated as the weight in kilograms divided by the height in metres squared. The baseline BMI was categorised as nonobesity (18.5≤BMI < 30 kg/m2) and obesity (BMI≥30 kg/m2).
PA was assessed by answers from two related questions of that how often to engage in moderate and vigorous-intensity PA, respectively, in daily life. Possible responses were as follows: ‘more than once a week’, ‘once a week’, ‘one to three times a month’ and ‘hardly ever or never’. Participants who reported ‘more than once a week’ for either vigorous- or moderate-intensity PA and who reported ‘once a week’ for both intensities were grouped as ‘physically active’. Others were grouped as ‘physical inactivity’.22 23
Covariates
The covariates in this study were self-reported via questionnaire at baseline, including age, country, educational level, cigarette smoking, alcohol drinking, depression, heart attack, arthritis, hypertension, hypercholesterolaemia and diabetes. These variables were selected as potential confounders in the relationship between obesity or physical inactivity and grip strength. Based on the International Standard Classification of Education (ISCED 97),24 educational level was categorised as follows: ‘primary level’ (ISCED 0–1), ‘lower secondary level’ (ISCED 2), ‘upper secondary level’ (ISCED 3–4) and ‘ tertiary level’ (ISCED 5–6).25 Depressive symptom was estimated by the Euro-depression (EURO-D) scale with greater score denoting higher level of depression.26 27 Cigarette smoking was categorised as ‘never’, ‘current’ or ‘former’. Alcohol drinking was grouped as ‘frequency more than recommended level’ and ‘frequency no more than recommended level’.28 Heart attack, arthritis, hypertension, hypercholesterolemia, diabetes and osteoporosis were dichotomised as ‘no’ or ‘yes’ based on the answers for the questions of ‘Have you been diagnosed with these problems by a doctor?’
Statistical analysis
We made the stratified analysis by sex. Identified outliers have been winsorised.29 First, mean or percentages were calculated to describe the characteristics of participants. Second, generalised estimated equation (GEE) models with five visits of grip strength as outcomes were conducted. The time variable was interacted with obesity or physical inactivity to identify the independent effects of exposures on the change of grip strength overtime. Third, to assess the combined impact of obesity and physical inactivity on grip strength, we grouped participants for all possible combinations, including nonobesity and physically active, obesity and physically active, nonobesity and physical inactivity as well as obesity and physical inactivity. GEE was carried out to explore the effect of the combined exposures on longitudinal change of grip strength.
All of the GEE models were adjusted for the potential confounders: age, country, educational level, cigarette smoking, alcohol drinking, as well as history of depression, heart attack, arthritis, hypertension, hypercholesterolemia and diabetes at baseline. The main exposures of obesity and physical inactivity were adjusted mutually in the separate analysis.
All the data were analysed using STATA V.14 (Stata Corp LP, College Station, Texas, USA). The p value <0.05 was defined as level of significance.
Results
Descriptive statistics
A total of 8616 males and 10 088 females aged 50 years and older were included in this study. The median of follow-up time was 9.42 years, ranging from 0.92 to 11.58 years. Descriptive statistics of baseline characteristics and five visits of grip strength for participants are presented in table 1. At baseline, the prevalence rates of obesity were 16.7% and 18.3% for males and females, respectively. About 35.9% males and 44.8% females reported physical inactivity. The average grip strength for each follow-up visit was lower, compared with the previous measurement, suggesting the trend of decrease in grip strength over time.
Descriptive statistics of participants (n=8616 for men and n=10 088 for women)
Impact of obesity and physical inactivity
Table 2 summarised the results of GEE. We also conducted the joint tests to assess the changed pattern of the associations between each main exposure and grip strength. Significant interactions between obesity and time with grip strength were identified in both males (joint test: χ2 interaction=16.65, df=4, p=0.002) and females (joint test: χ2 interaction=10.80, df=4, p=0.029). As shown in figure 1A,B, the decreasing rate of grip strength was faster in obesity group than in nonobesity group. Online supplementary file 2 listed the results of grouped comparison in grip strength at each visit. Compared with the participants with normal BMI, the participants with obesity had greater grip strength at baseline (β=1.070, p<0.001 for males and β=0.636, p<0.001 for females). However, no significant difference was found between two groups from the beginning at Visit 4 in males (β=0.044, p=0.897) and Visit 5f in females (β=0.215, P=0.322).
Supplemental material
Longitudinal association of baseline obesity and physical inactivity with grip strength change over time: generalised estimated equations.
Generalised estimated equation examining the associations of baseline obesity and physical inactivity with grip strength measured over median 9.42 years of follow-up
No significant interaction between physical inactivity and time with grip strength was identified in males (joint test: χ2 interaction=9.42, df=4, p=0.051) or females (joint test: χ2 interaction=5.62, df=4, p=0.230), suggesting the decreasing rates of grip strength were similar in active group and inactive group (figure 1C,D). Compared with the individuals with physically active, the individuals with physical inactivity had weaker grip strength from the beginning at Visit 1 (β=−2.753, p<0.001 for males and β=−1.529, p<0.001 for females) to Visit 6 (β=−2.794, p<0.001 for males and β=−1.550, p<0.001 for females) in both males and females.
Models were adjusted for age, country, educational level, cigarette smoking, alcohol drinking, depression, heart attack, arthritis, hypertension, hypercholesterolaemia, diabetes as well as obesity or physical inactivity as appropriate.
Combinations of obesity and physical inactivity
As shown in table 3, joint test identified the significant interactions between time and combination exposures with grip strength in males only (joint test: χ2 interaction=27.72, df=12, p=0.006 for males, χ2 interaction=16.76, df=12, p=0.159 for females). However, the interaction of Visit 6 × (obesity+inactive) on grip strength in females was statistically significant (β=−0.764, p=0.012). As illustrated in figure 2, there was a trend that the exposure to both obesity and physical inactivity predicted fastest decreasing rate of grip strength over time.
Generalised estimated equation examining combined impact of obesity and physical inactivity on longitudinal change of grip strength
Combined impact of obesity and physical inactivity on longitudinal change of grip strength: generalised estimated equations.
Models were adjusted for age, country, educational level, cigarette smoking, alcohol drinking, depression, heart attack, arthritis, hypertension, hypercholesterolemia and diabetes.
Discussion
This large longitudinal study documented three major findings. First, although the individuals with higher baseline BMI had greater grip strength, obesity status at baseline predicted the faster decline of grip strength. Second, no significant difference in the change of grip strength between the physically active group and physical inactivity group was found, higher levels of PA at baseline were significantly associated with stronger grip strength during the follow-up years. Third, the combination of obesity and physical inactivity might accelerate the decline of grip strength in middle-aged and older European adults.
This study showed the faster decline of grip strength in obesity group than in nonobesity group, confirming the observation that the earlier onset of obesity the lower grip strength in old age from the Finland study.8 The real mechanisms underlying the risk effect of obesity on the muscle performance are still not understood. Muscle impairment in individuals with obesity could be related to metabolic changes or changes in muscle architectural components through decreased muscle quality, increased subclinical inflammation, insulin resistance and fat infiltration.30 31
Previous literatures have investigated the longitudinal association of PA with grip strength from various angles. Data from Women’s Health Initiative showed positive associations between time-varying recreational PA and key physical performance measure, including grip strength, chair stands and gait speed over 6 years.32 By using the data from the 1946 British birth cohort, Dodds R identified that those in higher cumulative PA scores to age 53 years were less likely to experience decline in grip strength between 53 and 60–64 years old than those in lower scores, suggesting the protective effect of cumulative PA on the grip strength in early old age.33 A Finland cohort study found no association between PA at mean age 43 and change in grip strength 22 year later.34 Our study suggests that there is no independently protective effect of high baseline PA on longitudinal decline of grip strength over time; however, those who were less physically active at baseline had weaker grip strength during the whole follow-up years. Despite the different study design, all the above-mentioned study supported the view that PA earlier in life plays an important role in maintaining grip strength.
As far as we know, few previous studies focused on combined impacts of obesity and PA on grip strength. Although our data did not show the significant interactions between each visit and each combination exposure, there was a trend that individuals exposed to both obesity and physical inactivity had the weakest follow-up grip strength and the fastest decline rate during the 10 years. These results provide additional evidence for the guideline which recommend that PA and obesity prevention earlier in life are essential for healthy ageing.
A major strength of this study was large number of participants from a long-term prospective study, which gave our statistical analysis sufficient power to draw conclusions. Besides, grip strength was measured five repeatedly in an objective and valid method. Some limitations should be considered. First, when interpreting the findings of this study, it must be emphasised that we have explored the effects of baseline obesity and PA on the change of grip strength. We did not assess the associations of change in BMI and cumulative PA across the life span with grip strength. Second, the spread of follow-up years in this study was huge. Longitudinal data are often incomplete or unbalanced because of loss to follow-up. Previous studies reported that attrition in longitudinal survey was more complex than often assumed and it may not inevitably indicate bias and limit the generalisability of longitudinal comparisons.35 36 Third, self-reported evaluations of the weight and height were prone to reporting bias. Fourth, PA in SHARE did not differentiate between aerobic and strength training which may have skewed findings. Finally, despite controlling for many potential covariates, residual confounding may influence our observed associations between obesity and physical inactivity and change of grip strength.
Conclusion
In summary, results from this large-scale prospective study in middle-aged and older European adults indicated that baseline obesity was associated with an accelerated decline of grip strength. No independently protective effect of high baseline PA on longitudinal decline of grip strength over time was found; however, those who were less physically active at baseline had weaker grip strength during the whole follow-up years. These data support the recommendations that PA and obesity prevention should be engaged earlier in life.
What is already known on this subject?
Previous studies evaluating the associations of obesity and physical activity (PA) with grip strength among middle-aged and older population have produced inconsistent results.
Evidences for the effect of obesity and PA on the long-term change in grip strength are still insufficient.
What does this study add?
This large-scale prospective study in middle-aged and older European adults provide the additional evidence that PA and obesity prevention earlier in life play an important role in maintaining grip strength during ageing.
Acknowledgments
The SHARE data collection has been primarily funded by the European Commission through FP5 (QLK6-CT-2001-00360), FP6 (SHARE-I3: RII-CT-2006-062193, COMPARE: CIT5-CT-2005-028857, SHARELIFE: CIT4-CT-2006-028812) and FP7 (SHARE-PREP: N°211909, SHARE-LEAP: N°227822, SHARE M4: N°261982). Additional funding from the German Ministry of Education and Research, the Max Planck Society for the Advancement of Science, the US National Institute on Aging (U01_AG09740-13S2, P01_AG005842, P01_AG08291, P30_AG12815, R21_AG025169, Y1-AG-4553-01, IAG_BSR06-11, OGHA_04-064, HHSN271201300071C) and from various national funding sources is gratefully acknowledged (see www.share-project.org).
References
Footnotes
Contributors The study was designed by YW, TW, DZ and QT. The data were acquired by TW and YW. The data were analysed and interpreted by TW, YW, SL and WF. The manuscript was drafted by TW, YW, WF and SL. The manuscript for important intellectual content was critically revised by TW and YW. All authors read and approved the final manuscript.
Funding This work was supported by National Natural Science Foundation of China (grant number: 81773506).
Competing interests None declared.
Patient consent for publication Not required.
Provenance and peer review Not commissioned; externally peer reviewed.