Does dynapenic abdominal obesity accelerate the decline in physical performance in older adults?

Background There are few epidemiological evidences of sex differences in the association between dynapenic abdominal obesity and the decline in physical performance among older adults. Objectives To investigate whether the decline in physical performance is worse in individuals with dynapenic abdominal obesity and whether there are sexes differences in this association. Methods A longitudinal analysis was conducted with 3,881 participants of the English Longitudinal Study of Ageing aged 60 years or older in an eight-year follow-up period. The outcome was physical performance evaluated using the Short Physical Performance Battery (SPPB). Abdominal obesity was determined based on waist circumference (> 102 cm for men and > 88 cm for women). Dynapenia was determined based on grip strength (< 26 kg for men < 16 kg for women). The sample was divided into four different groups: non-dynapenic/non-abdominal obese (ND/NAO); non-dynapenic/abdominal obese (ND/AO); dynapenic/non-abdominal obese (D/NAO); and dynapenic/abdominal obese (D/AO). Changes in SPPB performance levels in these groups, stratified by sex, were analyzed using generalized linear mixed models adjusted by sociodemographic, behavioral and clinical characteristics.


Introduction
The decline in physical performance is commonly the first indicator of compromised functioning in Grip strength was measured using a manual dynamometer (Smedley, range: 0 to 100 kg). During the test, the participant remained standing with the arm alongside the trunk and the elbow flexed at 90 degrees 24 . Three maximum strength tests were performed with a one-minute rest period between readings and the highest value was considered for the analysis. Dynapenia was defined as grip strength <26 kg for men and <16 kg for women 25 .
Waist circumference was measured using a metric tape at the midpoint between the lowest rib and the upper edge of the iliac crest. The measurement was made twice at the end of the expiratory phase of the respiratory cycle 24 . A third measurement was performed if the difference between the first two measurements was greater than 3 cm. Abdominal obesity was defined as waist circumference >102 cm for men and >88 cm for women 26 .

Covariates
The socioeconomic variables were sex, age group (60 to 69; 70 to 79; 80 years or more), marital status (with or without a conjugal life), level of education (0 to 11; 12 to 13; >13 years) and total household wealth (quintiles).
Smoking was determined by asking the participants whether they were non-smokers, ex-smokers or current smokers. Regarding alcohol intake, the participants were classified as non-drinkers or rare drinkers (up to once per week), frequent drinkers (two to six times per week) or daily drinkers 28 .
Level of physical activity was determined using an instrument validated by the Health Survey for England 29 that considers the frequency of participation in vigorous, moderate and mild physical activities (more than once per week, once per week, one to three times per months or almost never).
Lifestyle was classified as sedentary (no weekly physical activity) or active (mild, moderate or vigorous physical activity at least once per week) 27 . Health status was ascertained by self-reported doctor diagnosis of diabetes, systemic arterial hypertension, stroke, heart disease, lung disease, cancer, joint disease, osteoporosis and falls in the previous 12 months. Cognitive function was evaluated based on the global score of immediate and delayed recall (range: 0 to 20 words) 30 . Depressive symptoms were determined using the Center for Epidemiologic Studies Depression Scale (CES-D), considering a cutoff of ≥4 points 31 .
The percentage change in weight between waves was analyzed to adjust the models, as weight loss can affect the relation between abdominal obesity and the decline in muscle strength. This variable was categorized as follows: stable weight, weight loss equal to or greater than 5% and weight gain equal to or greater than 5% compared to the previous wave 32 .
All covariates included in the analyses represent a wide range of risk factors associated with the progression of the decline in physical performance 33 . With the exception of age, all variables were treated as time-varying covariates (whenever a variable changes over time for the subjects) 34 .

Statistical analysis
Differences in baseline characteristics between (a) included individuals and those excluded due to missing data on the SPPB, grip strength, waist circumference or other covariates and (b) the four groups classified based on the presence/absence abdominal obesity and dynapenia were evaluated using the chi-squared test, analysis of variance (ANOVA) and Tukey's post hoc test. For all analyses, a p-value <0.05 was considered indicative of statistical significance.
Generalized linear mixed models stratified by sex were used to estimate the trajectories of physical performance using the XTMIXED procedure in Stata 14 SE (Stata Corp, College Station, TX, USA).
These models were chosen because they are more appropriate for unbalanced data from studies with repeated measures and enable the statistical modeling of time-dependent changes in the outcome variable (SPPB) and in the magnitude of associations between variables 35,36 .
The two models (one for each sex) include the interaction between time (in years of follow-up) and the status of abdominal obesity and dynapenia adjusted by the covariables. Univariate analyses were performed to select covariables to incorporate into the final model per sex. Only covariables that presented associations with a p-value ≤0.20 in the univariate analyses were selected for inclusion in the multiple models using the stepwise forward method.
In the final models, the intercept represents the mean estimated difference in performance on the SPPB at baseline between individuals categorized based on the presence/absence of abdominal obesity and dynapenia considering the ND/NAO group as the reference category. On the slope, time (in years) indicates whether the performance on the SPPB declines independently of the presence of covariables (that is, whether time per se is the determinant of the decline). The interaction between time and each status of abdominal obesity and dynapenia represents the estimated difference in the annual rate of decline in performance on the SPPB (slope) between each of the three groups (ND/AO, D/NAO and D/AO) and the reference group (ND/NAO), enabling the assessment of the annual rate of change in the SPPB in the four groups. The rates of the decline in performance were compared using the ß coefficient and 95% confidence interval (CI).
Sensitivity analysis was performed to investigate whether abdominal obesity (yes/no) and dynapenia (yes/no), when analyzed separately, were able to modify the association found between dynapenic abdominal obesity and the decline in physical performance.
In addition, statistics to estimate average population parameters, such as the marginal average, were used from predictions of a previously adjusted model.

Results
Among the 3,881 participants at baseline, 2,962 and 2,481 were reevaluated at the four-year and eight-year follow-up, respectively. Slightly more than 63% and the initial sample participated in the three waves and 76% participated in two waves of the study. The baseline characteristics according to the presence/absence of abdominal obesity and dynapenia, stratified by sex, are displayed in Tables 1 and 2. At baseline, the prevalence of D/AO and ND/AO was slightly higher in women than men ( In the analysis comparing the included individuals and those excluded due to missing data, the excluded individuals were mainly women, older, with no conjugal life, had less schooling and income, smoked more and had more cognitive decline, weakness, abdominal obesity, sedentary behavior, depressive symptoms, lung disease, heart disease, diabetes, systemic arterial hypertension, stroke, arthritis and osteoporosis (p <0.05, data not shown). Table 3  heart disease, stroke, joint disease, depressive symptoms and memory score (Table 3).
In clinical terms, D/AO men showed higher mean SPPB score at baseline compared to D/AO women Compared to the main analysis considering dynapenic abdominal obesity, the results of the sensitivity analysis considering abdominal obesity and dynapenia to be independent conditions showed that although the analyses on the intercept were similar, the analyses on the slope revealed that neither of the two conditions alone was associated with a greater decline in performance on the SPPB (Supplementary Table 1). This highlights the importance of the analytical approach adopted in the present study (considering the influence of combinations of abdominal obesity and dynapenia on the long-term decline in physical performance among older adults).

Discussion
In this population-based cohort, we demonstrated that older English men with dynapenic abdominal obesity have an accelerated decline in physical performance. Moreover, when analyzing abdominal obesity and dynapenia as independent conditions, neither was associated with an accelerated decline in physical performance in either men or women, which highlights the importance of dynapenic abdominal obesity as a clinical condition.
Previous studies offer divergent findings regarding the association between dynapenic obesity and poorer physical performance in older adults. In a cross-sectional study involving 616 men and women aged 60 years or older, Yang and collaborators 13 found that individuals with dynapenic obesity had a poorer physical performance than those who did not have obesity or dynapenia. Bouchard and Janssen 12 report similar results in a cross-sectional study analyzing 2,039 individuals aged 55 years or older. In contrast, Batsis and collaborators conducted a four-year follow-up study involving 2,025 individuals aged 60 years or older and although the authors found that dynapenic obesity was associated with limited physical performance at baseline, this was not confirmed in the longitudinal analyses 37 .
The most likely reason for the differences found between cross-sectional 12,13 and longitudinal 37 analyses seems to reside in how obesity is measured. General obesity indicators, such as the BMI used in the longitudinal study conducted by Batsis et al. 37 , may not capture age-related changes in the distribution of body fat. Therefore, waist circumference seems to be more appropriate for this assessment in older adults, despite not being as accurate.
The sex differences found in the present study may be explained by the different patterns of the decline in muscle strength and the distribution of body fat with aging between men and women. Men exhibit more age-related loss of muscle strength 17,19 and accumulate abdominal fat earlier, with greater intensity and a predisposition towards visceral fat deposition 14,38 . Furthermore, abdominal obesity is associated with a decline in a variety of neural and hormonal trophic signs in the muscles, given the link to chronic inflammation and the reduction in tolerance to glucose 39 . Thus, evidence of the association between abdominal obesity and the exacerbation of the process of dynapenia exclusively in men 40 lends support to the accelerated decline in physical performance in men with dynapenic abdominal obesity. In contrast, the buildup of central fat arises at an older age and in a subtler manner in women 15 , occurring after menopause and with subcutaneous deposition 14 . Thus, a milder production of inflammatory cytokines due to this alternate fat deposition 16 may attenuate the relationship between dynapenic abdominal obesity and the decline in physical performance in women over time.
The fact that both men and women with D/AO began the study with worse SPPB scores compared to their counterparts in the ND/NAO groups highlights the importance of dynapenic abdominal obesity as a clinical condition that affects physical performance. However, the lack of an association between D/AO and a poorer performance on the SPPB in women over time may reflect the smaller effect of abdominal fat on the loss of muscle strength, which was milder in women than men with dynapenic abdominal obesity (p < 0.01, data not shown).
Moreover, the sensitivity analyses showed that by not combining abdominal obesity with dynapenia may lead to neglecting important associations between these conditions and the decline in physical performance, as abdominal obesity and dynapenia alone were not associated with the outcome (Supplementary Table 1). This highlights the importance of the analytical approach adopted in the present study.
This study has several strengths. The major strength is the use of a representative national sample of community-dwelling older adults in England, which enabled us to perform analyses stratified by sex.
The use of objective measures of health and physical performance (waist circumference, grip strength and SPPB) is another strong point. Moreover, the analyses involved data from three waves and a long follow-up period, which enabled us to detect changes in physical performance over time. We also considered the influence of the regional redistribution of adipose tissue during the aging process and our models were adjusted by a wide range of important covariates associated with both the exposure   years, non-smokers, active, without diabetes, without lung disease, without stroke, without joint disease, without osteoporosis, mean Memory Score = 20 and stable weight.

Supplementary Files
This is a list of supplementary files associated with this preprint. Click to download.