Abstract
Background
How body composition, specifically skeletal muscle mass, compares in Mexican elderly to other ethnic groups has not previously been reported. We tested the hypothesis that older adults from Northwest Mexico (Mex) would have similar total appendicular skeletal muscle (TASM) compared with New York dwelling Caucasians (Cauc) and African-Americans (AA).
Methods
Two hundred and eighty nine Mex (135 males and 154 females), 166 AA (36 males and 130 females) and 229 Cauc (64 males and 165 females), aged 60–98 years were assessed. Total and regional fat and lean tissues were measured by whole-body dual energy X-ray absorptiometry where TASM is the sum of arm and leg bone-free and fat-free lean tissue. Differences in TASM were tested by ANCOVA, with age, height, and body mass index (BMI) as covariates.
Results
TASM adjusted for ethnicity, age, height and BMI, were 22.6 ± 0.2 kg and 17.8 ± 0.1 kg for males and females, respectively (p<0.001). Among males with similar age, height, and BMI, Mex had less TASM compared with AA and Cauc (p<0.001). Total body fat and truncal fat were higher (p< 0.001) and FFM lower (p<0.001) in Mex compared to both AA and Cauc males after adjusting for age and BMI. Among females, Mex had higher total and truncal fat (p<0.001) after adjusting for age and BMI, and significantly lower TASM (p<0.001) after adjusting for age, height, and BMI compared to AA and Cauc females.
Conclusions
Elderly Mex have a different body composition compared with AA and Cauc of a similar BMI and age. Mex have significantly less TASM with greater total and truncal fat. In the long-term, Mex elderly may be at greater risk for sarcopenic obesity compared to other ethnic groups.
Keywords: Appendicular skeletal muscle, fat mass, BMI, elderly, ethnicity
Introduction
Body composition, more specifically lean tissue and fat masses, over the course of the adult years, are in a dynamic state, with greater changes occurring in some components at specific ages compared to others (1–3). With regard to lean tissue mass of which skeletal muscle constitutes the largest component, the most significant negative changes occur in the senescence phase (aged over 60 y) (4). While body weight reflects the sum of fat and fat free mass (FFM), a stable body weight over time does not infer stability in these two components, as a negative change in FFM concomitant with a positive change in fat mass can result in a stable body weight (5). Thus body weight or body mass index (BMI) should be used with caution as surrogate measures of body composition. Moreover, the well established changes in body composition that occur with advancing age (1–2) combined with the established differences in fat distribution and muscle mass that exist in some ethnic/race groups indicate that BMI is not an appropriate tool for use in individuals or in populations in whom body composition proportions may be different (6–7). Recently, Romero-Corral et al. (8) reported that BMI has a good general correlation with percentage body fat, but it fails to discriminate between body fat and FFM, especially in men and the elderly.
Currently, there is much interest in understanding skeletal muscle mass and its determinants across the age span. Skeletal muscle mass is one of the metabolic and functional components of FFM and it is well known that skeletal muscle is influenced by age, height and gender (9). Longitudinal studies on total appendicular skeletal muscle (TASM) as a proxy for total body muscle mass have shown a significant effect of age in both men and women over age 60 years (2, 5). The clinical implication of the loss of skeletal muscle mass or sarcopenia below a critical threshold relates to impaired functional status and physical disability in older persons (10–12). More recently, sarcopenia has been proposed as an important component of the frailty syndrome in elderly (13).
TASM like other body components differs across ethnicities (14–18). A cross-sectional study in African-American and Caucasian adults (aged 20–70 years) using dual energy X-ray absorptiometry (DXA) estimates of TASM reported an impact of age, gender, and ethnicity, whereby African-American men and women had significantly higher TASM values after adjustment for height, body weight and age, compared with Caucasian groups (14).
The study aim was to test the hypothesis that elderly from Northwest Mexico (Mex) have similar TASM compared with New York dwelling Caucasians (Cauc) and African-Americans (AA). A secondary aim was to ascertain whether arm and leg skeletal muscle differs between these three ethnic groups.
Methods
Subjects
Two data sets containing several anthropometric and body composition variables were pooled. Measurement techniques were considered comparable. Data on African-American and Caucasian elderly came from studies performed at the Body Composition Unit, St Luke's-Roosevelt Hospital, New York, NY between 1993 and 2005. Data on Mexican elderly came from two studies performed in Hermosillo, Sonora, Mexico, between 2003 and 2007.
Six hundred and eighty-four subjects (289 Mex, 135 males and 154 females; 166 AA; 36 males and 130 females and 229 Cauc; 64 males and 165 females) aged 60–98 years were included in the analysis. Subjects were healthy, physically independent, and self-reported weight stable (less than 2 kg change over past 6 months), and were not involved in any type of routine or structured exercise program at the time of the study. Subjects reported to the laboratory in the morning having fasted for a minimum of eight hours, and underwent a medical examination and screening blood test. Subjects were free of known type 2 diabetes, cancer, and heart disease, and were not taking any medication known to affect body composition. Ethnicity for the USA sample was defined as previously reported (18), and the Mexican group was required to report being Mexican from Northwest Mexico. All studies were approved by the Institutional Review Boards at each participating institution, and all subjects gave written consent to participate.
Body composition measurements
Anthropometry
Body weight was measured using an electronic scale (Mexico: Body Composition System Life Measurement Instruments, Concord, CA, USA; New York: Weight Tronix, New York, NY, USA) with subjects barefoot wearing either a tight fitting bathing suit or a hospital gown. At both sites, the standing height was recorded to the nearest 0.5 cm (Mexico) or 0.1 cm (New York) using a Holtain stadiometer (Holtain Ltd., Dyfed, Wales, UK). Body mass index (BMI) kg/m2 was determined from these measurements.
Dual energy X-ray absorptiometry measurements
For all participants, TASM, total body fat (TBF) and regional fat mass, particularly truncal fat, and FFM were estimated by dual energy X-ray absorptiometry (DXA) using GE Lunar DPX-MD+ (Mexico), DPX and DPX-L (New York), GE Lunar Co; Madison, WI, USA. To minimize technical error relating to scan analysis, the scans from Mexico were analyzed by a single technician in the Body Composition Unit in New York using the software version 9.30 for Prodigy. The New York data were analyzed using software versions 1.3z, 3.6y, 4.7d, and 4e.
Subjects were measured in a supine position with arms positioned parallel to the body. The feet were strapped together using a velcro strap as per the manufacturers guidelines. The instruments were calibrated daily using the manufacturer's spine phantom and laboratory soft tissue phantoms as previously described (18).
Body composition analysis was performed according to the defined guidelines with special emphasis on separating the arms and legs from the trunk region (19). The cut lines were placed to distinguish arms from chest, legs from trunk and pelvis from trunk. Appendicular skeletal muscle mass is the sum of bone-free lean tissue in the arms and legs. DXA-derived TASM (kg) assumes that this entity represents limb skeletal muscle mass, with a further assumption that limb skeletal muscle mass represents 75% of total body skeletal muscle mass (20).
Statistical analysis
To test the hypothesis that elderly from Northwest Mexico have a similar TASM compared with Cauc and AA, and to ascertain whether skeletal muscle in the arms and legs differs between these three ethnic groups, an analysis of covariance (ANCOVA) was used, with age, height, and body mass index as covariates. Fisher's LSD multiple comparison test was used to make pair-wise comparisons among the means. Significant differences between groups for age, anthropometric and body composition variables were tested by analysis of variance. An ANCOVA was used to test for significant differences among the races in TBF, truncal fat, arm fat, and leg fat using age and BMI as covariates, and in FFM using age, height, and BMI as covariates. Correlation analysis was used to test the association between TASM and height, body weight, and age by group. Statistical significance was set at p≤0.05 for all tests. Data were analyzed using the statistical program NCSS 2001 (Number Cruncher Statistical System for Windows, Kaysville, UT, USA).
Results
The study sample included a total of 684 subjects (235 men and 449 women) aged 60–98 years, from three different ethnic groups. The age and gender adjusted mean values for BMI were 26.7 ± 0.3 kg/m2 (Mex), 27.8 ± 0.4 kg/m2 (AA) and 27.2 ± 0.3 kg/m2 (Cauc), which were not significantly different across groups (p=0.08). The mean values for total body fat adjusted for age, and BMI, were 26.4 ± 0.2 kg (Mex), 23.8 ± 0.4 kg (AA) and 24.5 ± 0.3 kg (Cauc), where total body fat was significantly higher for Mex compared to the other two groups (p<0.001).
TASM and other variables across gender
TASM was negatively associated with age (r=−0.1114; p=0.0035) and positively associated with body weight (r=0.6565; p=0.0001) and height (r=0.7792; p=0.0001) in the total sample. Within each gender, when TASM was adjusted for ethnicity, age, body mass index and height, men had approximately 5 kg more TASM than women (p<0.001).
After adjustment for ethnic group, there was an effect of gender on several variables: men had significantly higher mean values for age, body weight, and height, but significantly lower BMI compared with women. TASM adjusted for race, age, body mass index, and height was higher in men than women (men 22.6 ± 0.2 kg and women 17.8 ± 0.1 kg of TASM; p<0.001).
Among men, Mex were significantly younger compared with AA (p<0.001) with no between group differences in body weight (Table 1). However, after adjustment for age, Mex weight less than Cauc (p<0.05), and were shorter (p<0.001) than Cauc and AA. However, BMI was not statistically different across ethnic groups in men, even with adjustment for age (p=0.98).
Table 1.
Mexican | African-American | Caucasian | ||||
---|---|---|---|---|---|---|
Variables | Women (n= 154) | Men (n= 135) | Women (n= 130) | Men (n= 36) | Women (n= 165) | Men (n= 64) |
Age, years | 68.2 ± 0.5a | 69.4 ± 0.5a | 71.0 ± 0.7b | 73.6 ± 1.0b | 69.6 ± 0.7ab | 71.6 ± 1.1b |
Body weight, kg | 66.8 ± 1.0a | 74.7 ± 1.1a | 73.0 ± 1.3b | 76.6 ± 2.1a | 70.8 ± 1.2b | 78.4 ± 1.7a |
Height, cm | 155.8 ± 0.5a | 168.6 ± 0.5a | 159.9 ± 0.6b | 171.6 ± 1.3b | 159.3 ± 0.5b | 172.9 ± 1.0b |
BMI, kg/m2 | 27.5 ± 0.4a | 26.2 ± 0.3a | 28.5 ± 0.5a | 26.0 ± 0.7a | 28.0 ± 0.5a | 26.2 ± 0.5a |
BMI= Body mass index. Data are unadjusted mean ± standard error; Within sex between group differences are depicted by different letters (p<0.05).
Among women, Mex were significantly younger than AA, had lower body weight, and were shorter (p<0.0001) than Cauc and AA after adjusting for age (Table 1). After adjustment for age, BMI was not significantly different across the three ethnic groups (p=0.063).
TASM and other estimates across ethnic groups
Among men, TASM was significantly lower in Mex (Table 2) compared with AA and Cauc after adjustment for age, height, and body mass index (p<0.001). There were significant between-group differences in arm skeletal muscle where Cauc had less arm skeletal muscle compared to Mex and AA (p<0.001), and AA men had significantly higher values compared to Cauc and Mex (p<0.001). Leg skeletal muscle was lower in Mex compared with AA and Cauc men (p<0.001).
Table 2.
Men | Women | |||||
---|---|---|---|---|---|---|
Variables | Mexican (n= 135) | African-American (n= 36) | Caucasian (n= 64) | Mexican (n= 154) | African-American (n= 130) | Caucasian (n= 165) |
TASM, kg | 22.6 ± 0.2a | 25.7 ± 0.3b | 24.1 ± 0.2c | 16.0 ± 0.1a | 18.1 ± 0.1b | 16.9 ± 0.1c |
Arms LT, kg | 6.3 ± 0.1a | 6.6 ± 0.1b | 6.1 ± 0.1c | 4.1 ± 0.0a | 4.4 ± 0.0b | 4.0 ± 0.0c |
Legs LT, kg | 16.3 ± 0.1a | 19.1 ± 0.2b | 18.0 ± 0.2c | 11.9 ± 0.1a | 13.7 ± 0.1b | 12.8 ± 0.1c |
FFM,kg | 52.8 ± 0.3a | 57.6 ± 0.6b | 56.6 ± 0.4b | 38.3 ± 0.2a | 42.5 ± 0.2b | 41.6 ± 0.2c |
Total fat, kg | 22.2 ± 0.3a | 18.4 ± 0.6b | 19.9 ± 0.5b | 29.6 ± 0.3a | 27.9 ± 0.3b | 27.9 ± 0.3b |
Truncal fat, kg | 13.9 ± 0.2a | 10.1 ± 0.4b | 11.2 ± 0.3c | 15.5 ± 0.2a | 12.5 ± 0.2b | 13.2 ± 0.2c |
Arms fat, kg | 1.9 ± 0.0ab | 1.7 ± 0.1a | 2.0 ± 0.1b | 3.2 ± 0.1a | 2.9 ± 0.1b | 3.1 ± 0.1ab |
Legs fat, kg | 5.8 ± 0.1a | 5.8 ± 0.3a | 5.8 ± 0.2a | 10.1 ± 0.2a | 11.4 ± 0.2b | 10.7 ± 0.2c |
TASM= Total appendicular skeletal muscle, LT= Lean tissue, FFM= Fat- free mass; Data presented are adjusted mean ± standard error; Within gender between group differences are depicted by different letters by row (p<0.05).
Among women, TASM and leg skeletal muscle were significantly lower in Mex compared with AA and Cauc (p<0.001) after adjusting for age, height, and BMI. Cauc had lower arm skeletal muscle compared with Mexican and AA after adjustment for age, height, and body mass index (p<0.001). AA had significantly higher values for TASM, arm and leg lean tissue (Table 2) compared with both Cauc and Mex after adjusting for age, height, and BMI.
FFM was significantly lower in Mex men and women even after adjustment for age, height and body weight (p<0.001) compared to AA and Cauc groups (Table 2)
Total body fat and truncal fat were higher in Mex men and women (Table 2) compared with AA and Cauc men and women (p<0.0001; adjusted for age, and BMI).
Discussion
To our knowledge, this is the first report that compares estimates of skeletal muscle mass and body composition compartments in apparently healthy, non-institutionalized older Northwest Mexicans, to African-American and Caucasian older adults living in New York City. The main finding of this study is that older Mexican men and women have dissimilar amounts of skeletal muscle mass in spite of similar BMI's.
Within each gender, for a similar BMI, Mex men and women compared with AA and Cauc had significantly greater amounts of total and truncal fat. These findings are consistent with those reported by Fernández et al. (21) who found that the relationship between body fat and BMI in Hispanic-Americans women differed from that of European-American and African-American women, where Hispanic-Americans had a greater total body fat for the same BMI. A number of early studies have shown that ethnicity is an important factor when interpreting the relationships between body fat and BMI (16, 22). Among Chinese, Malay and Indian adults, for the same BMI, the Chinese had the lowest, and Indians the highest body fat (23).
A significant effect of ethnicity was found for other body composition components too. There was an effect of ethnicity on FFM and TASM where Mex men and women had significantly lower TASM and FFM, and higher total and truncal fat compared with AA and Cauc men and women. Recently, it was reported that BMI has a good general correlation with percentage body fat, but BMI fails to discriminate between body fat and FFM, especially in men and the elderly (8). The current study yet again demonstrates the inability of BMI to discriminate between persons who differ significantly in body composition. The latter has implications for the usefulness of using BMI alone when investigating body composition in relation to metabolic disease risk (eg, total and regional fat distribution effects on metabolic derangements) or physical function limitation (sarcopenia or osteopenia/osteoporosis) (24).
It is well recognized that muscle mass is influenced by age, height, body weight, gender, and ethnicity (9, 14, 25–26). The finding of significantly less TASM in Mex for a similar BMI may be related to differences in environmental conditions. It is well recognized that low muscle mass or sarcopenia is related to age, gender, body size or mass, levels of physical activity, and heritability (27–31). Information on levels of physical activity, nutritional intake, and genetic admixture were unavailable in these cohorts.
With respect to the TASM subcompartments in the arms and legs, Mex men and women had significantly less leg muscle compared to AA and Cauc, whereas Cauc men and women had significantly less arm muscle compared to Mex and AA (p<0.0001). The current study cannot address associations between levels of skeletal muscle mass and incidence of physical disability as these data were not collected. However, given that lower extremity muscle mass is an important determinant of physical performance among functionally-limited elders (32), a clinically relevant recommendation arising from the current data is that an intervention program targeted at increasing leg muscle mass in elderly Mex men and women could have merit in avoiding physical disabilities. It is important to point out that independent of ethnicity, increases in physical activity and resistance training are the most effective interventions to retard the loss of skeletal muscle mass in the elderly (33–34). An increase in muscle mass and strength in healthy elderly may have little effect on a specific physical performance, but a small increase in muscle mass among sarcopenic elderly could result in a significant improvement in physical performance despite a relatively small increase in muscle strength (35).
The finding of significantly less TASM in older Mexican compared to AA and Cauc men and women highlights the need to have specific cut-off points for TASM to define sarcopenia in the Mexican population. It is likely that young adult Caucasians and African-Americans have higher levels of skeletal muscle mass compared with age matched Mexican and Latin-American ethnic groups.
In the present study, Mex men and women had higher total body and truncal fat, with less muscle and FFM compared to the other ethnic groups. With respect to FFM, Obisesan et al. (17) using representative data from NHANES III reported an effect of age and ethnicity on FFM. Overall FFM and FFM-index (FFM-index defined as FFM (kilograms) divided by the square of body height (meter2) were significantly higher in black compared with white women, but similar in black compared to white men. In the current study, AA women had significantly higher FFM compared with Mex and Cauc, whereas in men there were no significant differences in FFM between AA and Cauc men. Previously, Casas et al. (15) reported that healthy Hispanic women have higher adiposity and lower amounts of FFM compared with white women. These findings suggest the need to look for sarcopenic obesity instead of sarcopenia alone in some ethnic groups. A recent longitudinal study reported that the elderly with sarcopenic obesity at baseline were two to three times more likely to report onset of disability in instrumental activities of daily living during follow-up than lean sarcopenic or nonsarcopenic obese subjects and those with normal body composition (36).
Limitations of the study
These results should be interpreted with caution due to the cross-sectional design of the study, a relatively small number of subjects per group, and reliance on self-report of ethnicity (especially for AA group where genetic admixtures is likely greater).
Conclusion
Mexican elderly have different body compositions compared with African-American and Caucasian adults of similar BMI and age. Within gender, Mexicans have significantly less TASM and FFM than Caucasian and African-American, for similar age and BMI. Both Mexican men and women have greater total and truncal fat. Overall, Mexicans may be at a greater risk for sarcopenic obesity. For Mexicans, both cross-sectional and longitudinal studies investigating the impact of age and ethnicity and physical activity patterns on skeletal muscle mass are warranted.
Acknowledgments
The studies performed in Mexico were supported by CONACYT (J37891-M) and IAEA (Research contract No. 12694/R0); and studies performed in New York were supported by NIH DK PO1-42618; DK RO1-37352, DK40414; P30 DK-26687; R29-AG14715; and RR24156.
Footnotes
Financial disclosure: None of the authors had any financial interest or support for this paper.
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