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Clinical Nutrition (U.G.K., K.M., C.P.)
Clinical Nutrition, Internal Medicine (M.P.-K.)
Geneva University Hospital, Institute of Movement Science and Sports Medicine, Faculty of Medicine, University of Geneva (B.K.)
Geneva, Orthopedics, Lausanne University Hospital, Lausanne (G.G.), SWITZERLAND
Address correspondence to: Claude Pichard, MD, PhD, Head, Clinical Nutrition, Geneva University Hospital, 1211 Geneva, SWITZERLAND. E-mail: claude.pichard{at}medecine.unige.ch
| ABSTRACT |
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Method: Fat-free mass (FFM) and body fat (BF) were assessed by bioelectrical impedance analysis (BIA). Subjects who regularly performed >3 hours per week of endurance type physical activity were classified as "Active". Others were classified as "Sedentary". Subjects were also separated by age (<45 yr vs
45 yr).
Results: FFM increased by 1.7 ± 2.8 kg in men <45 yr who gained 4.0 ± 5.0 kg of body weight and was maintained (0.5 ± 1.6 kg) in women <45 y who gained 1.6 ± 3.0 kg of weight. A weight gain of 1.2 ± 3.3 kg in men
45 yr was accompanied by stable FFM (0.1 ± 2.3 kg), and of 1.0 ± 3.2 kg was accompanied by a loss of FFM in women
45 yr. In active men
45 yr, maintenance of FFM was associated with smaller weight gains than in sedentary; sedentary men
45 yr decreased FFM with larger weight gains than active subjects. Sedentary women <45 yr were able to gain FFM; the active women maintained, but did not gain FFM with smaller weight gains than in sedentary women. FFM decreased in
45 yr women despite of small weight gains.
Conclusion: Weight change is clearly associated with a change in FFM. Weight gain is necessary to offset age-related FFM loss between 20 and 74 yrs. In active men, a FFM increase was associated with less weight gain than sedentary men. Future studies should evaluate the threshold of weight change and the level of physical activity necessary to prevent age-related losses of FFM.
Key words: bioelectrical impedance analysis (BIA), fat-free mass, body fat, BIA-measured FFM, body composition, longitudinal
Abbreviations: BF = body fat BMI = body mass index FFM = fat-free mass
| INTRODUCTION |
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Significant overall weight gains have been recently reported in North American [10] and Europe [11]. Increases in the prevalence in overweight and obesity will also affect the prevalence of excess BF. Weight and body mass index (BMI) alone are not an adequate guide to detect underlying changes in FFM and BF with age and physical activity [7]. Understanding the patterns of weight and body composition changes with aging and the factors that influence body composition can help elucidate the effects that excess body fat or inadequate muscle mass may have on morbidity and mortality.
There is little information available on longitudinal changes in FFM, BF and % BF and the composition of longitudinal weight loss or weight gain [1215]. Gallagher et al [16] found that weight stability masked sarcopenia in elderly subjects. Also in elderly subjects, Hughes et al [14] noted small decreases in FFM and they were masked by wide inter-individual variations that were dependent on the magnitude of weight change. Heitmann et al [15] found that weight changes were associated with more unfavorable relative changes in FFM in men than in women, even after considering age-related changes in FFM and the differences in percentage BF between men and women. However, differences between FFM and BF changes in older, compared to younger subjects has not been explored. Previous data [1,17] have shown that mean FFM peaks in 3544 yr old men and 4554 yr old women and declined thereafter. It is, therefore, possible that patterns of FFM and BF gain and loss may to be different in subjects <45 yr or
45 yr. The stratification of subjects as <45 yr and
45 yr, based on these previously noted body composition changes between 40 and 50 yrs of age [1] appears to be warranted.
In addition, regular physical activity has been shown to prevent body mass gain, and physical inactivity is a risk factor for body mass gain and obesity among adults [6,18]. Thus, the separate evaluation of physically active and sedentary is also warranted.
The purpose of this 8 yr longitudinal study in a cohort of healthy sedentary and physically active men and women, aged 20 to 74 yr was to determine: 1) the longitudinal changes in weight and body composition and 2) the associations of age and physical activity on the longitudinal changes in body composition.
| SUBJECTS AND METHODS |
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45 yr, based on previously noted body composition changes between 40 and 50 yrs of age [1]. The protocol to perform bioelectrical impedance analysis measurements and obtain physical activity, health status, and medication data was approved by the Geneva University Hospital Ethics Committee, and study subjects gave written informed consent.
Anthropometric Measurements and Bioelectrical Impedance Analysis
Body height was measured to the nearest 0.5 cm and body weight to the nearest 0.1 kg on a balance beam scale. Subjects were in indoor clothing without shoes.
FFM and BF were assessed by bioelectrical impedance analysis as previously described [19]. Standardized conditions [24] with regard to body position, previous physical exercise, dietary or fluid intake and skin temperature were observed. Measurements were performed at the same time of day in each subject. In case of the participants to the Geneva fun run, BIA was measured before the race. Whole-body resistance (R) was measured with surface electrodes placed on the right wrist and ankle. Briefly, an electrical current of 50 kHz and 0.8 mA was produced by a generator (Bio-Z2® (Spengler, Paris, France; RJL Systems, Clinton Twp) and applied to the skin using adhesive electrodes (3M Red Dot T, 3M Health Care, Borken, Germany) with the subject lying supine [20]. The skin was cleaned with 70% alcohol before application of the contact electrodes, as previously described [19,21].
FFM was determined by the previously validated Geneva bioelectrical impedance analysis equation [21]. FFM (kg): 4.104 + (0.518 * height2 (cm)/resistance (
)) + (0.231 * weight (kg)) + (0.130 * reactance (
)) + (4.229 * sex (with men = 1, women = 0)). This equation was validated against dual-energy x-ray absorptiometry (Hologic QDR-4500, whole body version 8.26a:3) [21] in adults (n = 343, age 20 to 94 yr) and further validated in healthy elderly subjects (n = 206, age 65 to 94 yrs) [22].
Physical Activity
Subjects completed a brief questionnaire about the number of hours per week and the type, frequency and intensity of their physical activity during the last 4 seasons to take into account the seasonal effect on physical activity in Switzerland. The subjects who performed >3 hours per week of endurance type physical activity, including but not limited to jogging, tennis, gymnastics, skiing and swimming on a regular basis were classified as "Active." The follow-up physical activity category was used to classify subjects. Only physical activity with an intensity code of 4.0 or more as defined by the activity intensity codes classified by the Minnesota Leisure Time Activities Questionnaire [23] were counted. Subjects who reported less than 3 hours of physical activity per week were classified as "Sedentary", as previously reported by our group [5,6].
Statistics
The statistical analysis program StatView, version 5 (Abacus Concepts, Berkeley, CA) was used for statistical analysis. The results are expressed as mean ± standard deviation (x ± SD). Paired and unpaired t-tests were used to identify differences in FFM, BF and % BF by age group (<45 yr versus
45 yr), sex and physical activity level. The differences between weight gain and loss categories were analyzed by analysis of variance (ANOVA), with post-hoc Bonferroni test after one factor analysis. A two-factor ANOVA was used to test for interaction between age, sex and activity and FFM or BF.
In addition, categorical variables were created for relative changes in weight and FFM by using a cutoff of >3%. This cutoff point was based on the reported coefficient of variation for bioelectrical impedance analysis-determined FFM and a change >3% was unlikely to represent only measurement error. For consistency, the change in weight was categorized by using the same cutoff value. Chi2 was used to test differences in incidence of body composition loss, maintenance or gain. Simple regression analysis was used to determine association between weight or FFM change, weight change and FFM change and age. Stepwise multiple regression analysis was used to determine the effects of gender, age, physical activity and baseline body composition parameters on changes in FFM and weight. Statistical significance was set at p < 0.05 for all tests.
| RESULTS |
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45 yr than <45 y men or women (Table 2). Sedentary women
45 yr maintained weight, whereas active women continued to gain weight (Table 3).
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45 yr and women <45 yr had stable FFM with weight gains of >1.2 kg. A weight gain of 1.0 ± 3.2 kg in women
45 yr was accompanied by stable FFM. The weight and FFM changes were greater in men <45 than in women <45 yr both as a percentage of baselines and as a change/yr. In spite of weight gain noted in
45 yr men and women, FFM was stable in men and decreased in women
45 yr. BF changes were greater in men <45 yr and women
45 yr than in men
45 yr and women <45 yr (Table 2).
Physical Activity
Longitudinal changes in FFM and BF in sedentary versus active subjects were variable depending on weight gain (Fig 1). Weight gain was associated with maintenance or gain of FFM in <45 yr sedentary men and active men and
45 yr active men (Fig 1). Sedentary men
45 y were unable to maintain FFM with a weight gain of 3.2 kg. Active <45 yr and sedentary and active
45 yr women were also unable to maintain FFM with weight gains of 0.5 to 1.7 kg. The ANOVA for FFM change, which included sex, age and activity, was significant only for age (<45 versus
45 yr: p < 0.001). There was no interaction between the main effects. The ANOVA for BF change was significant only for the interaction between sex and activity (p 0.02). The ANOVA for weight change was significant for age (<45 versus
45 yr: p 0.03) and sex (p 0.02). There was no interaction between the main effects.
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45 yr were more likely to experience a FFM loss than active younger women, and sedentary women <45 yr were significantly more likely to have high FFM (Fig. 2).
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Predictors of Changes in Body Weight and Body Composition
When classifying the subjects by weight loss or gain category (Fig. 3), it is noted that weight loss resulted in loss of FFM and weight gain resulted in FFM gain and this is seen in both men <45 yr and
45 yr. On the other hand, women
45 y who were weight stable or gained weight and women <45 yr who gained weight lost FFM and this is confirmed by the prevalence of 40% of weight-gaining
45 yr women losing FFM (Fig. 4). Furthermore it is noted that few men and women
45 yr who gained weight also gained FFM (Fig. 4). Weight loss resulted in BF loss and weight gain resulted in BF gain.
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Simple regressions between change in FFM and change in weight (Table 4) show that, with weight maintenance, men would lose 0.12 kg FFM over the follow-up period, whereas women would lose 0.29 kg. Additionally, it indicates that a gain or loss of 1 kg body weight is associated with a gain or loss of FFM of 0.40 kg in men and 0.26 kg in women. Multiple regressions showed that change in FFM was significantly predicted by weight change and age (Table 4). Together they explained 47% of the variance in FFM changes over the follow-up period. FFM changes were unrelated to baseline weight, gender or activity level. Multiple regressions also showed that weight change was independently and inversely predicted only by baseline % BF (Table 4). Weight change was not significantly associated with baseline age, baseline weight, gender or activity level.
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| DISCUSSION |
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45 y, classified as sedentary or active. Our study showed that body weight gain is positively associated with FFM maintenance and has an influence on age-related FFM loss. Physical activity exerted a significant effect on both FFM and BF.
Changes in Body Mass
Significant increases in body weight and BMI were noted both in active and sedentary men and women during the follow-up period. The weight increase after 45 y continued at a lower rate than in younger men. Weight gain in <45 yr old was lower in women than in men and the gain was lower in active than in sedentary women.
BMI increases were somewhat smaller in men (<45 yr: 0.17/y;
45 y 0.10/y) than BMI increases reported in US men [24] (<45 yr: 0.20;
45 yr 0.12) and in women (<45 y 0.12/y;
45 yr: 0.15/y) compared to US women (<45 yr: 0.16/y;
45 yr: 0.18/y). A BMI increase of about 1.01.7 kg/m2 per decade would lead to significant weight increases in Swiss adults and would suggest that the prevalence of overweight is likely to increase in the future in Swiss adults, as has been noted in other European countries [25] and confirms population trends in Switzerland [26,27].
Changes in FFM
Our study shows a clear association between weight gain and FFM gain. Weight-gaining subjects were able to maintain FFM, as long as weight-related FFM gain was greater than age-related FFM loss. In active men, a smaller gain in weight was necessary to maintain FFM than in sedentary subjects, and this is noted in both men <45 yr and
45 yr. The lower weight gain in women than in men resulted in a loss of FFM in women, except in sedentary women <45 yr. Thus, women
45 yr were vulnerable to FFM loss even with weight gain.
The % FFM change per kg weight change was greater in men than in woman, which suggests greater loss or gain of FFM in men than in women. Visser et al [28] and Gallagher et al [16] also reported greater loss of absolute lean mass in older men than in women. In our study over a longer period of time, sedentary men increased their FFM, whereas active women <45 yr who gained less weight lost FFM. This suggests that the weight-related increase in FFM in sedentary women was greater than age-related loss in FFM.
We found that FFM changes were larger in our men and women (Table 2) than those reported in US men and women [24] (men: <45 yr: 0.08 ± 0.45 kg/yr;
45 yr; 0.13 ± 0.63 kg/yr; women: <45 yr: 0.04 ± 0.57 kg/yr;
45 yr: 0.0 ± 0.56 kg FFM/yr). The larger gain in FFM in <45 yr and the smaller loss of FFM in
45 yr per year might be related to higher physical activity levels in our subjects, since 69% reported
3 h physical activity per week. Visser et al [28] and Gallagher et al [16] have reported loss of appendicular skeletal muscle mass, which was masked by simultaneous gain in body fat.
Predictors of Changes in Body Weight and Body Composition
Weight change is clearly associated with a change in FFM [14,29]. There was a moderate correlation between weight change and FFM change (r 0.60, p < 0.001). Multiple regressions confirmed that FFM change was significantly predicted by weight change and age (p < 0.001).
Age is a significant predictor of FFM change in men (r = 0.34, p < 0.002), but not in women (r = 0.25, p < 0.07). The age-related longitudinal changes in FFM (based on linear regression between FFM and age) were 0.9 kg/decade for men and 0.4 kg/decade for women. This is lower than the FFM changes reported in cross-sectional studies of 1.5 kg/decade in men and 0.8 kg/decade in women [30] and longitudinal changes of 1.2 and 0.1 kg FFM per decade in weight-stable elderly men and women, respectively [14]. Our results suggest that the decreases in FFM/decade are smaller in younger subjects than in subjects
45 yr, because higher weight gains in younger subjects contributed to greater gains in FFM than in older subjects. Thus weight-related FFM gains partially offsets the age-related FFM loss in our study. However, we are unable to determine the threshold of weight gain necessary to maintain FFM during aging from our data.
The active men were able to increase their FFM with less weight gain than sedentary men. The active men
45 yr were also able to maintain FFM with smaller gains in weight, whereas FFM decreased in sedentary men
45 yr that had larger weight gains. Sedentary women <45 yr were able to gain FFM, whereas the active maintained, but did not gain FFM with smaller weight gains than noted in sedentary woman. FFM decreased in
45 yr women despite of small gain in weight. These results suggest that physical activity influences the FFM changes with age. Our results also indicate, as suggested by Forbes [31], that physical activity does not prevent FFM loss if weight loss occurs in physically active subjects as a result of an energy deficit.
In healthy subjects, higher FFM has been reported in obese subjects, because more FFM is required to carry excess body weight [32]. Higher FFM appears to be beneficial, especially in older subjects, because it represents greater FFM reserves in case of illness and protects from negative effects of low FFM. Low FFM is a major contributor to the loss of functional ability and health [33]. Further research is necessary to determine the threshold of where high BF outweighs the benefit of high FFM.
Multiple regression analysis (Table 4), however, did not show a significant association between physical activity and FFM change. Our study, therefore, indicated that endurance training is not an independent predictor of changes in FFM. This may be due the fact that physical activity in our study was below the threshold of
1 hour of physical activity per day or that the physical activity levels of greater than 1.41.6 times the basal metabolic rate are necessary for physical activity to show an effect on weight or BMI and body composition [34]. However, resistance training does appear to lower the loss of lean tissue with age [35].
It has been previously shown that there is an inverse relation between physical activity and body fatness, and that body fat reserves change with structured physical activity [36,37]. Because physical activity affects body weight, changes in FFM with age are also influenced by physical activity-related weight changes [18,38,39]. Furthermore, physical activity behavior may differ in subjects with varying levels of obesity [40,41]. The non-significant association between physical activity and FFM change in the multiple regression analysis suggests that physical activity levels of 3 hours per week (30 minutes most days of the week) [42], representing 150200 kcal/day of energy expenditure due to physical activity are inadequate to have a significant effect on body composition. Further research is necessary to determine if physical activity levels of 1.75 times the resting metabolic rate, as recommended by the World Health Organization [43] would have an effect on body composition.
Study Limitations
Limitations of this study are that no information was available about tobacco use or hormone replacement therapy in women. The subjects were volunteers in good health and their body weight was comparable to those reported by Swiss population studies [26], but were not randomly selected and may therefore not be strictly representative of the general population.
The results of the study might have been affect by changes in activity level in the 8-year follow-up period. We classified the subject as "active" or "sedentary" based on the most recent physical activity questionnaire. Thus subjects who were active, but became sedentary would be classified as sedentary and vice versa. Review of follow-up data during the course of the 8-year study period shows that most active subjects remained active throughout the study period and less than 10% of subjects changed activity level classification. We believe that changes in activity level during the course of the study did not affect the results.
With regard to BIA measurements, standardized conditions with regard to body position, previous exercise, dietary intake and skin temperature must be respected [4446]. Consumption of food and beverage may decrease impedance by 4 to 15
over a 2 to 4 h period after meals, representing an error smaller than 3% [44,46]. We did not correct for subjects not having eaten for 4 hours prior to the measurement. The effects of food and beverage have been shown to be small and would not have significantly altered the results because measurements were performed at the same time of day [47].
| CONCLUSION |
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| ACKNOWLEDGMENTS |
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| FOOTNOTES |
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Received December 7, 2004.
Revised December 19, 2005.
| REFERENCES |
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