Original Communication Age-related differences in fat-free

European Journal Clinical Nutrition (2001) 55, 663±672
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Original Communication
Age-related differences in fat-free mass, skeletal muscle, body cell
mass and fat mass between 18 and 94 years
UG Kyle1, L Genton1, D Hans2, L Karsegard1, DO Slosman2 and C Pichard1*
1
Clinical Nutrition, Geneva University Hospital, Geneva, Switzerland; and 2Nuclear Medicine, Geneva University Hospital, Geneva,
Switzerland
Objective: To determine (1) lean and fat body compartments, re¯ected by fat-free mass (FFM), appendicular
skeletal muscle mass (ASMM), body cell mass (BCM), total body potassium (TBK), fat mass and percentage fat
mass, and their differences between age groups in healthy, physically active subjects from 18 to 94 y of age; and
(2) if the rate of decrease in any one of the parameters by age might be accelerated compared to others.
Methods: A total of 433 healthy ambulatory Caucasians (253 men and 180 women) aged 18 ± 94 y were measured
by dual-energy X-ray absorptiometry (DXA) and whole body scintillation counter (TBK counter) using a large
sodium iodide crystal (203 mm diameter).
Results: The ASMM change (716.4 and 712.3% in men and women, respectively) in > 75 y-old compared to 18
to 34-y-old subjects was greater than the FFM change (711.8 and 79.7% in men and women, respectively) and
this suggests that skeletal muscle mass decrease in older subjects was proportionally greater than non-skeletal
muscle mass. BCM (725.1 and 723.2% in men and women, respectively) and TBK differences were greater than
the differences in FFM or ASMM suggesting altered composition of FFM in older subjects. Women had lower
peak FFM, ASMM, BCM and TBK than men.
Conclusions: The decline in FFM, ASMM, BCM and TBK is accelerated in men and women after 60 y of age and
FFM, ASMM, BCM and TBK are signi®cantly lower than in younger subjects. Fat mass continued to increase
until around 75 y.
Sponsorship: Foundation Nutrition 2000Plus, Geneva, Switzerland.
Descriptors: dual energy X-ray absorptiometry (DXA); total body potassium (TBK); fat-free mass; appendicular
skeletal muscle mass (ASMM); body cell mass (BCM); fat mass.
European Journal of Clinical Nutrition (2001) 55, 663 ± 672
Introduction
Signi®cant changes in body composition are known to
occur with aging and are believed to be a consequence
*Correspondence: C Pichard, Clinical Nutrition and Diet Therapy, Geneva
University Hospital, 1211 Geneva, Switzerland.
E-mail: [email protected]
Contributors: UGK was mainly responsible for the original idea, and
provided the ®nal data collection, executed the mathematical and statistical
analysis, participated in designing the study and in the writing of the paper.
LG and LK organized and coordinated the data collection of the research
project, contributed to interpreting the data and the writing of the paper.
DH and DOS participated in designing the study, analyzing the data and
writing the paper. CP participated in developing the original idea,
designing the study, analyzing the data and writing the paper. He also
directed protocol execution, adherence and funding.
Received 10 October 2000; revised 17 January 2001;
accepted 18 January 2001
of imbalances between energy intake and energy needs
associated with increasing sedentary lifestyle. In addition
to progressive increases in fat mass with age, progressive
reduction in fat-free mass (FFM) is also noted. Large
absolute differences are known to exist between young and
old subjects of similar body size in the individual compartments that compose the FFM (Mazariegos et al, 1994).
Because weight and body mass index (BMI) alone are
not adequate guides of underlying changes in FFM and fat
mass during menopause (Heyms®eld et al, 1994) and aging
in general (Guo et al, 1999), body composition should be
measured in clinical management programs and epidemiological and clinical studies of aging (Guo et al, 1999). Body
composition changes with aging are of interest because the
age-related loss of muscle mass or `sarcopenia' is prevalent
in the elderly and is strongly associated with impaired
mobility, increased morbidity and mortality, and lower
quality of life (Baumgartner et al, 1998; Kehayias et al,
1997; Roubenoff, 2000). Visser et al (1998) also found that
Age-related differences in FFM
UG Kyle et al
664
high body fat mass was an independent predictor of
mobility-related disability in older men and women. High
BMI, increased waist circumference and therefore high fat
mass have also been associated with increased risk for
cardiovascular disease and mortality (Allison et al, 1997;
Heitmann et al, 2000).
Recent advances in body composition measurements
now allow the simultaneous measuring of fat and lean
components and their regional distribution. Dual-energy
X-ray absorptiometry (DXA) is being used to explore
changes in regional fat and muscle mass. Recent studies
(Heyms®eld et al, 1990; Jebb et al, 1993; Wang et al, 1996)
support the validity of DXA-determined estimates of
appendicular skeletal muscle mass (ASMM).
In addition, whole body counting of potassium permits
the evaluation of the quantitative relationship between body
cell mass (BCM), and FFM and their changes during aging.
Total body potassium (TBK) and BCM, the TBK-derived
metabolically active portion of the FFM, are known to
decrease with age. Low TBK values and TBK=FFM ratio
indicate low BCM. However, BCM and FFM do not
maintain a constant relationship to each other across
heterogeneous populations (Gallagher et al, 1996). Thus
de®cient BCM or TBK in older compared to younger
subjects would also indicate de®cient muscle mass.
A number of studies (Bartlett et al, 1991; Deurenberg et al,
1991; Gallagher et al, 1995, 1996; Guo et al, 1999) have
evaluated associations between body composition parameters
and age in healthy subjects. Nevertheless this is the ®rst study
to evaluate lean body parameters (FFM, ASMM, BCM, TBK)
and fat mass, derived from two independent methods, in 433
healthy subjects between 18 and 94 y and compared their
differences between age groups and between genders.
The purpose of this study was to (1) determine lean and
fat body compartments re¯ected by FFM, ASMM, BCM,
TBK, fat mass and percentage fat mass, and their differences between age groups in healthy, physically active
subjects from 18 to 94 y of age; and (2) determine if the
rate of change in any one the parameters might be greater
than the change in other parameters.
Table 1
Subjects and methods
Subjects
Four-hundred and thirty-three healthy ambulatory Caucasians (253 men and 180 women) aged 18 ± 94 y (Table 1)
were included in this study. Subjects were non-randomly
recruited through advertisement in local newspapers and
invitations to participate in the study sent to members of
elderly leisure clubs. Exclusion criteria were acute medical
treatment or hospitalization within 3 months of measurement or physical handicap that might interfere with body
composition measurement (amputation, paralysis, etc).
Each subject was ®rst measured by DXA, then by TBK.
All subjects signed an informed consent statement. The
study protocol was approved by the Geneva University
Hospital Ethics Committee.
Body composition measurements
Body height was measured to the nearest 0.5 cm and body
weight was measured to the nearest 0.1 kg on a balance
beam scale. Height and weight of both men and women
were normally distributed.
Fat-free mass and appendicular skeletal muscle mass.
FFM was measured using whole-body DXA (Hologic
QDR-45001 instrument, Enhanced Whole Body 8.26a software version; Hologic Inc. Waltham, MA, USA). The
precision of the measurements is 1.0 and 2.0% for the FFM
and FM, respectively (Mazess et al, 1990; Slosman et al,
1992). The effective total body radiation dose is 5.2 mSv
(Blake et al, 1996; Lewis et al, 1994). Percentage of body
fat was measured using the manufacturer's default de®nition. Trunk fat mass was determined by DXA as the total
trunk region fat mass, excluding limb and head fat mass.
ASMM was measured as the sum of the lean soft tissue
masses for the arms and legs as described by Heyms®eld
et al (1990). ASMM index, adjusted for differences in body
Anthropometric characteristics of a healthy Caucasian population
Age
18 ± 94 y
Range
18 ± 34 y
35 ± 59 y
60 ± 74 y
Men
n
Height (cm)
Weight (kg)
BMI (kg=m2)
IBW (%)
253
175.3 7.7
77 9.8
25.1 2.8
109.4 12.1
(155 ± 199)
(51.3 ± 106)
(18.8 ± 32.3)
(82 ± 140.9)
68
177.7 6.4
76.0 9.9
24.0 2.6
106.1 11.4
90
178.2 6.7
80.5 9.2*
25.4 2.8*
111.8 12.2*
47
171.6 6.4**
75.8 10.2*
25.8 3.2
111.3 13.7
48
170 8.4
72.9 8.3
25.2 2.5
107.7 9.9
Women
n
Height (cm)
Weight (kg)
BMI (kg=m2)
IBW (%)
180
162.0 6.0
63.0 9.7
24.0 3.5
106.0 15.1
(147 ± 176)
(41.8 ± 92.5)
(17.5 ± 33.9)
(76 ± 151)
40
166.2 4.9
61.4 6.4
22.2 2.1
99.5 9.2
35
163.8 5.2*
62.5 9
23.3 2.8
103.4 12.8
55
161.5 5.5*
66.2 11.4
25.3 4.0*
111.6 17.5*
50
158.0 5.2*
61.2 9.6*
24.5 3.5
106.8 15.5
BMI ˆ body mass index; IBW ˆ ideal body weight (Metropolitan Life Insurance, 1983).
ANOVA comparison between adjacent age groups, *P < 0.05; **P < 0.001.
European Journal of Clinical Nutrition
> 75 y
Age-related differences in FFM
UG Kyle et al
mass and skeletal size, was derived in the same fashion
as BMI: ASMM index (kg=m2 ˆ ASMM (kg) divided by
height (m) squared.
Visser et al (1999) validated the Hologic QDR-4500
instrument in elderly subjects and found FFM was
positively associated with FFM by four-compartment
model (r2 ˆ 0.98, s.e. of estimate ˆ 1.6 kg) and with
computed tomography at all four leg regions (r2 ˆ
0.86 ± 0.96).
Total body potassium and body cell mass. The potassium40 body content was measured by using a whole body scintillation counter. Subjects were reclined in a tilting chair
and were placed in the ®eld of view of a large sodium
iodide crystal (203 mm diameter). The natural K-40 isotope
exists at a known and constant natural abundance of
0.0012%. It was measured by counting the total pulses recorded in the channels of the photo peak of this isotope for
30 min. This technique in humans, at our institution, has an
accuracy of 5% and a precision of 2% (Wenger & Soucas,
1964). Others reported a variability of potassium-40 counting in an anthropometric phantom is > 5% and in humans
around 5% (Lukaski et al, 1981).
BCM was calculated from TBK using the equation,
BCM (kg) ˆ 0.00833 TBK (mmol) (Moore & Boyden,
1963).
Physical activity
In subjects > 60 y, physical activity was determined using
a frequency questionnaire (Bernstein et al, 1999). The time
spent on total physical activity was calculated by multiplying the frequency and duration of each activity in the
previous week, summing the values across activities, and
dividing by 7. Intensity scores, previously reported (Voorrips et al, 1991), were used to make the differences in
energy expenditure of the various activities and sports
activities comparable. The intensity scores are based on
net energy cost of activities in mega joules per hour (Bink
et al, 1966).
Statistics
Descriptive statistics were calculated for height, weight,
percentage ideal body weight, BMI, FFM, ASMM, BCM,
TBK, TBK=FFM ratio, fat mass and percentage fat mass,
and are expressed as mean standard deviation (x s.d.)
ANOVA was used to test for differences between age
groups. Differences for body composition parameters for
each age group compared to healthy young subjects (age
18 ± 34 y) were calculated as: percentage difference ˆ
x 7 y=y 100, where x is FFM, BCM etc of each individual and y is the mean value for FFM, BCM etc of the 18 to
34-y-old men or women.
Height-normalized FFM, ASMM, BCM, TBK,
TBK=FFM ratio, fat mass and percentage fat mass were
plotted against age to compare decreases in < 60 y com-
pared to > 60-y-old subjects and determine if decreases
with age in some parameters might be greater than
decreases in others. The height was normalized to the
median height of all men or women: 175 cm for men and
161.2 cm for women, respectively. Differences between
two or more population regression coef®cients were
tested as previously described (Zar et al, 1999). Statistical
signi®cance was set at P 0.05 for all tests.
665
Results
Table 1 shows the anthropometric characteristics of the
healthy subjects between 18 and 94 y of age. Height was
signi®cantly lower in 60 to 74-y-old than 35 to 59-y-old
men and weight was highest in 35 to 59-y-old men. Height
was signi®cantly lower in 60 to 74-y-old than 35 to 59-yold women and 35 to 59-y-old than 18 to 34-y-old women.
Weight was highest in 60 to 74-y-old women and was
signi®cantly lower in older age groups. Peak BMI and
percentage ideal body weight were noted in 60 to 74-y-old
for both genders and were lower in younger and older age
groups.
Fat-free mass and appendicular skeletal muscle mass
FFM, ASMM and ASMM index peaked in men (Table 2,
height adjusted Table 4) in 35 ± 59 y and were signi®cantly
lower in older age groups. In women, FFM, ASMM and
ASMM index (Table 3, height-adjusted, Table 4) were
highest in the 18 to 34-y-olds and became gradually
lower and were signi®cantly lower after 60 y of age
compared to younger subjects.
The FFM and ASMM changes as a percentage by which
the parameters were lower than values in healthy men and
women aged 18 ± 34 y are shown in Tables 2 and 3,
respectively. The percentage change in ASMM was greater
than the percentage change in FFM and this suggests that
skeletal muscle was proportionally smaller than nonskeletal muscle mass in older men and women.
The FFM (calculated from linear regressions in Figure 1)
was 1.5 kg=decade lower in men and 0.8 kg=decade in
women when reported as overall change and 1.7 kg=decade
in men and 1.1 kg=decade noted in > 60 y women compared a 0.4 kg=decade in men and 0.3 kg=decade higher
FFM in women < 60-y-old subjects. Similarly, the changes
were much greater in > 60-y-old (71.0 kg=decade in men
and 70.4 kg=decade in women) compared with stable
ASMM in < 60-y-olds.
Total body potassium and body cell mass
BCM, TBK and TBK=FFM ratio were highest in the 18 to
34-y-olds, became gradually lower and were signi®cantly
lower in > 60-y-old compared with younger men (Table 2,
height adjusted Table 4) and women (Table 3, height
European Journal of Clinical Nutrition
Age-related differences in FFM
UG Kyle et al
666
Table 2
Body composition changes with age in healthy men
Age
n
Fat-free mass (kg)
Da (%)
ASMM (kg)
Da (%)
ASMM index (kg=m2)
Da (%)
Body cell mass (kg)
Da (%)
BCM=FFM (kg=kg)
Total body potassium (g)
Da (%)
TBK=FFM (g=kg)
Da (%)
Fat mass (kg)
Da (%)
Fat mass (%)
Da (%)
18 ± 94 y
18 ± 34 y
35 ± 59 y
60 ± 74 y
< 75 y
253
60.4 6.6
68
62.3 6.1
25.8 3.6
27.2 3.0
8.38 0.85
8.59 0.76
31.5 5.2
34.8 3.8
0.52 0.05
147.8 24.2
0.56 0.04
163.4 17.9
2.44 0.25
2.63 0.20
16.7 5.4
14.0 4.8
21.4 5.3
18.1 4.9
90
63.3 5.6
70.7 8.8
27.5 3.0
0.5 10.9
8.66 0.82
0.7 9.5
34.0 3.5
71.1 10.3
0.54 0.04{
159.7 16.6
71.1 10.3
2.53 0.16{
72.1 6.3
17.3 5.3{
11.7 34.2{
21.2 4.9{
8.5 24.8{
47
57.3 5.5{
78.3 9.0{
23.8 2.7{
12.1 10.6{
8.10 0.82{
75.8 9.6*
28.0 2.7{
717.5 8.9{
0.49 0.04{
131.6 12.5{
717.5 8.6{
2.30 0.18{
710.7 6.8{
18.6 5.5
19.1 35.9
24.0 4.6{
21.7 23.9*
48
55.1 6.0
712.4 9.5*
22.7 2.9
17.2 10.5*
7.84 0.75
78.8 8.7{
25.4 3.6{
726.3 10.5{
0.46 0.04{
119.2 17.0{
726.3 10.5{
2.16 0.18{
716.2 7.0{
17.6 4.7
13.7 30.2
24.0 4.9
22.9 25
ASMM ˆ appendicular skeletal muscle mass; TBK ˆ total body potassium; FFM ˆ fat-free mass.
Percentage difference compared to 18 to 34-y-old group.
ANOVA comparison between adjacent age groups (adjusted for height and weight), *P < 0.05; {P < 0.001.
a
adjusted Table 4), and were also signi®cantly lower in 35 to
59-y-old compared with 18 to 34-y-old woman. The TBK
change was greater in men (78.7 g=decade) than in women
(75.4 g=decade) and greater in > 60-y-old than < 60-yold men and women (Figure 2).
The percentage change in TBK and BCM (Tables 2 and
3) was approximately twice the change in FFM and
ASMM. The BCM=FFM ratio was also signi®cantly
lower in older men and women. Thus it appears that the
BCM and TBK changes are greater than changes in either
FFM or ASMM. Women had lower peak FFM, ASMM,
BCM and TBK than men.
Table 3
Changes in body composition in > 60-y-old compared
to < 60-y-old subjects
Linear regressions for changes in height-adjusted body
composition parameters for men and women, separated
into < 60 and > 60 y, are shown in Figures 1 ± 3. The
slopes of the regressions for FFM and ASMM (Figure 1)
were non-signi®cantly positive in < 60-y-old men and
women and signi®cantly negative in men > 60-y-old
(FFM P 0.015; ASMM P 0.007) and non-signi®cantly
negative in women. The change in FFM in > 60-y-old was
greater in men than in women.
Body composition changes with age in healthy women
Age
n
Fat-free mass (kg)
Da (%)
ASMM (kg)
Da (%)
ASMM index (kg=m2)
Da (%)
Body cell mass (kg)
Da (%)
BCM=FFM (kg=kg)
Total body potassium (g)
Da (%)
TBK=FFM (g=kg)
Da (%)
Fat mass (kg)
Da (%)
Fat mass (%)
Da (%)
18 ± 94 y
18 ± 34 y
35 ± 59 y
60 ± 74 y
> 75 y
180
42.8 4.6
40
45.0 3.6
17.2 2.3
18.5 1.9
6.55 0.68
6.71 0.58
20.8 3.5
24.1 2.5
0.49 0.06
97.7 16.4
0.54 0.04
113.3 11.6
2.28 0.26
2.52 0.21
20.7 7.2
17.3 5.8
31.6 6.6
26.9 4.6
35
44.4 4.2
70.4 9.3
18.0 2.2
71.8 11.9
6.69 0.65
70.1 9.6
22.6 2.6*
74.4 11.2*
0.51 0.04*
106.0 12.3*
74.5 11.1{
2.39 0.19*
74.1 7.4*
18.6 5.6
8.2 32.5
29.0 5.2
6.8 19.3
55
42.5 4.6*
74.6 10.3*
16.9 2.2*
77.6 12.2*
6.47 0.69
73.4 10.3
19.9 2.7{
715.5 11.4{
0.47 0.05{
93.4 12.7{
15.9 11.4{
2.19 0.21{
712.1 8.4{
24.1 8.4{
40.3 48.9{
34.9 6.6{
28.6 24.5{
50
40.2 4.2*
710.0 9.5*
16.0 2.1*
712.7 11.4*
6.40 0.74
74.4 11.0*
17.9 2.5{
724.0 10.6{
0.45 0.04*
84.2 11.7{
24.2 10.5{
2.10 0.20*
715.8 8.l{
21.1 6.4*
22.8 37.1*
33.8 5.9
24.5 21.7
ASMM ˆ appendicular skeletal muscle mass; TBK ˆ total body potassium; FFM ˆ fat-free mass.
Percentage difference compared to 18 to 34-y-old group.
ANOVA comparison between adjacent age groups (adjusted for height and weight); *P < 0.05; {P < 0.001.
a
European Journal of Clinical Nutrition
Age-related differences in FFM
UG Kyle et al
667
Figure 1 Fat-free mass (FFM) (top) and appendicular skeletal muscle mass (ASMM) (bottom), normalized for height (men ˆ 175 cm, women ˆ 161.2 cm)
vs age in 18 to 59-y-old (left) and 60 to 94-y-old (right) men and women.
Table 4 Height-adjusteda body composition changes with age in healthy men and women
Age
18 ± 94 y
18 ± 34 y
35 ± 59 y
60 ± 74 y
> 75 y
Men
n
Fat-free mass (kg)
ASMM (kg)
Body cell mass (kg)
Total body potassium (g)
TBK=FFM (g=kg)
Fat mass (kg)
253
60.2 5.1
25.7 2.9
31.4 4.4
147.2 20.8
2.44 0.24
16.7 5.4
68
61.3 4.9
26.7 2.5
34.3 3.4
160.8 15.8
2.59 0.23
13.7 4.6
90
62.1 4.4
27.0 2.6
33.4 3.1
156.8 14.3
2.48 0.20{
17.0 5.3{
47
58.4 4.8{
24.5 2.4{
28.6 2.5{
134.2 11.6{
2.35 0.20{
18.9 5.5*
48
56.6 4.4
23.3 2.3
26.1 3.l{
122.5 14.5{
2.23 0.21*
18.2 4.9
Women
n
Fat-free mass (kg)
ASMM (kg)
Body cell mass (kg)
Total body potassium (g)
TBK=FFM (g=kg)
Fat mass (kg)
180
42.5 3.6
17.1 2.0
20.7 3.0
97.0 14.2
2.26 0.25
20.6 7.2
40
43.7 2.9
18.0 1.6
23.4 2.3
109.9 10.9
2.45 0.23
16.8 5.7
35
43.7 3.2
17.7 1.8
22.2 2.2*
104.2 10.5*
2.35 0.20
18.2 5.3
55
42.4 3.9
16.9 2.0*
19.9 2.4{
93.0 11.1{
2.18 0.21{
24.0 8.3{
50
40.9 3.6*
16.3 1.9
18.3 2.3{
85.8 10.8{
2.14 0.22
21.5 6.4
ASMM ˆ appendicular skeletal muscle mass; TBK ˆ total body potassium; FFM ˆ fat-free mass.
Parameters normalized for median height in all subjects (175 cm for men, 161.2 cm for women).
ANOVA comparison between adjacent age groups, *P < 0.05; {P < 0.001.
a
European Journal of Clinical Nutrition
Age-related differences in FFM
UG Kyle et al
668
Figure 2 Body cell mass (BCM) (top), and total body potassium (TBK) (middle), TBK=FFM ratio (bottom), normalized for height (men ˆ 175 cm,
women ˆ 161.2 cm) vs age in 18 to 59-y-old (left) and 60 to 94-y-old (right) men and women.
The BCM and TBK (Figure 2) were non-signi®cantly
lower in men < 60 y, but signi®cantly (P 0.006) in women
< 60 y and men and women > 60 y (P 0.001). TBK=FFM
European Journal of Clinical Nutrition
was signi®cantly lower in men and women < 60 y and
> 60 y (P 0.010). The BCM, TBK and BCM=FFM ratio
(not shown) decreases were greater in women than in men
Age-related differences in FFM
UG Kyle et al
< 60 y and in men than in women > 60 y. The slopes of the
regression for TBK=FFM ratio in younger and older subjects and BCM=FFM ratio in older subjects (data not
shown) were similar in men and women.
Signi®cant differences (P ˆ 0.001) existed between
regression coef®cients between men and women and
< 60 y and > 60-y-old for each parameter in Figures 1 ± 3,
except for TBK=FFM ratio between men and women
> 60 y and men and women < 60 y.
Fat mass and percentage fat mass
Both absolute and percentage fat mass were highest in 60 to
74-y-old men (Table 2, height adjusted Table 4) and
women (Table 3, height adjusted Table 4) and remained
stable thereafter, except for fat mass which was signi®cantly lower in > 75-y-old women. The percentage fat
mass change was greatest in 60 to 74-y-old men and
women and was greater in women than in men.
Trunk fat mass was higher (P 0.0001) in 60 to 74-yold (9.8 3.5 kg) than in 18 to 34-y-old men (6.5 2.7 kg)
and in 60 to 74 y (10.9 4.37 kg) than in 18 to 34-y-old
(6.2 2.0 kg) women, and was lower thereafter (70.6 kg in
men and 71.2 kg in women). The trunk fat mass, as a
percentage of total fat mass, changed from 45.6 to 52.21%
in youngest vs oldest men and from 36.7 to 45.2% in
women. Appendicular (leg and arm) fat mass was also
higher (7.7 2.3 kg) in 60 to 74-y-old compared to youngest (6.5 2.2 kg) men (P 0.016) and in women
(12.0 4.0 kg compared to 9.6 2.4 kg respectively,
P 0.005) and decreased thereafter (70.2 kg in men and
71.3 kg in women). Appendicular fat mass as a percentage
of total fat mass was lower (P ˆ 0.0001) in older (42.2%)
compared to youngest men (46.9%) and older (50.8%)
compared to youngest (57.3%) women and remained
stable after 75 y.
Fat mass and percentage fat mass (Figure 3) became
signi®cantly higher (P 0.02) in men and women < 60 y
and remained stable > 60 y in men and women.
Discussion
The loss of FFM and muscle mass and increased fat mass
with aging has been documented in a number of studies
using a variety of methods and it appears to occur even in
relatively healthy elderly persons (Baumgartner et al, 1995;
Gallagher et al, 1995). This is the ®rst study to evaluate
lean body parameters (FFM, ASMM, BCM, TBK) and fat
mass, derived from two independent methods, in 433
healthy subjects between 18 and 94 y and compare their
differences between age groups and between genders. The
results show that the parameters re¯ecting lean body mass
changed at a faster rate after 60 y of age in both men and
women and were signi®cantly lower in older men and
women.
Fat-free mass and appendicular skeletal muscle mass
669
Our study shows that the height-adjusted FFM and
ASMM remained stable until 60 y of age but that there
was an accelerated change in FFM and ASMM after 60 y.
Our results agree with Kehayias et al (1997), who
reported a decrease in TBK between 20 and 90 y and an
accelerated loss in older subjects. The relatively stable
FFM seen until 60 y in this study has been reported by
others (Chumlea et al, 1999; Pichard et al, 2000). In a
comparison between a small number of younger (n ˆ 19,
29.9 4.4 y) and older women (74.2 6.7 y), Mazariegos
et al (1994) found lower FFM, ASMM and BCM in
weight-matched older women. The FFM and ASMM
change in our study was greater in men than in women,
con®rming results by others (Gallagher et al, 1995).
Gallagher reported linear decreases in ASMM between
20 and 90 y and suggested that a nonlinear decrease was
not found in their subjects due to limited inclusion of very
old subjects.
However, the accelerated changes noted in FFM and
ASMM after 60 y has not been previously reported, primarily because few studies (Gallagher et al, 1995; Starling
et al, 1999) have investigated ASMM across the age span
of 20 ± 94 y.
The greater percentage decrease in ASMM than in FFM
would suggest that the loss of skeletal muscle mass is
greater than loss of non-skeletal muscle mass, and this is
con®rmed by the ASMM index which indicates loss of
muscle mass after controlling for body mass. These results
agree with Cohn et al (1985) who reported a greater
decrease with age in muscle than non-muscle lean (organ)
mass and TBK.
Total body potassium and body cell mass
BCM and TBK (Table 2 and Figure 2) changes were found
to be greater than the changes in FFM and ASMM and
greater in > 60 y than < 60 y men and women. TBK and
BCM were approximately 25% lower in oldest than youngest men and women.
The results of this study also indicate that BCM and
FFM do not maintain a constant relationship to each other
with aging. This is con®rmed by the signi®cantly lower
BCM=FFM ratio and lower TBK=FFM ratio with age.
These ®ndings agree with those from other studies (Cohn
et al, 1985) reporting a greater change with age in TBK
than FFM.
Mazariegos et al (1994) postulated that the lower FFMto-protein ratio found in their older women was possibly
due to a relative increase in connective tissue=structural
protein with age, which would explain the lower decrease
in ASMM than BCM. They found inconsistent differences
between three markers of skeletal muscle: TBK, ASMM
and cross-sectional limb muscle area by anthropometrics.
As in our study, they found ASMM to be 11% and TBKdetermined BCM 17% lower in older women. Our study
European Journal of Clinical Nutrition
Age-related differences in FFM
UG Kyle et al
670
Figure 3 Fat mass (top) and percentage fat mass (bottom), normalized for height (men ˆ 175 cm, women ˆ 161.2 cm) vs age in 18 to 59-y-old (left) and 60
to 94-y-old (right) men and women.
also found similarly lower ASMM and BCM in men. They
suggested that skeletal muscles atrophy with increasing age
and that the atrophied muscle is characterized by loss of
myo®brils and associated loss of potassium and increased
extracellular ¯uids, connective tissue and fat (Lowry &
Hastings, 1942). The replacement of cell mass by collagen
and the relative expansion of extracellular ¯uid in elderly
subjects would explain the lower changes in ASMM than in
BCM. Baumgartner et al (1995) suggested that the active
cell mass may be replaced to a greater extent in women
than in men, but had no explanation for this apparent sex
difference.
Lexell et al (1983) found 18% smaller muscle size and
25% fewer number of muscle cells at autopsy in elderly
men (70 ± 73 y) than in young men (19 ± 37 y), which is
close to the 16% lower ASMM and 25% lower BCM noted
in this study. Thus sarcopenia in elderly subjects may be
due to muscle atrophy due to a gradual and selective loss of
European Journal of Clinical Nutrition
cell mass, and a decrease in number and size of muscle
®bres (Lexell et al, 1995). The results of this study show
that ASMM and BCM appear to parallel the gradual loss of
cell mass and muscle ®bre loss noted with increasing age.
Fat-free mass and physical activity
Results from a physical activity questionnaire completed by
all > 69-y-old subjects in our study, results reported elsewhere (Kyle et al, 2001) revealed no physical limitations or
restrictions in mobility in the older subjects in this study.
The lower FFM, ASMM and ASMM index noted in our
older subjects did not appear to cause physical disability or
loss of functioning, since all of the subjects were fully
independent, without limitations in mobility and reported
relative high physical activity levels (men ˆ 202 108 min=day, women ˆ 222 98 min=day, and < 20.9%
of men and < 15% of women reported < 120 min=day of
Age-related differences in FFM
UG Kyle et al
physical activity). Thus FFM, ASMM and BCM appear to
decrease as part of normal aging and in spite of considerable activity reported by the older adults in this study.
Activities reported were predominantly walking, general
household and gardening activities which are not generally
considered `body building or strength activities' and thus
would not necessarily have prevented muscle wasting, but
would have contributed to maintenance of body weight.
Visser et al (1998) did not ®nd that low skeletal mass was
associated with self-reported disability. However,
they could not rule out that persons with low skeletal
muscle mass dropped out earlier in the study. Further
research should be directed at determining the threshold of FFM and ASMM necessary for normal physical
functioning.
Fat mass
Our results show that fat mass accumulates with age in men
and women until 74 y and decreases slightly thereafter in
women. These ®ndings agree with Bartlett et al (1991),
Pichard et al (2000) and Kyle et al (2001) who found that
fat mass increased beyond middle age, but contradicts
®ndings by a previous report (Chumlea et al, 1998) that
there is little or no further gain in fat mass during old age.
In addition, our data con®rms previous reports (Baumgartner et al, 1995) that fat mass, in terms of percentage fat
mass, may be relatively stable in elderly men but may
decrease with age in elderly women. Fat mass gain was
lower in our subjects < 60 y (0.21 kg=y in men and
0.14 kg=y in women) compared to 0.37 kg=y and 0.41 kg=y
reported by Guo et al (1999) in men and women, respectively, and may be explained by lower rates of weight gain
with age in our subjects, Percentage fat mass was lower in
our subjects than in subjects with higher weights reported
by Cohn et al, (1985).
We found trunk and appendicular fat mass became
progressively higher until 60 ± 74 y, where peak fat mass
was noted in men and women and was lower thereafter.
Our results contradict Baumgartner et al (1995) who
suggested that the accumulation of abdominal and visceral
fat that has been observed in both men and women with age
occurs primarily during middle age and there may be little
or no further increase during old age. Longitudinal studies
need to con®rm this observation. Visser et al (1998) found
high levels of disability in subjects with high fat mass
(> 32.0% and 43.7% in men and women, respectively).
Less than 2.8% of our subjects exceeded these levels of fat
mass. This study neither con®rms nor contradicts ®ndings
that high fat mass leads to increased disability. Waist
circumference strongly predicted death from cardiovascular
disease in older men (Allison et al, 1997; Heitmann et al,
2000). We are unable to determine whether the age-related
increase in trunk fat mass affects cardiovascular risk.
The greater fat mass observed in the elderly subjects in
spite of only slightly higher BMIs suggests that the proportion of mass at a given BMI is different in young and old.
These ®ndings give further evidence of the limitation of
using BMI as an indicator of fatness or leanness. Individual
body composition compartments, ie FFM and fat mass,
should, therefore, be measured to evaluate changes in body
composition with aging. This is especially important in
subjects in whom an increased fat mass might mask
decreases in FFM that might not be observed when assessment is limited to determining BMI only.
671
Limitations of study
The subjects in this study were not randomly selected.
However, the BMI in our study was similar to a randomly
sampled Swiss population (Euralim Study, a European
public health study of eating habits and cardiovascular
disease and cancer risk factors; Morabia et al, 1997).
The subjects in this study were volunteers in good
health, and may not be representative of the general
population, especially in the > 60 y groups. The absence
of mobility problems and the relative high prevalence of
regular physical activity appears to have aided in maintaining functional functioning and may have limited the loss of
FFM and ASMM.
The accuracy and precision of DXA is known to depend
in part on the thickness of the X-ray absorber. The extent to
which beam hardening or insuf®cient X-ray attenuation
may affect the accuracy of whole body and body segment
estimates of the lean tissue is not well established. DXAmeasured ASMM includes non-muscle fat-free components, such as skin, connective tissue and non-lipid portions
of adipose tissue, but their amounts are likely to be small
relative to ASMM (Gallagher et al, 1995).
This study did not measure total body water compartment and their in¯uence on FFM composition with age, but
this should be further explored.
Conclusion
This is the ®rst study to evaluate lean body parameters
(FFM, ASMM, BCM, TBK) and fat mass, derived from
two independent methods, in 433 healthy subjects between
18 and 94 y. The decline in FFM, ASMM, BCM and TBK
is accelerated in men and women after 60 y of age and
FFM, ASMM, BCM and TBK are signi®cantly lower than
in younger subjects. Fat mass continued to increase until
around 75 y.
Acknowledgements ÐWe thank the Foundation Nutrition 2000Plus for its
®nancial support. We are indebted to Giulio Conicella, Luc Terraneo and
Sophie Namy for technical assistance.
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