Yves Rolland, Valérie Lauwers-Cances, Christelle Cristini, Gabor Abellan van Kan, Ian Janssen, John E Morley, and Bruno Vellas

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1 Difficulties with physical function associated with obesity, sarcopenia, and sarcopenic-obesity in community-dwelling elderly women: the EPIDOS (EPIDemiologie de l OSteoporose) Study 1 3 Yves Rolland, Valérie Lauwers-Cances, Christelle Cristini, Gabor Abellan van Kan, Ian Janssen, John E Morley, and Bruno Vellas ABSTRACT Background: In elders, decreased muscle mass (sarcopenia) and increased fat mass (obesity) may contribute to difficulties with physical function. Objective: The objective was to examine the association of obesity, sarcopenia, and their combination (sarcopenic-obesity) with selfreported difficulties performing physical function in a cohort of community-dwelling elderly women. Design: We assessed muscle and fat mass by dual-energy X-ray absorptiometry and self-reported difficulties with physical function in 1308 healthy women aged 75 y. Sarcopenia was defined as an appendicular skeletal muscle mass 2 SD below the mean in a young female reference group. Obesity was defined as a percentage body fat above the 60th percentile. Thirty-six sarcopenic-obese, 90 purely sarcopenic, 435 purely obese, and 747 women with a healthy body composition were studied. Anthropometric measures, health status, lifestyle habits, and self-reported difficulties with 6 different physical functions were obtained. Results: Compared with women with a healthy body composition and after adjustment for confounders, purely sarcopenic women had no increased odds of having difficulties for all of the physical functions assessed, purely obese women had a 44 79% higher odds of having difficulties with most of the physical functions assessed (P, 0.05), and sarcopenic-obese women had a 2.60 higher odds of having difficulty climbing stairs and a 2.35 higher odds of having difficulty going down stairs (all P, 0.05). Conclusions: Sarcopenia is not associated with physical difficulties in the absence of obesity. However, in the presence of obesity, sarcopenia tends to add difficulty for some physical functions. Am J Clin Nutr 2009;89: INTRODUCTION A decreased muscle mass with aging results in sarcopenia, whereas an increased fat mass results in obesity. Each of these conditions is believed to contribute, at least in part, to difficulties with physical function and increased levels of physical disability (1, 2). Whereas the loss of muscle mass and the gain of body fat with aging may potentiate each other, maximizing their effects on functional limitation in older persons (3), studies thus far have investigated the role of low muscle mass or high body fat separately. Of these 2 common age-related body-composition changes, an increased fat mass may be more predictive of selfreported disability, functional limitation, and poor physical performances than a decreased muscle mass (3). Sarcopenia may only affect physical performance and function in the presence of an increased fat mass (4). Furthermore, the concurrence of both obesity and sarcopenia, a condition known as sarcopenic-obesity, which occurs in 6% of communitydwelling elderly Americans (5, 6), has been reported to be a much more pejorative condition of the development of physical disabilities than either sarcopenia or obesity alone (5). However, a limited number of studies have examined the association between sarcopenic-obesity and physical function among older persons. The aim of this study was to examine the association between different body-composition profiles (obesity, sarcopenia, and their combination) and difficulties with physical function in a community-dwelling population of elderly women. SUBJECTS AND METHODS Data for this study were obtained in the EPIDOS (EPI- Demiologie de l OSteoporose) Study a prospective cohort study whose primary purpose was to assess hip fracture risk factors in a healthy community-dwelling population of elderly women. The sampling and data collection procedures were previously described in detail (7). Briefly, the EPIDOS Study was conducted in 5 French cities (Amiens, Lyon, Montpellier, 1 From Service de Médecine Interne et de Gérontologie Clinique, Hôpital La Grave-Casselardit, Toulouse, France (YR, GAvK, and BV); Unité Inserm 558 (Dr Hélène Grandjean), Faculté de Médecine de Toulouse, Toulouse, France (YR, VL-C, and BV); Laboratoire d Épidémiologie et Santé Communautaire, Faculté de Médecine, Toulouse, France(VL-C and CC); School of Kinesiology and Health Studies and the Department of Community Health and Epidemiology, Queen s University, Kingston, Canada (IJ); and the Geriatric Research, Education and Clinical Center, Saint Louis VA Medical Center and the Division of Geriatrics, Saint Louis University, Saint Louis, MO (JEM). 2 Supported by the Health Minister of France. 3 Address correspondence to Y Rolland, Service de Médecine Interne et de Gérontologie Clinique, Hôpital La Grave-Casselardit, 170 avenue de Casselardit, Toulouse, France. rolland.y@chu-toulouse.fr. Received September 9, Accepted for publication March 12, First published online April 15, 2009; doi: /ajcn Am J Clin Nutr 2009;89: Printed in USA. Ó 2009 American Society for Nutrition 1895

2 1896 ROLLAND ET AL Paris, and Toulouse) from 1992 to All women aged 75 y and living in 1 of the 5 cities were invited to participate by mail through the use of population-based listings, such as voterregistration or health-insurance membership rolls or conferences in associations such as the Third-Age University and advertisements. To be included, women had to live in the community, have no previous history of hip fracture or hip replacement, be able to walk independently, and be able to understand and answer the questionnaire. The present study was limited to the 1454 Toulouse participants who completed a body-composition assessment. All participants gave written informed consent. The program was approved by the Toulouse Hospital ethics committee. Demographic and health assessment The baseline examination was performed in a clinical research center by a trained geriatric nurse. A physical examination and health status questionnaire were used to record comorbid conditions (hypertension, diabetes, coronary heart disease, cancer, stroke, Parkinson disease, depression, or other chronic disease) and pain (pain of the back, hip, knee, ankle, or feet: no, sometimes, or very often). Cognitive impairment was assessed with Pfeiffer s test (8), and a test score,8 was considered low. Alcohol intake and smoking (previous or current) were noted. The highest level of education (illiterate, elementary, primary school, high school, or postgraduate degree) was noted. Participants also self-reported in a structured questionnaire whether they regularly practiced leisure physical activities such as walking, gymnastics, cycling, swimming, or gardening. The type, frequency, and duration of each leisure physical activity were recorded. Women were considered physically active if they practiced at least one recreational physical activity for 1 h/wk for the past month or more. Monthly income was divided into 3 groups:.900v, V, and,450v. Anthropometric measures and body-composition assessment Anthropometric measurements (weight and height) were performed by using standardized techniques (9). Dual-energy X-ray absorptiometry (DXA; QDR 4500 W Hologic, Waltham, MA) was used to measure fat mass and skeletal muscle mass. DXA measurements were performed by a trained technician, and the DXA machine was regularly calibrated. Definition of sarcopenia and obesity Sarcopenia was based on appendicular skeletal muscular mass (ASM) measures (10). ASM corresponds to the sum of the 2 upper and lower limb muscular masses in kilogram. ASM was normalized for height (ASM/height 2 ), and the cutoff to define sarcopenic women was based on previous work (2). Women were classified as sarcopenic if their relative skeletal muscle mass was 2 SDs below the mean of a reference population from the Rosetta Study, which included 229 healthy Americans aged y (11). The cutoff corresponded to 5.45 kg/m 2 in women. Obesity was defined according to total body fat mass assessed by DXA. The cutoff to define obesity was also based on previous work (2, 5). Women were classified as obese if their percentage body fat (% fat mass ¼ fat mass/body weight 3 100) was above the 60th percentile of the present study sample, which corresponded to 40% body fat. On the basis of the sarcopenia and obesity cutoffs, the participants were classified into 4 groups: sarcopenic-obese, purely obese, purely sarcopenic, and healthy body composition. Other variables To further investigate the association between body composition and physical function, body mass index [in weight (kg)/ height 2 (m)], the ratio of fat mass to lean mass, the ratio of fat mass to ASM, the percentage of body fat (% fat mass ¼ fat mass/body weight 3 100), the percentage of lean mass (% lean mass ¼ lean mass/body weight 3 100), and the percentage of ASM (%ASM ¼ ASM/body weight 3 100) were calculated. Physical function assessment Participants were asked by a trained research nurse if they had difficulty (no, some, or serious difficulty) performing different physical tasks: walking, climbing stairs, going down stairs, rising from a chair or bed, picking up an object from the floor, and lifting heavy objects or reaching an object. For each physical task, women who reported some or serious difficulty were considered to have difficulty performing that task; all other women were considered to have no difficulty. We also grouped together women with 3 self-reported difficulties among the 5 physical tasks (walking, climbing stairs, rising from a chair or a bed, picking up an object from the floor, and lifting heavy objects or reaching an object) and called this outcome moving difficulties. Having difficulty performing several functional tasks may better characterize women with high limitations in everyday life than would be characterized based on difficulty performing a single physical function. Statistical analysis Initial analyses described the participant characteristics according to the 4 body-composition groups (healthy, purely sarcopenic, purely obese, and sarcopenic-obese). Continuous variables were expressed as means 6 SDs or as medians and interquartile ranges for skewed variables. Categorical variables were expressed as percentages. Differences between the 4 groups were determined by using analysis of variance (continuous variables) and the chi-square test or Fisher s exact test (categorical variables). Assumptions concerning the normality distribution of residuals and constant SD have been checked. Associations between body-composition status and difficulty with the physical function measures were assessed by using logistic regression. The healthy body-composition group served as the referent group. Age, weight, income, physical activity, level of education, eyesight, pain, hypertension, diabetes, depression, smoking, alcohol, coronary heart disease, cancer, stroke, Parkinson disease, osteoporosis, and cognitive status were considered as covariates in the logistic model. To be included as covariates, these variables had to be related in bivariate analyses to the physical function measure at a P value of Tests were 2-sided, and P values,0.05 were considered significant. To determine whether the risk estimates for physical function were greater in the sarcopenic-obese group than in the purely

3 OBESITY AND SARCOPENIA IN ELDERLY WOMEN 1897 sarcopenic and purely obese groups, additional logistic regression models were run in which the purely sarcopenic or purely obese groups served as the referent. Data analysis was performed by using Stata 7.0 software (Stata Corp, College Station, TX). RESULTS The analyses were conducted in 1308 persons (90% of the 1454 Toulouse EPIDOS participants); 146 women were excluded because of incomplete body-composition information (weight, height, fat mass, or ASM). There was no statistical difference for anthropometric measurements between the 146 excluded women and the 1308 women. Within the 1308 elderly women, 31.2% reported difficulty walking, 41.3% had difficulty climbing stairs, 32.6% had difficulty going down stairs, 22.1% had difficulty rising from a chair or bed, 34.1% had difficulty picking up objects from the floor, 47.6% had difficulty lifting heavy objects or reaching an object, and 34.1% had moving difficulties. The characteristics of the study population according to the 4 different body-composition categories are shown in Table 1. Most of the participants had a healthy body composition based on the study criteria (n ¼ 747; 57.1%), 90 (6.8%) were purely sarcopenic, 435 (33.2%) were purely obese, and 36 (2.75%) were sarcopenicobese. Purely obese women had twice as much fat as purely sarcopenic women (29.8 compared with 14.2 kg). The purely obese group had the highest ASM, whereas the sarcopenic-obese group had the highest ratio of fat mass to ASM and the lowest percentage of ASM. The physical disabilities, on average, were most prevalent in the sarcopenic-obese women (exception: walking and moving difficulties) and least prevalent in the women with a healthy body composition (exception: rising from a chair or a bed, going down stairs). The adjusted odds ratios (ORs) for difficulty with the physical function measures in the 4 different body-composition categories are shown in Table 2. For each of the physical function measures, the ORs were not significantly higher in purely sarcopenic women than in women with a healthy body composition. Surprisingly, purely sarcopenic women were less likely to report having difficulty rising from a chair or bed (OR: 0.46; 95% CI: 0.23, 0.93). Compared with the group with a healthy body composition, purely obese women had a 44 79% higher odds of having difficulties performing the different physical function measures (all significant except for walking and rising from a chair or bed). Compared with the women with a healthy body composition, sarcopenic-obese women had a 2.60 higher odds of having difficulty climbing stairs, 2.35 higher odds of having difficulty going down stairs, and 1.54 higher odds of having moving difficulties (all P values,0.05). The ORs for difficulty walking, rising from a chair or bed, picking up an object from the floor, and lifting heavy objects or reaching an object were not significantly elevated in sarcopenic-obese women. Additional logistic regression analyses were performed to determine whether sarcopenic-obese women had an increased odds of having difficulty with the physical function measures compared with purely obese and purely sarcopenic women. Although the ORs for having difficulty performing the physical function measures tended to be higher in sarcopenic-obese women than in purely obese women, the association was only statistically significant for the going down stairs measure (OR: 2.18; 95% CI: 1.00, 4.74; P ¼ 0.05). Significantly higher ORs for having difficulty climbing stairs (OR: 2.45; 95% CI: 0.99, 6.04; P ¼ 0.05), going down stairs (OR: 3.41; 95% CI: 1.35, 8.57; P, 0.01), and rising from a chair or bed (OR: 2.89; 95% CI: 1.01, 8.30; P ¼ 0.04) were observed in sarcopenic-obese women than in purely sarcopenic women. DISCUSSION In this cross-sectional study, obesity was associated with having difficulty with physical function either or its own or in the presence of sarcopenia. Conversely, sarcopenia was only associated with having difficulty with physical function in the presence of obesity. With only 36 women with sarcopenicobesity, our study was underpowered to test the interaction between sarcopenia and obesity. However, the group of elderly women with sarcopenic-obesity tended to have the greatest likelihood of having difficulty with physical function. Our results reinforce evidence suggesting that higher amounts of body fat are more associated with poor physical performance, functional limitation, and subsequent disability than is low muscle mass (3, 12, 13). Sarcopenia has become an important area of clinical and experimental research because it is considered to be, according to the sarcopenia hypothesis (14), an important contributor to the age-related loss of physical function. Nonetheless, the contribution of a low muscle mass to mobility disability has not been confirmed in most of the epidemiologic studies (4, 15). Our results, and those of other studies (3, 5, 16 19), indicate that sarcopenia is only an important predictor of poor physical function after consideration of the body weight or fat mass of the individual. For example, Newman et al (19) reported that skeletal muscle mass adjusted for both height and body weight, but not height alone, was a significant predictor of mobility limitation in a large sample of elderly men and women. These results must be considered with regard to our definition of sarcopenic-obesity. There is no consensual criteria for defining sarcopenic-obesity, and different approaches have different applications and may result in different conclusions. First, one can create a continuous sarcopenic-obesity index by adjusting muscle mass for weight or fat mass using a regression-based approach (19). Conversely, as done here and elsewhere (5, 6), one could cross-classify subjects using measures of muscle mass and adiposity to create a categorical variable. Whereas the former approach is statistically sound, the later approach has the advantage of being easily interpretable for clinical and public health practice. Second, one could choose to use absolute (kg) or relative (% body fat) measures of adiposity. We, like others (2, 5), defined obesity according to percentage body fat. With this approach, purely obese women tend to have a much higher absolute fat mass than do sarcopenic-obese women (eg, a 5.4-kg difference in this study), and women with a normal body composition tend to have a higher fat mass than purely sarcopenic women (eg, a 3.8-kg difference in this study). Within the present study, the protective effect of pure sarcopenia on difficulties with rising from a chair or a bed might be explained by the lower body weight and fat mass in this group of women than in the normal body-composition group. Janssen and Castaneda (20) attempted to get around this issue by using waist circumference instead of fat mass or percentage fat to define obesity in their sarcopenic-obesity study. Although waist circumference may

4 1898 ROLLAND ET AL TABLE 1 Characteristics of the Toulouse EPIDOS (EPIDemiologie de l OSteoporose) Study participants by sarcopenic-obesity status 1 Characteristics Healthy body composition (n ¼ 747) Purely sarcopenic 2 (n ¼ 90) Purely obese 3 (n ¼ 435) Sarcopenic-obese (n ¼ 36) P Age (y) a, a,b b,c a,c,0.01 Education level (%) Illiterate or elementary 19.9 a 10.0 a,b 19.6 b,c 16.7 a,c 0.01 Primary 36.1 a 45.6 a 44.5 a 47.2 a High school or postgraduate degree 44.0 a 44.4 a 35.9 a 36.1 a Income (%).900 V/mo 58.9 a 63.6 a 56.9 a 58.3 a V/mo 35.4 a 30.3 a 37.9 a 37.5 a,450 V/mo 5.7 a 6.1 a 5.2 a 4.2 a Lifestyle habits (%) Physically active a 50.0 a,b 30.3 b,c 27.8 a,c,0.001 Smoking, former or current 11.7 a 14.6 a 15.0 a 8.3 a 0.34 Anthropometric measures Weight (kg) b c a b,0.001 Height (m) a a a a 0.84 BMI (kg/m 2 ) b c a b,0.001 Fat mass (kg) c d a b,0.001 Lean mass (kg) a b a b,0.001 Appendicular skeletal muscle mass (kg) b c a c,0.001 Fat mass/lean mass 0.5 ( ) b,6 0.5 ( ) c 0.8 ( ) a 0.8 ( ) a,0.001 Fat mass/appendicular skeletal muscle mass 1.3 ( ) c 1.1 ( ) c 1.9 ( ) b 2.0 ( ) a,0.001 Fat mass (%) 33.6 ( ) b 30.2 ( ) c 43.7 ( ) a 43.8 ( ) a,0.001 Lean mass (%) 62.7 ( ) a 64.5 ( ) a 53.4 ( ) b 52.8 ( ) b,0.001 Appendicular skeletal muscle mass (%) 26.8 ( ) a 26.1 ( ) b 23.1 ( ) c 21.7 ( ) d,0.001 Comorbidities (%) Hypertension 44.3 a 45.6 a 52.7 a 41.7 a 0.04 Diabetes 6.1 a 2.3 a,c 4.4 b,c 5.6 a,b 0.35 Coronary heart disease 17.7 a 12.2 a 21.0 a 16.7 a 0.21 Cancer 5.4 a 4.6 a 4.6 a 0.0 a 0.61 Stroke 1.7 a 0.0 a 1.6 a 2.8 a 0.54 Parkinson disease 4.3 a 1.1 a 2.3 a 2.8 a 0.19 Cognitive impairment 15.9 a 15.1 a 12.1 a 8.8 a 0.27 Joint pain (%) 79.7 c 75.6 a,c 86.0 a,b 80.6 b,c 0.02 No 20.3 a 24.4 a,b 14.0 b,c 19.4 a,c Sometimes 49.9 a 36.7 a 46.0 a 47.2 a Very often 29.8 a 38.9 a 40.0 a 33.3 a,0.01 Difficulties with physical function (%) Walking 26.3 c 27.8 a,c 40.5 a,b 33.3 b,c,0.001 Climbing stairs 32.5 b 34.4 b 52.8 a 61.1 a,0.001 Going down the stairs 25.9 b 23.3 b 40.6 a 47.2 a,0.001 Rising from a chair 18.4 a 12.2 a 24.8 b 25.0 a,b,0.01 Rising from a chair or a bed 25.2 a 14.4 a,b 30.3 a 30.6 a 0.01 Picking up an object from the floor 26.8 a 27.8 a,c 41.4 b,c 41.7 a,b,0.001 Lifting heavy objects or reaching an object 41.4 a 48.9 a,c 50.9 b,c 55.6 a,b,0.01 Moving difficulties c 27.8 a,c 42.1 a,b 41.7 b,c, Values in a row with different superscript letters are significantly different, P, 0.05 (ANOVA or chi-square test followed by the Bonferroni test). 2 Women were classified as sarcopenic if their relative skeletal muscle mass was,2 SD below the mean of a sample of 229 healthy young (18 40 y) adults. For women, this cutoff was 5.45 kg/m 2. 3 Women were classified as obese if their percentage of body fat was above the 60th percentile of the study sample. 4 Mean 6 SD (all such values). 5 Defined as participation in a recreational physical activity (hiking, gymnastics, cycling, swimming, or gardening) regularly (1 h/wk) for 1 mo. 6 Median; interquartile range in parentheses (all such values). 7 Defined as 3 difficulties among the following physical functions: walking, climbing stairs, rising from a chair or a bed, picking up an object from the floor, and lifting heavy objects or reaching an object. not be affected by muscle mass when defining obesity, one could also argue that it is not a substitute for whole-body fat mass assessed by DXA. Sarcopenia was not associated with difficulty in physical function in the nonobese but tended to add difficulties in the obese. Mechanistically, this may be explained by the increased load faced by the limited muscle mass in individuals with sarcopenicobesity compared with the purely sarcopenic. Furthermore, excess accumulation of fatty acids around the muscle fibers may interfere with their functioning (21) and thereby reduce muscle quality (muscle strength adjusted for muscle size) within the sarcopenic-obese. In addition, lifestyle habits may help explain

5 OBESITY AND SARCOPENIA IN ELDERLY WOMEN 1899 TABLE 2 Associations between purely sarcopenic, purely obese, or sarcopenic-obese subjects and self-reported difficulties with physical function 1 Purely sarcopenic 2 (n ¼ 90) Purely obese 3 (n ¼ 435) Sarcopenic-obese (n ¼ 36) Physical function difficulty OR 95% CI OR 95% CI OR 95% CI Walking (n ¼ 1252) , , , 3.17 Climbing stairs (n ¼ 1258) , , , 7.74 Going down stairs (n ¼ 1252) , , , 7.08 Rising from a chair or bed (n ¼ 1259) , , , 3.01 Picking up object from floor (n ¼ 1259) , , , 4.34 Lifting heavy objects or reaching an , , , 4.10 object (n ¼ 1252) Moving difficulties (n ¼ 1258) , , , Healthy body composition served as the referent group [odds ratio (OR): 1.00] for the logistic regression analysis. 2 Women were classified as sarcopenic if their relative skeletal muscle mass was,2 SD below the mean of a sample of 229 healthy young (18 40 y) adults. For women, this cutoff was 5.45 kg/m 2. 3 Women were classified as obese if their percentage of body fat was above the 60th percentile of the study sample. 4 Defined as 3 difficulties among the following physical functions: walking, climbing stairs, rising from a chair or a bed, picking up an object from the floor, and lifting heavy objects or reaching an object. our results. In the present study, sarcopenic-obese women were not as physically active as were purely sarcopenic women (Table 1). Although we controlled for physical activity in the regression models examining the relation between body composition and physical function, the measure of physical activity used in this study was rather crude; therefore, we may not have completely controlled for the confounding effects of physical activity in the analysis. The pathway leading to the development of sarcopenic-obesity is unclear at this time. Fat accumulation in the muscle may negatively affect muscle mass through a higher concentration of proinflammatory cytokines (eg, tumor necrosis factor-a and interleukin-6) (22). The excess in proinflammatory cytokines caused by obesity may act synergistically to accelerate the loss of muscle mass and muscle strength (23). Another explanation could be that obesity leads to functional limitation and a sedentary lifestyle, which, in turn, result in a loss of muscle mass and poor muscle quality. Whereas obesity may precede sarcopenia, the reverse is also true. In 2000, Roubenoff (24) suggested that the loss of muscle mass results in lower physical activity, which, in turn, results in reduced energy expenditure, fat gain, and obesity. Because of the cross-sectional nature of this study, we can only speculate as to whether the sarcopenic-obese women were initially purely obese or purely sarcopenic. However, other studies in postmenopausal women have shown that a higher body mass index is a risk factor for loss of muscle mass (25). Furthermore, other prospective cohort studies have noted that the age-related increase in fat mass generally precedes the loss of muscle mass (6). This study had several limitations. First, it was not possible to determine the causal relation between the body-composition profile and physical function measures in this cross-sectional study. Second, the results may not be applicable to men, given that the relation between obesity and functional difficulties has been reported to be modified by sex (26). Third, the physical function measures were self-reported and thus open to selfreporting error and bias. Fourth, our results must be interpreted with regard to the definitions of sarcopenia and obesity adopted in our well-functioning population. Only 36 women, or 2.75% of the total sample, were sarcopenic-obese. 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