ORIGINAL ARTICLE
Behavioral and physiological regulation of body
fatness: a cross-sectional study in elderly men
V Rimbert
1, C Montaurier
1, M Bedu
2, Y Boirie
1and B Morio
11
Protein and Energy Metabolism Research Unit, Human Nutrition Research Centre of Auvergne, INRA, Auvergne University,
Clermont-Ferrand, France and
2Laboratory of Physiology and Biology of Sport, Human Nutrition Research Centre of
Auvergne, Auvergne University, Clermont-Ferrand, France
Objective: To identify the characteristics of physical activity that are the most correlated to total and truncal fatness and to physiological parameters involved in fat oxidation in elderly men.
Design: Cross-sectional study.
Subjects: A total of 25 healthy elderly men selected with a wide range of physical activity behavior (65.973.4 years). Measurements: Total and truncal fat masses (by dual-energy X-ray absorptiometry), time spent and energy expended (EEday) at
specific activity intensities (o40, 40–60, 460% VO2max) during 1 week in free living conditions (using heart rate recording and
individual calibrated equations), sport-exercising volume (Vsport, using Baecke questionnaire), maximal oxygen uptake (VO2max),
muscle fat oxidative capacity (OXFA, using muscle biopsy), lipid oxidation and respiratory exchange ratio during exercise at 50%
VO2max(using indirect calorimetry).
Results: Vsport was the main determinant of total and truncal fatness, VO2max and OXFA (r ¼ 0.69, Po0.0001; r ¼ 0.80,
Po0.0001; r ¼ 0.70, Po0.0001; r ¼ 0.66, Po0.001, respectively). Among physical activity parameters measured over a week, total EEdaywas the main determinant of total fat mass. Furthermore, EEdayat % VO2max460 was closely correlated to truncal fat
mass, VO2maxand OXFA(r ¼ 0.58, P40.01; r ¼ 0.55, Po0.01; r ¼ 0.49, Po0.05, respectively). Finally, VO2maxand OXFAwere
positively correlated to absolute fat oxidation and to the contribution of fat to energy production during moderate exercise. Conclusion: Sport-exercising volume is the main factor regulating total and truncal fat masses and physiological parameters involved in fat oxidation. With regard to the characteristics of physical activity, overall energy expended during the alert period plays a major role in the regulation of total body fatness. In addition, vigorous exercises may be beneficial for the regulation of abdominal fat depot partly through the stimulation of muscle fat oxidation during the effort.
International Journal of Obesity (2006) 30, 322–330. doi:10.1038/sj.ijo.0803113; published online 4 October 2005 Keywords: aging; substrate utilization; metabolic syndrome
Introduction
Fat is a major source of energy for muscle contraction during low- and moderate-intensity exercises. The pattern of substrate utilization (fat vs glucose) during physical activities depends on the interaction between exercise intensity and exercising-induced physiological adaptations such as mus-cular biochemical adjustments that increase the muscle fat
oxidative capacity.1,2Although controversial,3 high muscle
fat oxidative capacity has been suggested to enhance
fat oxidation during exercises at moderate intensity,4
with significant consequences on daily fat oxidation.4,5
Therefore, the optimization of muscle fat oxidative capacity by means of adequate physical activities may be beneficial for the regulation of fat balance, and ultimately of body fat mass.
Position papers6–8 have concluded, according to
popula-tion-based epidemiological studies, that weight gain and disease risk, particularly cardiovascular risk, were limited with increasing amounts of daily physical activity even of low intensity. Current public health recommendations for physical activity promote 30 min of moderate-intensity activity each day. However, more recently, this amount of physical activity was shown to be insufficient to prevent
unhealthy weight gain.9–11 It was therefore proposed that
more vigorous exercises would more appropriate. Received 15 December 2004; revised 9 July 2005; accepted 20 July 2005;
published online 4 October 2005
Correspondence: Dr B Morio, Protein and Energy Metabolism Research Unit, Human Nutrition Laboratory, Human Nutrition Research Centre of Auvergne, Auvergne University, BP 321, 58 Montalembert Street, 63009 Clermont-Ferrand cedex 1, France.
E-mail : morio@clermont.inra.fr
Performing household tasks and leisure activities is associated with increased energy expenditure (EE) and enhanced fat oxidation, both being involved in the regula-tion of fat balance. However, we can hypothesize that the volume of vigorous exercises may be more effective than activities of moderate intensity through their stimulating effect on physiological adaptations that improve fat
utiliza-tion during muscle contracutiliza-tion.2
Individuals aged 65 and over constitute the most rapidly growing segment of the population in industrialized coun-tries. By the year 2030, people over 65 years could comprise nearly 25% of the population in these countries. Aging is often associated with increased sedentary lifestyle. In all, 65% of the adults aged 75 years and older report no leisure physical activity, while only 12% engage into 30 min of
moderate physical activity 5 or more days per week.12If the
decline in daily EE is greater than the diminution in daily energy intake, a positive energy balance is created that is
responsible for increased central and total body fat depots.13
Presently, the characteristics of physical activity, that is, frequency, intensity and duration, required to prevent this situation are still unknown.
The present study aimed therefore at identifying the characteristics of physical activity that are the most corre-lated to total and central fatness in 25 healthy elderly men selected with a wide range of physical activity behavior. Furthermore, we determined the strength of the association between physiological parameters that determine fat
oxida-tion (i.e. muscle oxidative capacity and VO2max) and fat
balance and body fatness.
Subjects and methods
Subjects
The present study involved 25 healthy elderly men
(65.973.4 years), who were characterized by a large range
of physical activity from sedentary to athletic. All subjects had normal physical and medical examination. They were nonobese, weight stable, nonsmokers, not suffering from any diagnosed disease, and under no medication known to influence energy and lipid metabolism. The nature and potential risks of the study were fully explained and written
informed consent was obtained from each participant. The experimental protocol was approved by the ethical commit-tee of Clermont-Ferrand and performed according to the principles expressed in the Declaration of Helsinki and the French legislation (Huriet law).
General study design
The study design is illustrated in Table 1. The inclusion period included an activity questionnaire, a medical exam-ination and a maximal aerobic power test. The measurement period started with heart rate (HR) recording over 1 week in free-living conditions. Then, the subjects were placed on a controlled diet 3 days before and throughout the metabolic measurements in order to normalize their nutritional intakes. Body composition measurement, 36 h whole-body indirect calorimetry and muscle biopsy were performed on separate days.
Physical activity characterization
Activity questionnaire. A sport index was calculated using the
activity questionnaire from Baecke et al.14The calculation of
the sport index takes into account three coefficients: the intensity (type of exercise), the duration (hours per week) and the regularity (months per year) of the physical exercising. Three levels of intensity were considered and included light-intensity fitness exercises such as golf, archery, billiards, motorized sports; moderate-intensity fit-ness exercises such as walking, tennis, swimming, skiing and high-intensity fitness such as running, cycling, soccer, handball, hockey and gymnastics. Five levels of duration per week were considered: less than 1 h, 1–2, 2–3, 3–4 and more than 4 h per week. Finally, five levels of regularity over a year were considered: less than 1 month, 1–3, 4–6, 7–9 and more than 9 months per year. The product of the three coefficients was calculated for each sport. Then, all scores were added to calculate the sport index.
Maximal aerobic power test. The tests were all performed on the same cycloergometer (Ergomeca, Monark, Sweden) under cardiovascular supervision by a cardiologist, as
described previously.15 Maximal oxygen uptake (VO
2max)
Table 1 General study design
Inclusion period Measurement period
Controlled diet
Body composition Indirect calorimetry Muscle biopsy Medical examination Heart rate recording Controlled diet
Activity questionnaire In free living conditions VO2max
Duration 7 days 3 days 1 day 1.5 day 1 day
VO2max, maximal oxygen uptake.
was determined when the following criteria were reached: a respiratory quotient 41.1, a maximal HR close to the theoretical maximal HR (220age (year)), a plateau in
oxygen consumption and/or exhaustion. VO2max was
ex-pressed in ml min1kg fat-free mass (FFM)1(VO2max/FFM).
HR recording
HR was recorded minute-by-minute using telemetry (Polar protrainert Polar Electro Oy, Finland) during 1 week in free
living conditions as described previously.16Using these HR
recordings, the energy expended during the alert period
(from 0700 to 2300 h) (total EEday), the energy expended at
specific activity intensities (EEdayat VO2maxo40, 40–60 and
460%) and the time spent at specific activity intensities
(o40, 40–60 and 460% of VO2max) were calculated using
individual relationships set up between HR and EE and
between HR and %VO2max. These equations were established
using the combined measurements obtained during 36 h in whole-body indirect calorimetric chambers and during the maximal aerobic power test. Indeed, these combined data allowed to calibrate individual equations that took into
account HR, EE and %VO2max from sleeping and resting
conditions to maximal values. EEdaywere expressed per kg of
body weight.
Controlled diet
The controlled diet was balanced in lipids (35% of energy), carbohydrates (50%) and proteins (15%), and was calculated to meet the subjects’ energy needs on a personal basis, as
described previously.15
Body composition assessment
Body mass was measured to the nearest 0.1 kg on SECA 709 or 812 scales (SECA, Les Mureaux, France). Height was measured to the nearest 0.5 cm. A transverse scan of total body was performed using DEXA (Hologic QDR 4500 X-Ray bone densimeter, Hologic, Waltham, MA, USA) for determi-nation of total and regional (arms, legs and trunk) body
compositions, as described previously.15
Program and measurements in the calorimetric chambers After one night of adaptation, subjects spent 24 h in the calorimetric chambers while the diet and the activity program were controlled.
Activity program and food intakes in the calorimeters. The activity program in the calorimeters consisted of four periods
of 30-min walking at 50% VO2max. During the remaining
time, subjects had resting activities such as watching TV, reading and writing. The energy supply (ES) was calculated to meet each subject’s energy needs on a personal basis. For that purpose, expected daily EE was calculated from the duration
and the energy cost of the various activities in the
calorimeters (e.g., walking)15 and from each subject’s
predicted BMR.17
Indirect calorimetry measurements. Respiratory gas exchanges were measured continuously using two open-circuit
whole-body calorimetric chambers as described previously.15 Gas
analyzers were calibrated upon commencement, after 13 h (evening) and at the end of the 24-h measurement period using standard gas mixtures. Gas exchanges were computed from the minute-by-minute measurement of outlet air flow, differences in gas concentrations, atmospheric pressure, chamber air temperature and hygrometry, and taking into account the gas analyzers drifts and the variations of the
volumes of CO2and O2in the chambers. The validity of gas
exchange measurements was checked gravimetrically,
com-paring the amounts of gases (CO2, O2) analyzed and those
expected from the weights of gases (CO2, N2) injected into
the chambers during a 24-h period. The recovery was
98.571.0% for N2and 100.171.0% for CO2.
Urine was collected over 24 h, partitioned into two periods (alert period from 0700 to 1100 h, and sleep from 1100 to 0700 h) for the determination of urinary nitrogen excretion.
EE was calculated using Weir’s equation18from the
minute-by-minute measurement of gas exchanges corrected for the urinary nitrogen excretion. Daily energy balance was calculated from the difference between daily energy intake and daily EE, and expressed as percentage of daily EE.
The indirect calorimetry measures during walking periods (2 h, 4 times 30 min) were analysed. Respiratory exchange
ratio (RER) was calculated as the ratio of CO2 production
divided by O2consumption. Lipid oxidation was calculated
from gas exchanges and urinary nitrogen excretion over the
periods of interest using Ferrannini’s equations.16In
parti-cular, respiratory gaseous exchanges during walking were determined over the last 20 min of each session.
Determination of the relationships EE¼ f(HR) and %VO2max¼
f(HR). HR was continuously monitored in the calorimeters.
HR, EE and %VO2maxwere averaged over 30-min intervals.
As low levels of HR, EE and %VO2maxwere obtained in the
calorimeters, measures of HR, EE and %VO2max acquired
during the maximal aerobic power test were added to improve the quality of the model adjustment. Individual relationships between HR and EE and between HR and
%VO2max were then established using a third-degree
poly-nomial adjustment.16
Muscle biopsy and assay
Muscle biopsy. After an overnight fast, biopsies were obtained from the vastus lateralis muscle under a local anesthetic
(5 ml lidocaı¨ne 2%) with a percutaneous needle.19
Chemicals. [1-14C]palmitic acid was purchased from
Amer-sham International (Bucks, UK). ATP, NADþand cytochrome
c were supplied by Boeringer-Mannheim (Meylan, France). Antimycin A, acetyl-coenzyme A, fatty acid-free bovine
serum albumin,L-carnitine, palmitic acid, rotenone,
oxalo-acetate, L-malate and coenzyme A were purchased from
Sigma (St Louis, MO, USA). Other chemicals used were of the highest grade commercially available.
Muscle fat oxidative capacity. Fresh muscle (90 mg) was
homogenized in ice-cold buffer consisting of 0.25Msucrose,
2 mMEDTA and 10 mMTris HCl (pH 7.4) using a Polytron PT
1200C homogenizer (Bioblock Scientific, Illkirch, France) for
5 s at maximum power. [1-14C]palmitate oxidation by fresh
muscle homogenate was performed using the method
described previously.4 Briefly, the total palmitate oxidation
rate was calculated from the amount of 14CO2 and 14
C-labeled acid-soluble metabolites produced over 30 min at 371C. Total palmitate oxidation rate was expressed in nanomoles palmitate per gram of wet tissue per minute. All assays were performed in triplicate.
Statistical analysis
Results are reported as mean7s.d. Correlation coefficients
are Pearson product–moment correlations. Stepwise linear regressions were used to identify the main determinants of
body fatness, VO2max/FFM and muscle fat oxidative capacity
among physical activity parameters. Results were considered statistically significant at the 5% level. Statistics were performed using Statview 5.0 (SAS Institute Inc., Cary, NC, USA).
Results
Subjects’ characteristics and physical activity parameters are summarized in Table 2. As shown in Table 3, sport-exercising volume, evaluated with the sport index, was positively
correlated to total EEday (Po0.05), EEday at %VO2maxo40
(Po0.05) and EEdayat %VO2max460 (Po 0.01). Total EEday
was positively correlated to EEday at %VO2maxo40
(Po0.0001) and to a lesser extent to EEdayat %VO2max460
(Po0.01). Time spent at %VO2maxo40 was negatively
correlated to total EEday(Po0.05), EEdayat %VO2max¼ 40–
60 (Po0.0001) and EEday at %VO2max460 (Po0.05), while
times spent at %VO2max¼ 40–60 and %VO2max460 were
Table 2 Subjects characteristics and physical activity parameters Mean7s.d. (n ¼ 25) Range min–max Age (years) 65.973.4 60.0–75.0 Height (cm) 17376 161–187 Body weight (kg) 76.5710.1 60.6–97.5 BMI (kg m2) 25.272.9 20.0–29.8 Fat mass (kg) 16.274.8 7.8–24.9 Fat mass (%) 20.974.5 12.8–28.5
Truncal fat mass (kg) 8.073.2 3.1–13.7
Truncal fat/body fat mass (%) 49.079.0 16.3–58.5
Fat free mass (kg) 60.376.8 49.4–73.0
Lipid oxidation (g h1kg FFM1) during walking at 50% VO2max
0.15170.056 0.065–0.281 RER during walking at 50% VO2max 0.91970.020 0.879–0.962 VO2max/FFM (ml min1kg FFM1) 40.977.0 29.1–58.1 OXFA(nmol palmitate min1g
tissue1)
50.7719.7 21.5–97.7 Time spent at %VO2maxo40
(h day1)
14.870.6 13.5–15.7 Time spent at %VO2max¼ 40–60
(min day1)
52.4730.5 7.1–128.4 Time spent at %VO2max460
(min day1) 18.9719.3
0–68.0
Sport index 4.773.6 0–13.8
Total EEday(kcal kg BW1) 32.778.2 23.5–53.7
EEdayat %VO2maxo40 26.575.8 19.7–43.0
EEdayat %VO2max¼ 40–60 3.872.1 0.4–8.8
EEdayat %VO2max460 2.472.7 0.0–9.0
BMI, body mass index; RER, respiratory exchange ratio; VO2max/FFM, maximal oxygen uptake expressed per kg fat free mass; OXFA, muscle fat oxidative capacity; EEday, daily energy expenditure during alert period expressed in kcal kg body weight1.
Table 3 Pearson correlation coefficents between characteristics of physical activity behavior
Time spent at Sport index Total EEday
%VO2maxo40 (h day1) %VO2max¼ 40–60 (min day1) %VO2max460 (min day1) EEday
Total 0.462 1 0.488 NS 0.474
Po0.05 Po0.05 Po0.05
%VO2maxo40 0.414 0.951 NS NS NS
Po0.05 Po0.0001
%VO2max¼ 40–60 NS 0.667 0.812 0.820 NS
Po0.001 Po0.0001 Po0.0001
%VO2max460 0.525 0.558 0.434 NS 0.948
Po0.01 Po0.01 Po0.05 Po0.0001
EEday, daily energy expenditure during the alert period, expressed per kg body weight, time spent at specific activity intensity during the alert period.
only positively correlated to EEday at %VO2max¼ 40–60
(Po0.0001) and EEdayat %VO2max460 (Po0.0001),
respec-tively. Finally, sport index was positively correlated to the
time spent at %VO2max460 (r ¼ 0.45, Po0.05), but not to the
time spent at %VO2maxo40 and %VO2max¼ 40–60 (P ¼ NS).
Influence of physical activity behavior on body fatness (Tables 4 and 5)
Total (Po0.0001) and truncal (Po0.0001) fat masses were the most negatively correlated to sport index. When considering characteristics of physical activity determined over a week in free living conditions, total and truncal body
fatness were negatively correlated to EEdaytotal (Po0.001),
at %VO2maxo40 (Po0.01) and at %VO2max460 (Po0.01),
but not at %VO2max¼ 40–60 (P ¼ NS) (Table 4). By contrast,
total and truncal body fat masses were not significantly correlated to the time spent at specific intensities (P ¼ NS)
(Table 4). Stepwise regression showed that total EEdaywas the
main determinant of total body fat mass and %fat mass,
whereas EEdayat %VO2max460 was the main factor
explain-ing differences in truncal fat mass (Table 5).
Influence of physical activity behavior on VO2maxand muscle
fat oxidative capacity (Table 4)
VO2max/FFM was positively correlated to sport index
(Po0.0001), EEday total (Po0.05) and at %VO2max460
(Po0.01), but not to the energy expended during low
and moderate-intensity activities (P ¼ NS). Furthermore,
VO2max/FFM was positively correlated to the time spent at
%VO2max460 (Po0.05). Among the physical activity
para-meters determined over 1 week in free living conditions,
stepwise regression identified EEdayat %VO2max460 as the
main determinant of VO2max/FFM (R2¼ 0.31, Po0.01).
Similarly, muscle fat oxidative capacity was positively
correlated to sport index (Po0.001), EEdaytotal (Po0.05), at
%VO2maxo40 (Po0.05) and at %VO2max460 (Po0.05), but
not at %VO2max¼ 40–60 (P ¼ NS) (Table 4). Among the
physical activity parameters determined over 1 week in free living conditions, stepwise regression identified
EEday and the time spent at %VO2max460 as the main
Table 4 Pearson correlation coefficents between body fatness, VO2max/FFM, muscle fat oxidative capacity and characteristics of daily physical behavior
FM (kg) FM (%) Truncal FM (kg) VO2max/FFM OXFA
Sport index 0.688 0.583 0.805 0.704 0.657
Po0.0001 Po0.01 Po0.0001 Po0.0001 Po0.001
EEday
Total 0.639 0.642 0.541 0.431 0.451
Po0.001 Po0.001 Po0.01 Po0.05 Po0.05
%VO2maxo40 0.562 0.605 0.445 NS 0.398
Po0.01 Po0.01 Po0.05 Po0.05
%VO2max¼ 40–60 NS NS NS NS NS
%VO2max460 0.510 0.456 0.584 0.554 0.486
Po0.01 Po0.05 Po0.01 Po0.01 Po0.05
Time spent at
%VO2maxo40 NS NS NS NS NS
%VO2max¼ 40–60 NS NS NS NS NS
%VO2max460 NS NS NS 0.438 NS
Po0.05
EEday, daily energy expenditure during alert period expressed per kg body weight; FM, fat mass; VO2max/FFM, maximal oxygen uptake expressed per kg of fat free mass (ml min1kg1); OXFA, muscle fat oxidative capacity (nmol palmitate min1g wet tissue1).
Table 5 Main predictors of body fatness, among physical activity parameters measured during 1 week, derived from stepwise linear regressions in 25 elderly males
FM (kg) FM (%) Truncal FM (kg) Variance (%) explained by:
Total EEday 40.9 42.7 NS
Po0.001 Po0.001
EEdayat %VO2maxo40 NS 8.1 NS
Po0.01
EEdayat %VO2max¼ 40–60 NS NS NS
EEdayat %VO2max460 NS NS 34.1
Po0.01
Time spent at %VO2maxo40 NS NS NS
Time spent at %VO2max¼ 40–60
NS NS NS
Time spent at %VO2max460 NS NS NS
Total variance (R2) explained by the model:
0.409 0.508 0.341
Po0.001 Po0.001 Po0.01
FM, fat mass; EEday, daily energy expenditure during alert period expressed per kg body weight; R2, correlation coefficient derived from stepwise linear regression between fat mass measures and their predictors. NS: not included in the stepwise regression.
determinants of muscle fat oxidative capacity (R2¼ 0.38,
Po0.01). Finally, as expected, muscle fat oxidative capacity
was positively correlated to VO2max/FFM (r ¼ 0.72,
Po0.0001; Figure 1a).
Influence of VO2max/FFM and muscle fat oxidative capacity on
body fatness
To evaluate the implication of physiological adaptations in the regulation of body fatness, we tested the association
between body fat mass and VO2max/FFM and muscle fat
oxidative capacity. Total fat mass and central fat mass were
negatively correlated to VO2max/FFM (r ¼ 0.60, Po0.001
and r ¼ 0.68, Po0.0001, respectively) and muscle fat
oxidative capacity (r ¼ 0.59, Po0,01 and r ¼ 0.56,
Po0.01, respectively).
Lipid oxidation and RER during exercise at 50% VO2max
As presented in Figure 1b and c, lipid oxidation (g h1kg
FFM1) and RER during exercise at 50% VO2max were
significantly correlated to VO2max/FFM after adjustment for
differences in energy balance (r ¼ 0.73, Po0.0001 and
r¼ 0.59, Po0.01, respectively).
Discussion
The aim of the present study was to identify in elderly men the characteristics of physical activity that better correlate to body fatness and physiological parameters known to
poten-tially improve fat oxidation (i.e. VO2max and muscle fat
oxidative capacity). The volume of sport exercising, a
self-reported index that quantified the sum of
intensi-ty duration frequency of all sport exercises practiced by a subject over a year, was the most correlated to total and
central body fatness, VO2max and muscle fat oxidative
capacity. When considering the characteristics of physical activity determined over a week using HR recordings, the
energy expended during vigorous activities (460% VO2max)
was the most correlated to truncal fatness, VO2max and
muscle fat oxidative capacity, while the overall energy expended during the alert period was the most correlated to total body fatness. Interestingly, energy expended during
moderate activities (40–60% VO2max) was not associated
with differences in body fatness, VO2max and muscle fat
oxidative capacity. These results confirm that regular sport exercising is a major factor regulating the whole body fat balance in elderly men. Daily EE, which is positively correlated to the volume of sport exercising, is an important component involved in the regulation of fat balance. Furthermore, the volume of vigorous activities may play an important role in the regulation of fat balance (especially in the abdominal area), possibly through the stimulation of physiological parameters that promote fat oxidation.
We found that the volume of sport exercising was the most negatively correlated to total and truncal fat masses. The beneficial effect of sport exercising on body fatness may act through (1) the enhancement of EE and (2) the enhance-ment of fat utilization. First, the volume of sport exercising was positively associated with the overall energy expended during the alert period. More specifically, it was positively 120 100 80 60 40 20 0 25 30 35 40 50 55 60 0.10 0.06 0.02 -0.02 -0.06 25 35 45 55 0.03 0.01 0.02 0 -0.01 -0.02 -0.03 35 25 45 55 45 Muscle f at o xidativ e capacity nmol palmitate .min -1 .g w et tisue -1 RER residues dur ing e x ercise at 50% V O2 max (adjusted f or energy balance) VO2max ml.min-1.kg FFM-1 VO2max ml.min-1.kg FFM-1 VO2max ml.min-1.kg FFM-1 Lipid o xidation residues dur ing e x ercise at 50% V O2 max (adjusted f or energy balance)
c
b
a
R2=0.52 P<0.0001 R2=0.52 P<0.0001 R2=0.35 P<0.01Figure 1 Correlations between maximal oxygen uptake (VO2max/FFM) and (a) muscle fat oxidative capacity, (b) lipid oxidation during exercise adjusted for energy balance, (c) RER during exercise adjusted for energy balance in 25 healthy elderly men.
correlated to the energy expended during low and vigorous activities, but not to the energy expended during moderate activities. Therefore, the beneficial effect of sport exercising on body fatness may act through increased EE during vigorous activities and also during nonexercising periods, which may be associated with fidgeting, maintenance of
posture and other physical activities of daily life.20Secondly,
sport exercising was strongly correlated to VO2max and
muscle fat oxidative capacity, and the latter were positively correlated to fat oxidation and to the contribution of fat to ES during an exercise at moderate intensity. These results suggest that high volume of sport exercising may improve the regulation of fat balance through the promotion of fat utilization during exercise. However, the effect of training on the amount and proportion of fat oxidized during exercise of the same relative intensity is controversial. While long-itudinal studies have supported the notion that training has
no significant effect on fat oxidation during exercise,3,21,22
cross-sectional studies have demonstrated a higher fat oxidation rate in trained subjects than in untrained
individuals.23,24In addition, the increased proportion of fat
oxidized during exercise at the same relative intensity is in contrast with the data presented by Achten and
Jeukendr-up.2The authors showed that, despite a 17% higher absolute
fat oxidation rate when cycling at 62% VO2max in
well-trained athletes compared to moderately well-trained individuals, the relative contribution of fat to EE was 30% in both groups. Therefore, further studies are needed to clarify this question. Finally, it is tempting to hypothesize that, because the volume of sport exercising was more closely correlated to body fatness than the characteristics of physical activities determined over a week, the beneficial effects of regular sport exercising may also act through others parameters, such as the control of food intake and of mood, and improvement of
circulating hormones.25,26
Our results suggest that practicing daily activities at an
intensity higher than 60% VO2max may be specifically
beneficial for the regulation of truncal fat depot. This is in agreement with some cross-sectional studies that showed that subjects practicing vigorous activities on a regular basis had lower abdominal fat than those not performing these
activities.27,28 In addition, an intervention study reported
that vigorous aerobic training induced a reduction in
abdominal fat in middle-aged and older men.29 However,
Cox et al.30did not observe changes in abdominal fat depot
after a 4-month vigorous exercise program consisting of three half-hour sessions per week. Thus, it remains to be determined whether a threshold of vigorous activities volume has to be reached to affect truncal fat mass. The latter is composed of abdominal subcutaneous and visceral fat depots. Lipolysis in abdominal subcutaneous adipose
tissue was shown to increase during31and after32an exercise
of high intensity. In addition, visceral adipocytes have a higher responsiveness to the lipolytic effect of
cate-cholamines than subcutaneous adipocytes.33,34 Therefore,
vigorous exercise-induced catecholamine secretion might
promote the mobilization of fatty acids from visceral and abdominal subcutaneous adipocytes to provide energy for muscle contraction.
A moderate increase in EE, achieved through walking, household tasks and other light-intensity activities, has been recently proposed to limit the risk of metabolic diseases
associated with increased body fatness.35,36In addition, the
current recommendation for sedentary adults to prevent the transition to overweight or obesity is the practice of
moderate intensity activity for 45–60 min per day.10 The
present results are partly in agreement with these recom-mendations, as we observed that the volume of sport exercising was the main determinant of body fatness. However, our results also suggest that practicing activities of vigorous intensity may be important to better regulate abdominal fat mass, which is particularly related to the
metabolic syndrome.37,38 Furthermore, the present study
showed that regular sport exercising is associated with an increase in the energy expended during low-intensity activities, in addition to the periods of vigorous activities. This suggests that engagement in vigorous exercises may be more beneficial for the regulation of fat balance than practicing moderate-intensity activities, possibly through an increased tonicity which helps to substantially increase the
overall EE. Using personal data39,40 and the
Compen-dium of Physical Activities Tracking Guide (University of South Carolina, USA: http://prevention.sph.sc.edu/tools/
compendium.htm), we found that 60% VO2max may be
almost reached or exceeded during home repair, aerobic exercises, walking at sustained speed (i.e. around 5–
6 km h1), gardening with vigorous activity, cycling and
light jogging in sedentary individuals. By contrast, sport exercises (e.g. moderate to vigorous cycling and running) have to be performed to reach this threshold of intensity in moderately trained men (Figure 2).
In conclusion, our results showed that, in healthy elderly men, total and truncal fat masses and physiological
para-meters involved in fat oxidation (i.e. VO2max and muscle
fat oxidative capacity) were closely associated with the volume of sport exercising that integrates the intensi-ty duration frequency of all sport exercises practiced by a subject over a year. When only considering physical activity characteristics determined over a week in free living conditions, the overall energy expended during the alert period was the main factor explaining differences in body fat mass, demonstrating that increasing EE, whatever the activity, plays a major role in the regulation of total body fatness. However, other physiological adaptations associated with regular exercising (such as energy intake) might also contribute to the regulation of body fatness, but this aspect deserves further investigations. Furthermore, the energy
expended during vigorous activities (460% VO2max) was
the main determinant of truncal fat mass, VO2max and
muscle fat oxidative capacity. The beneficial effect of vigorous exercises on abdominal fat depot may possibly act through a higher abdominal fat mobilization and a higher 328
muscle fat oxidation during the effort. Finally, the present study stresses the importance of regular sport exercising, particularly vigorous activities, throughout life span for the prevention of age-associated unhealthy weight gain.
Acknowledgements
This work was supported by research founds from the Institut National de la Recherche Agronomique (INRA). We
thank Dr Isabelle Petit, Jean-Franc-ois Hocquette, Liliane
Morin, Christophe Giraudet, Paulette Rousset, Marion Brandolini and Guy Manlhiot for their skillful technical assistance, Michel Vermorel and Dr He´le`ne Derumeaux for their valuable comments on the manuscript and the volunteers for their participation.
References
1 Brooks GA, Mercier J. Balance of carbohydrate and lipid utilization during exercise: the "crossover" concept. J Appl Physiol 1994; 76: 2253–2261.
2 Achten J, Jeukendrup AE. Optimizing fat oxidation through exercise and diet. Nutrition 2004; 20: 716–727.
3 Friedlander AL, Casazza GA, Horning MA, Usaj A, Brooks GA. Endurance training increases fatty acid turnover, but not fat oxidation, in young men. J Appl Physiol 1999; 86: 2097–2105. 4 Morio B, Hocquette JF, Montaurier C, Boirie Y,
Bouteloup-Demange C, McCormack C et al. Muscle fatty acid oxidative capacity is a determinant of whole body fat oxidation in elderly people. Am J Physiol Endocrinol Metab 2001; 280: E143–E149. 5 Zurlo F, Nemeth PM, Choksi RM, Sesodia S, Ravussin E.
Whole-body energy metabolism and skeletal muscle biochemical characteristics. Metabolism 1994; 43: 481–486.
6 Pate RR, Pratt M, Blair SN, Haskell WL, Macera CA, Bouchard C et al. Physical activity and public health. A recommendation from the Centers for Disease Control and Prevention and the American College of Sports Medicine. JAMA 1995; 273: 402–407.
7 NIH Consensus Development Panel on Physical Activity and Cardiovascular Health. Physical activity and cardiovascular health. JAMA 1996; 276: 241–246.
8 Centers for Disease Control and Prevention. Surgeon General’s report on physical activity and health. JAMA 1996; 276: 522. 9 Erlichman J, Kerbey AL, James WP. Physical activity and its
impact on health outcomes. Paper 2: Prevention of unhealthy weight gain and obesity by physical activity: an analysis of the evidence. Obes Rev 2002; 3: 273–287.
10 Saris WH, Blair SN, van Baak MA, Eaton SB, Davies PS, Di Pietro L et al. How much physical activity is enough to prevent unhealthy weight gain? Outcome of the IASO 1st Stock Conference and consensus statement. Obes Rev 2003; 4: 101–114.
Average intensity for :
sedentary moderately trained
100% 90% 80% 70% 60% 50% 40% 30% 20% 10% 0% sleeping Sitting quietly Reading-w ritin g Watching TV Sitting wit h ar m ac tivity
Standing with light ac tivity
Standing with mod erate activit
y Child care
House-k eeping act
ivities light eff ort Vaccum c leane r House-k eeping activit ies moder ate eff ort House-k eeping ac
tivities vigorous eff ort Hom e repairYo ga Aerobic lo w im pact Stretching Aerobic , moder
ate impactShopp ing Walking at nor mal speed Walking at sustained s peed Gardening w ith light activity
Gardening w ith moder ate activity Gardening w ith vigorous activit y Cycling leisure Cycling light eff
ort jogging gener al Cycling m oder ate e ffort Runn ing sustain ed speed Cycling vigoro us eff ort
Figure 2 Mean relative intensity of usual daily physical activities determined in sedentary (&) and moderately endurance-trained (’) elderly men using personal data39,40and the Compendium of Physical Activities Tracking Guide (University of South Carolina, USA).
11 Blair SN, LaMonte MJ, Nichaman MZ. The evolution of physical activity recommendations: how much is enough? Am J Clin Nutr 2004; 79: 913S–920S.
12 Conn VS, Minor MA, Burks KJ, Rantz MJ, Pomeroy SH. Integrative review of physical activity intervention research with aging adults. J Am Geriatr Soc 2003; 51: 1159–1168.
13 Starling RD. Energy expenditure and aging: effects of physical activity. Int J Sport Nutr Exerc Metab 2001; 11 (Suppl): S208–S217.
14 Baecke JA, Burema J, Frijters JE. A short questionnaire for the measurement of habitual physical activity in epidemiological studies. Am J Clin Nutr 1982; 36: 936–942.
15 Morio B, Montaurier C, Ritz P, Fellmann N, Coudert J, Beaufrere B et al. Time-course effects of endurance training on fat oxidation in sedentary elderly people. Int J Obes Relat Metab Disord 1999; 23: 706–714.
16 Lazzer S, Boirie Y, Bitar A, Montaurier C, Vernet J, Meyer M et al. Assessment of energy expenditure associated with physical activities in free-living obese and nonobese adolescents. Am J Clin Nutr 2003; 78: 471–479.
17 Black AE, Coward WA, Cole TJ, Prentice AM. Human energy expenditure in affluent societies: an analysis of 574 doubly-labelled water measurements. Eur J Clin Nutr 1996; 50: 72–92.
18 Weir JB. New methods for calculating metabolic rate with special reference to protein metabolism. 1949. Nutrition 1990; 6: 213–221.
19 Guillet C, Prod’homme M, Balage M, Gachon P, Giraudet C, Morin L et al. Impaired anabolic response of muscle protein synthesis is associated with S6K1 dysregulation in elderly humans. FASEB J 2004; 18: 1586–1587.
20 Levine JA, Eberhardt NL, Jensen MD. Role of nonexercise activity thermogenesis in resistance to fat gain in humans. Science 1999; 283: 212–214.
21 Bergman BC, Butterfield GE, Wolfel EE, Casazza GA, Lopaschuk GD, Brooks GA. Evaluation of exercise and training on muscle lipid metabolism. Am J Physiol 1999; 276: E106–E117.
22 Carter SL, Rennie C, Tarnopolsky MA. Substrate utilization during endurance exercise in men and women after endurance training. Am J Physiol Endocrinol Metab 2001; 280: E898–E907.
23 Bergman BC, Brooks GA. Respiratory gas-exchange ratios during graded exercise in fed and fasted trained and untrained men. J Appl Physiol 1999; 86: 479–487.
24 Coggan AR, Raguso CA, Gastaldelli A, Sidossis LS, Yeckel CW. Fat metabolism during high-intensity exercise in endurance-trained and untrained men. Metabolism 2000; 49: 122–128.
25 Nemet D, Connolly PH, Pontello-Pescatello AM, Rose-Gottron C, Larson JK, Galassetti P et al. Negative energy balance plays a major role in the IGF-I response to exercise training. J Appl Physiol 2004; 96: 276–282 (Epub 2003 August 29).
26 Loucks AB. Energy balance and body composition in sports and exercise. J Sports Sci 2004; 22: 1–14.
27 Tremblay A, Despres JP, Leblanc C, Craig CL, Ferris B, Stephens T et al. Effect of intensity of physical activity on body fatness and fat distribution. Am J Clin Nutr 1990; 51: 153–157.
28 Visser M, Launer LJ, Deurenberg P, Deeg DJ. Total and sports activity in older men and women: relation with body fat distribution. Am J Epidemiol 1997; 145: 752–761.
29 Pratley RE, Hagberg JM, Dengel DR, Rogus EM, Muller DC, Goldberg AP. Aerobic exercise training-induced reductions in abdominal fat and glucose-stimulated insulin responses in middle-aged and older men. J Am Geriatr Soc 2000; 48: 1055–1061.
30 Cox KL, Burke V, Morton AR, Beilin LJ, Puddey IB. The independent and combined effects of 16 weeks of vigorous exercise and energy restriction on body mass and composition in free-living overweight men – a randomized controlled trial. Metabolism 2003; 52: 107–115.
31 de Glisezinski I, Moro C, Pillard F, Marion-Latard F, Harant I, Meste M et al. Aerobic training improves exercise-induced lipolysis in SCAT and lipid utilization in overweight men. Am J Physiol Endocrinol Metab 2003; 285: E984–E990.
32 Mulla NA, Simonsen L, Bulow J. Post-exercise adipose tissue and skeletal muscle lipid metabolism in humans: the effects of exercise intensity. J Physiol 2000; 524 (Part 3): 919–928. 33 Hellmer J, Marcus C, Sonnenfeld T, Arner P. Mechanisms for
differences in lipolysis between human subcutaneous and omental fat cells. J Clin Endocrinol Metab 1992; 75: 15–20. 34 Vikman HL, Savola JM, Raasmaja A, Ohisalo JJ. Alpha
2A-adrenergic regulation of cyclic AMP accumulation and lipolysis in human omental and subcutaneous adipocytes. Int J Obes Relat Metab Disord 1996; 20: 185–189.
35 Knowler WC, Barrett-Connor E, Fowler SE, Hamman RF, Lachin JM, Walker EA et al. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 2002; 346: 393–403.
36 Franks PW, Ekelund U, Brage S, Wong MY, Wareham NJ. Does the association of habitual physical activity with the metabolic syndrome differ by level of cardiorespiratory fitness? Diabetes Care 2004; 27: 1187–1193.
37 Chan JM, Rimm EB, Colditz GA, Stampfer MJ, Willett WC. Obesity, fat distribution, and weight gain as risk factors for clinical diabetes in men. Diabetes Care 1994; 17: 961–969. 38 Folsom AR, Kushi LH, Anderson KE, Mink PJ, Olson JE, Hong CP
et al. Associations of general and abdominal obesity with multiple health outcomes in older women: the Iowa Women’s Health Study. Arch Intern Med 2000; 160: 2117–2128.
39 Morio B, Ritz P, Verdier E, Montaurier C, Beaufrere B, Vermorel M. Critical evaluation of the factorial and heart-rate recording methods for the determination of energy expenditure of free-living elderly people. Br J Nutr 1997; 78: 709–722.
40 Rimbert V, Boirie Y, Bedu M, Hocquette J, Ritz P, Morio B. Muscle fat oxidative capacity is not impaired by age but by sedentarity. Association with insulin sensitivity. FASEB J 2004; 18: 737–739.
