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Francesca Amati, John J. Dubé, Chris Shay and Bret H.

Goodpaster
J Appl Physiol 105:825-831, 2008. First published Jul 10, 2008; doi:10.1152/japplphysiol.90384.2008

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J Appl Physiol 105: 825–831, 2008.
First published July 10, 2008; doi:10.1152/japplphysiol.90384.2008.

Separate and combined effects of exercise training and weight loss on


exercise efficiency and substrate oxidation

Francesca Amati,1 John J. Dubé,2 Chris Shay,3 and Bret H. Goodpaster1,2


1
Department of Health and Physical Activity, School of Education, University of Pittsburgh, 2Division of Endocrinology
and Metabolism, Department of Medicine, University of Pittsburgh, and 3Department of Epidemiology, University
of Pittsburgh, Pittsburgh, Pennsylvania
Submitted 10 March 2008; accepted in final form 8 July 2008

Amati F, Dubé JJ, Shay C, Goodpaster BH. Separate and combined Skeletal muscle work efficiency may be expressed as gross
effects of exercise training and weight loss on exercise efficiency and efficiency (GE), net efficiency, or delta efficiency. The basic
substrate oxidation. J Appl Physiol 105: 825–831, 2008. First published definition of GE during steady-state exercise is the ratio of
July 10, 2008; doi:10.1152/japplphysiol.90384.2008.—Perturbations work accomplished to the total energy expended during that
in body weight have been shown to affect energy expenditure and specific activity and is expressed as a percentage (13). Net
efficiency during physical activity. The separate effects of weight loss efficiency and delta efficiency use the change in work per-
and exercise training on exercise efficiency or the proportion of
formed and the change in energy expanded either from baseline

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energy derived from fat oxidation during physical activity, however,
are not known. The purpose of this study was to determine the
(13) or computed from the slope of a linear relationship
separate and combined effects of exercise training and weight loss on between energy expended and work accomplished (8). Another
metabolic efficiency, economy (EC), and fat oxidation during steady- common concept related to efficiency is the term of economy
state moderate submaximal exercise. Sixty-four sedentary older (67 ⫾ (EC), which is a measure of oxygen consumption (V̇O2) per
0.5 yr) overweight to obese (30.7 ⫾ 0.4 kg/m2) volunteers completed unit of work (26).
4 mo of either diet-induced weight loss (WL; n ⫽ 11), exercise The concept of exercise efficiency may be important to
training (EX; n ⫽ 36), or the combination of both interventions consider from two very different perspectives. A higher or
(WLEX; n ⫽ 17). Energy expenditure, gross efficiency (GE), EC, and improved efficiency may be beneficial to sports performance in
proportion of energy expended from fat (EF) were determined during athletes. Coyle et al. (8) have shown that competitive cyclists
a 1-h submaximal (50% of peak aerobic capacity) cycle ergometry who had a higher proportion of type 1 muscle fibers with a
exercise before the intervention and at the same absolute work rate higher oxidative capacity were more efficient during cycling.
after the intervention. We found that EX increased GE by 4.7 ⫾ 2.2%. On the other hand, and perhaps counterintuitively from a sports
EC was similarly increased by 4.2 ⫾ 2.1% by EX. The addition of performance perspective, requiring less energy for activity, i.e.,
concomitant WL to EX (WLEX) resulted in greater increases in GE greater efficiency, may be a disadvantage for obesity, weight
(9.0 ⫾ 3.3%) compared with WL alone but not compared with EX
loss, or maintenance of weight loss. Obese subjects have a
alone. These effects remained after adjusting for changes in lean body
lower efficiency than normal-weight subjects for cycling (22)
mass. The proportion of energy derived from fat during the bout of
moderate exercise increased with EX and WLEX but not with WL. as well as for walking and stepping (7). During and after
From these findings, we conclude that exercise training, either alone weight loss, skeletal muscle work efficiency is increased (34);
or in combination with weight loss, increases both exercise efficiency this is even most evident at lower levels of physical activity
and the utilization of fat during moderate physical activity in previ- (29, 34). However, these studies did not examine the separate
ously sedentary, obese older adults. Weight loss alone, however, effects of increased physical activity and weight loss on exer-
significantly improves neither efficiency nor utilization of fat during cise efficiency. Therefore, the purpose of this study was to
exercise. determine the separate and combined effects of weight loss and
exercise training on exercise efficiency and economy in older
gross efficiency; exercise economy; aging
overweight and obese subjects. Moreover, another objective
was to determine the distinct and combined effects of weight
OBESITY AND AGING HAVE BOTH been associated with alterations loss and exercise on substrate, i.e., fat and carbohydrate utili-
in resting energy metabolism (10, 33). A number of studies zation during the same bout of moderate exercise. We hypoth-
have also examined the effects of diet-induced weight loss (23, esized that chronic exercise would have more of an impact on
32), exercise (15, 35), and the combination of diet and exercise exercise efficiency and fat oxidation compared with diet-
(27, 37) on energy expenditure and substrate metabolism induced weight loss.
during resting postabsorptive, postprandial, or insulin-stimu- METHODS
lated conditions. Far fewer studies have been conducted to
examine energy metabolism during physical activity in obesity Study Design and Subjects
(16, 19) or aging (5). In particular, the effects of weight loss or A total of 64 older (67 ⫾ 0.5 yr old) overweight or obese (30.7 ⫾
exercise training on energy metabolism during physical activ- 0.4 kg/m2) volunteers (38 women and 26 men) were included in this
ity have not been fully elucidated. study. Fifty-two of them participated in a 3 arms randomized clinical

Address for reprint requests and other correspondence: B. H. Goodpaster, The costs of publication of this article were defrayed in part by the payment
Univ. of Pittsburgh, 3459 Fifth Ave., MUH N807, Pittsburgh, PA 15213 of page charges. The article must therefore be hereby marked “advertisement”
(e-mail: bgood@pitt.edu). in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

http://www. jap.org 8750-7587/08 $8.00 Copyright © 2008 the American Physiological Society 825
826 EXERCISE TRAINING, WEIGHT LOSS, AND MUSCULAR EFFICIENCY

trial consisting in a 16-wk intervention of either diet-induced weight type I and type II muscle fibers were determine by the use of
loss (WL) or exercise training (EX) or the combination of both histochemical analysis as previously described (31).
interventions (WLEX). Twelve subjects were part of our pilot study A steady-state submaximal exercise test was performed 1 wk apart
and received without randomization the EX intervention. of the overnight visit. At baseline, subjects exercised on the braked
None of the volunteers were engaged in regular physical exercise cycle ergometer (Ergoline 800S, Sensormedics) at 50% of their
(⬎1 time/wk) and all were weight stable (⫾3 kg) for at least 6 mo predetermined peak aerobic capacity. After the intervention, the
before the study. Subjects were excluded if they had a history of type participants repeated the test at the same absolute work rate compared
2 diabetes, coronary heart disease, peripheral vascular disease, or with preintervention. Indirect calorimetry, used to measure V̇O2 and
uncontrolled hypertension or if they were taking chronic medications carbon dioxide production (V̇CO2), was performed at 15, 30, 45, and
known to affect glucose homeostasis. We also excluded subjects who 60 min of exercise. Cadence was maintained constant throughout the
had among the screening testing an anemia (hematocrit ⬍34%), 1-h exercise bout and was similar in the pre- and postintervention
clinical hypothyroidism (thyroid-stimulating hormone ⬎8␮IU/ml), or measurements. Only data from the last three time points (minutes
elevated liver enzymes (25% above the reference range). The protocol 28 –30, 43– 45, and 58 – 60) were used to ascertain steady-state levels.
was approved by the University of Pittsburgh Institutional Review We did not use the first 15 min of data due to the fact that during the
Board. All volunteers gave written informed consent. preintervention, workload adjustments were made during that time
window to match exactly 50% of the V̇O2peak. Subjects were in-
Intervention Groups structed to avoid strenuous physical activity for 2 days before and to
eat at least 200 g of carbohydrates for 3 days before the submaximal
WL. To achieve the goal of 10% weight loss, subjects were
exercise test to ensure adequate glycogen stores for the exercise bout.
prescribed a caloric deficit of 500 –1,000 kcal/day based on recent
In addition, they were asked to record food intake in a diary for the 3
food records combined with a low-fat diet (⬍30% of calories from
days before this test so that they could replicate their diet during the
fat). Subjects met weekly with a registered dietician for individual

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3 days preceding the postintervention test. To assess the variation in
counseling, review of food records, and weight monitoring.
the measurement tool and a possible learning effect, a subset of
EX. The exercise training protocol consisted of a 16-wk moderate-
individuals (n ⫽ 14) performed two tests before and two tests after the
intensity supervised aerobic exercise regimen. Subjects were asked to
intervention. For each of these time points, V̇O2 at the same work was
engage in three to five sessions per week with at least three sessions
not lower in the second test compared with the first test, indicating no
supervised in our facility. The intensity and duration of the exercise
learning effect.
sessions was progressively adapted to reach 45 min and 75% of their
peak aerobic capacity (V̇O2peak). Subjects could walk, bike, or row, Efficiency and Substrate Oxidation Computations
although walking was the primary mode of exercise. Exercise inten-
sity was monitored by the use of heart rate (HR) monitors (Polar The mean values of V̇O2 and V̇CO2 of the last five data points
Electro Oy, Kempele, Finland). For the first 8 wk, the prescription was collected at each of the three steady-state time points from the
based on the subject’s peak HR achieved during the baseline graded submaximal exercise test were used to compute cycling efficiency and
exercise test. For the second 8 wk, the prescription was adapted from substrate oxidation values.
a submaximal exercise test performed at the midpoint. Exercise logs Energy expended (EE) during steady-state exercise (expressed in
and HR monitors were also used for the unsupervised sessions. kcal/min) was calculated adapting the formula of Brouwer (6):
WLEX. Subjects in this group received both of the interventions
described above. EE (kcal/min) ⫽ 共兵关V̇O2(l/min) ⫻ 3.869兴 ⫹ 关V̇CO2(l/min) ⫻ 1.195兴
⫻ 共4.186/60兲 ⫻ 1,000 ⫻ 4.2其/1,000兲 ⫻ 60
Outcome Measures and Testing
GE during steady-state exercise was calculated as the ratio of the
All of the outcome measures were assessed before and after the work accomplished per minute (W converted into kcal/min) to the EE
16-wk intervention following a preintervention-postintervention re- per minute (in kcal/min) (8):
search design. It is important to note that the two groups who
underwent weight loss maintained stable weight for a period of 2 wk GE ⫽ Work(kcal/min)/EE(kcal/min)
before the postintervention measurements.
Exercise economy (EC) was computed as the ratio of the work
Anthropometric measures included weight and height. Weight was
accomplished per minute (W converted to kcal/min) by the mean V̇O2
measured on a calibrated medical digital scale (model BWB-800,
(l/min) (26):
Tanita, Tokyo, Japan) in undergarments. Height was measured at the
same time with a wall-mounted stadiometer. Body mass index (BMI) EC (kcal/l) ⫽ Work(kcal/min)/V̇O2(l/min)
was calculated as weight (kg) divided by square height (m2).
Blood analyses performed for the screening procedure were pro- Systemic carbohydrate (Cho-ox) and fat oxidation (Fat-ox) rates
cessed through standard hospital-certified laboratory protocols. were calculated using the stoichiometric equations of Frayn (11):
Lean body mass (LBM) and fat mass (FM) were assessed by Fat-ox (mg/min) ⫽ 1.67V̇O2 ⫺ 1.67V̇CO2
dual-energy X-ray absorptiometry (GE Lunar Prodigy and Encore
2005 software version 9.30, Lunar). LBM was used to express Cho-ox(mg/min) ⫽ 4.55V̇CO2 ⫺ 3.21V̇O2
measures and computations in relative units.
V̇O2peak was measured using a graded exercise protocol on an The Fat-ox value were then transformed into kilocalories per
electronically braked cycle ergometer (Ergoline 800S, Sensormedics, minute and expressed as a proportion of energy derived from fat (EF):
Yorba Linda, CA) as described previously (31). HR, blood pressure, EF共%兲 ⫽ 关Fat-ox(kcal/min)/EE(kcal/min)兴 ⫻ 100
and electrocardiogram were recorded before, during and after the
exercise test. V̇O2 was computed via indirect calorimetry (Moxus, AEI Protein oxidation rates were not included based on our laboratory’s
Technologies, Pittsburgh, PA). To account for a possible learning prior work demonstrating that rates of urinary nitrogen excretion were
effect, 14 subjects repeated this test at both time points; thus they similar in lean and obese subjects during resting conditions (16) and
performed a total of 4 tests (2 before the intervention and 2 after the on the assumptions that the amount of proteins oxidized and other
intervention). metabolic processes (such as gluconeogenesis from proteins, ketone
Percutaneous muscle biopsies were obtained by a physician from body formation, and lipogenesis) during exercise are quantitatively
the vastus lateralis muscle after an overnight visit. The proportions of negligible compared with glucose and fatty acid oxidation (28).

J Appl Physiol • VOL 105 • SEPTEMBER 2008 • www.jap.org


EXERCISE TRAINING, WEIGHT LOSS, AND MUSCULAR EFFICIENCY 827
Statistical Analysis among the three groups whether the data were expressed in
absolute terms (Table 1) or relative to LBM (data not shown).
Data are presented in terms of means ⫾ SE. After exploring the
data for outliers and checking the assumptions, one-way ANOVAs All of the variables were normally distributed with the excep-
were performed to compare baseline characteristics between groups. tion of EE and EF. Equality of variances was assumed for all
When needed, post hoc tests were used with the Tukey-Kramer the variables except for LBM or EF. However, a nonparametric
honestly significant adjustment. If the assumptions of normality (Sha- test (Kruskal Wallis) revealed that EE, LBM, and EF were also
piro-Wilk test) and of equal variances (Levene test) were not met, similar among groups.
baseline comparisons between groups for these specific variables were At baseline, BMI was negatively associated with GE (R2 ⫽
performed using the nonparametric Kruskal Wallis test. Baseline sex 0.09, P ⫽ 0.02). In contrast, V̇O2peak was positively associated
differences were explored with an independent t-test or the nonpara- with GE (R2 ⫽ 0.41, P ⬍ 0.01). Similar associations were
metric Mann-Whitney test. found with GE normalized to LBM (Fig. 1). The same pattern
Simple linear regressions were performed to look at the linear
relationship between efficiency measures and BMI, V̇O2peak and
was observed between BMI and EC (R2 ⫽ 0.15, P ⬍ 0.01) and
proportion of muscle fiber type I. between V̇O2peak and EC (R2 ⫽ 0.22, P ⬍ 0.01). No significant
A 3 ⫻ 2 repeated-measures ANOVA was performed on the baseline association was found between the percentage of
dependent variables as a function of intervention (3 levels: WL, EX, type I fibers and GE (R2⫽ 0.01, P ⫽ 0.43) or EC (R2 ⫽ 0.01,
WLEX) and time (2 levels: pre- and postintervention). Pairwise P ⫽ 0.44).
comparisons using the Bonferroni adjustment for multiple compari- At baseline, men (n ⫽ 26) weighed on average 11.5 kg more
sons were conducted (on the between and/or the within subject (P ⬍ 0.001) and had on average 16.8 kg more (P ⬍ 0.001)
factors) to discriminate between means when ANOVA yielded sig- LBM than women (n ⫽ 38). The mean BMI was similar in men

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nificant results. The assumptions of compound symmetry were and women (30.6 and 30.8 kg/m2, respectively). Men had a
checked with the Box’s M and the Mauchly’s test. To examine the higher cardiorespiratory fitness (V̇O2peak) than women when
additive effect between the WL and the EX interventions, a priori
pairwise comparisons were performed on the effects of intervention
expressed in absolute terms (l/min) (52.3%; P ⬍ 0.001). This
on the efficiency measures (GE and EC). The pairs (WLEX vs. WL) difference, however, was reduced when expressed in units
and (WLEX vs. EX) were compared using post hoc (pairwise com- relative to LBM (7.8%; P ⫽ 0.10). EE during the submaximal
parisons on the between subject variable) within the 3 ⫻ 2 repeated- exercise bout was 47.9% higher (P ⬍ 0.001) in men compared
measures ANOVA model. with women. However, this difference disappeared (3.2%; P ⫽
A multivariate regression analysis was used to look at the predic- 0.3) when expressed in relative units (kcal䡠min䡠kgLBM). The
tors of the change in efficiency. baseline values for GE ranged from 6.8 to 19.0% with a mean
For all analyses, the alpha level was set a priori at 0.05. All of 11.5 ⫾ 0.3%. This is somewhat lower than that reported for
statistics were performed using JMP version 5.0.1.2 and SPSS 16.0 trained athletes (19.8 ⫾ 0.6%) (26) but within the range
for Macintosh. reported for healthy women (11.8 ⫾ 0.3%) (4) and men
RESULTS (14.3 ⫾ 0.1%) (14). In our study, GE was 14.8% higher (P ⫽
0.008) in men than women when expressed in absolute units,
Baseline Characteristics but women had a 23.8% greater (P ⫽ 0.002) GE when
expressed relative to LBM. EC had a similar pattern with a
Baseline characteristics in the three groups are presented in higher (16.3%; P ⫽ 0.005) absolute economy in men compared
Table 1. BMI was lower (P ⬍ 0.05) in the EX group compared with women, but women had a 23.1% higher (P ⫽ 0.002)
with the WL and WLEX group. All of the submaximal exercise economy than men when EC was expressed relative to LBM.
measures (EE, GE, EC, and EF) at baseline were similar The proportion of type I fibers was not significantly different
between the sexes (49.8 ⫾ 2.6% in women and 44.6 ⫾ 3.1%
in men; P ⫽ 0.20). Women had a higher exercise Fat-ox
Table 1. Baseline characteristics compared with men (16.7 vs. 13.2 ␮mol䡠min⫺1 䡠kgLBM⫺1; P ⫽
0.01) with a higher proportion of EF (46.7% vs. 36.1%; P ⫽
WL EX WLEX
0.005). Conversely, men had a higher exercise Cho-ox com-
n 11 36 17 pared with women (89.0 vs. 69.2 ␮mol䡠min⫺1 䡠kgLBM⫺1; P ⫽
Sex, male/female 5/6 13/23 8/9 0.005).
Age, yrs 68.2⫾1.5 67.0⫾0.6 66.2⫾0.9
BMI, kg/m2 31.6⫾1.0A 29.7⫾0.6B 32.2⫾0.8A
LBM, kg 47.3⫾2.5 47.8⫾1.5 51.6⫾2.9 Changes in Physical Characteristics
FM, kg 38.4⫾2.0A 31.4⫾1.5B 36.3⫾1.9A
BF, % 43.6⫾1.8 38.4⫾1.6 40.3⫾1.8 Changes in BMI, FM, and LBM are presented in Table 2.
Type I fibers, % 51.9⫾3.9 44.2⫾3.1 50.7⫾2.9 Although all groups lost a statistically significant amount of
V̇O2peak, ml 䡠 kgLBM⫺1 䡠 min⫺1 29.3⫾1.6 33.5⫾1.0 33.3⫾1.2 weight, BMI, and FM, the WLEX and WL groups lost signif-
EE, kcal/min 4.2⫾0.28 4.6⫾0.21 5.0⫾0.33 icantly more weight in line with their weight-loss goal (8.5 ⫾
GE 0.10⫾0.01 0.12⫾0.01 0.12⫾0.00
EC, kcal/l 0.49⫾0.03 0.58⫾0.02 0.58⫾0.02
0.8 and 9.2 ⫾ 1.4% for WLEX and WL, respectively). The WL
EF, % 38.4⫾2.0 44.2⫾2.5 41.1⫾4.6 group lost more LBM than the other groups (interaction effect
P ⬍ 0.001). None of the intervention groups had a significant
Values are means ⫾ SE; n, no. of subjects. WL, diet-induced weight loss;
EX, exercise training; WLEX, combination of both interventions; BMI, body
change in their fiber type proportion (Table 2).
mass index; LBM, lean body mass; FM, fat mass; BF, percent body fat;
V̇O2peak, peak oxygen uptake; EE, energy expenditure during submaximal Changes in Physical Fitness and Physical Activity
exercise; GE, gross efficiency; EC, economy; EF, proportion of energy derived
from fat. Values with different letters are significantly different (1-way The EX and WLEX groups had an increase (P ⬍ 0.05) in
ANOVA), P ⬍ 0.05. V̇O2peak compared with WL (Table 2). Moreover, V̇O2peak
J Appl Physiol • VOL 105 • SEPTEMBER 2008 • www.jap.org
828 EXERCISE TRAINING, WEIGHT LOSS, AND MUSCULAR EFFICIENCY

A Changes in EE During Submaximal Cycling Exercise


Cadence was maintained constant throughout the submaxi-
mal test with an average of 61.0 ⫾ 0.8 revolutions/min in the
preintervention test and 63.0 ⫾ 0.8 revolutions/min in the
postintervention testing. To achieve 50% of their V̇O2peak
during the submaximal test, subject’s power output ranged
from 20 to 75 W, with an average of 37.6 ⫾ 1.9 W in the pre
testing. The exact same wattage was maintained during the
postintervention testing with an average of 37.6 ⫾ 1.9 W. The
mean V̇O2 for all subjects combined was 0.94 ⫾ 0.03 l/min at
baseline and 0.90 ⫾ 0.03 l/min following intervention. Within
each test, V̇O2 was constant across the last 45 min of submaxi-
mal exercise. V̇O2 values were also similar in two identical
exercise bouts separated by 1 wk, both before and after the
intervention (n ⫽ 14; P ⬎ 0.05).
Changes in EE during submaximal exercise are presented in
Fig. 2A. A main effect of time was found (P ⬍ 0.001). Post hoc
B analysis revealed that the decreased EE was only significant
(P ⫽ 0.004) for the WLEX group.

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Changes in GE During Submaximal Cycling Exercise
Changes in GE during submaximal exercise are presented in
Fig. 2B. Significant main effects of intervention (P ⫽ 0.04) and
of time (P ⫽ 0.005) were found. The EX and the WLEX
groups both had an increase in GE with intervention. The

Fig. 1. Simple linear correlations at baseline between gross efficiency (GE),


body mass index (BMI), and peak aerobic capacity (V̇O2peak). A: correlation
between GE normalized to lean body mass and BMI. B: correlation between
GE and V̇O2peak normalized to lean body mass (LBM).

increased (P ⬍ 0.05) within EX and within WLEX. The same


pattern was found with unadjusted means. In the EX group,
subjects exercised on average 3.5 ⫾ 0.1 sessions/wk, expend-
ing 835 ⫾ 67 kcal/wk over the course of the intervention. The
WLEX group exercised on average 3.6 ⫾ 0.2 sessions/wk,
expending 912 ⫾ 87 kcal/wk.

Table 2. Changes in body composition and V̇O2peak


with intervention
WL EX WLEX

BMI ⫺9.3⫾1.4 * B
⫺1.3⫾0.4 * A
⫺8.6⫾0.8B*
FM ⫺16.4⫾2.6B* ⫺3.6⫾1.1A* ⫺18.7⫾2.1B*
LBM ⫺4.3⫾1.2C* 0.1⫾0.4A ⫺1.5⫾0.5B*
Type I fibers ⫺1.2⫾8.7 16.7⫾8.1 ⫺1.6⫾7.1 Fig. 2. Changes in energy expenditure (EE) and GE during submaximal
V̇O2peak 0.4⫾4.5B 10.4⫾2.1A* 4.3⫾3.2A* exercise. A: percent change in EE. B: percent change in GE. Groups: diet-
induced weight loss (open bar), exercise training (gray bar), combination of
Values are means ⫾ SE given as percent change from baseline. Type I both interventions (black bar). Values are mean changes ⫾ SE. Values with
fibers, proportion of type I fibers. Values with different letters are significantly different letters (A and B) are significantly different, P ⬍ 0.05 (repeated-
different, P ⬍ 0.05 (repeated-measures ANOVA). *P ⬍ 0.05 preintervention- measures ANOVA). *P ⬍ 0.05 preintervention-postintervention comparison
postintervention comparisons (within-subject post hoc test). (within-subject post hoc test).

J Appl Physiol • VOL 105 • SEPTEMBER 2008 • www.jap.org


EXERCISE TRAINING, WEIGHT LOSS, AND MUSCULAR EFFICIENCY 829
change in GE was not significant for the WL group. In the a does not appear to significantly enhance either exercise effi-
priori pairwise comparisons, the WLEX group had a greater ciency or fat oxidation during exercise in older overweight to
improvement in GE compared with the WL group (P ⫽ 0.02) obese men and women.
but not to the EX group (P ⫽ 0.78). These increases in exercise efficiency and EC are consistent
with previous work by Rosenbaum and colleagues (34), who
Changes in EC During Submaximal Cycling Exercise found that a program of combined weight loss and increased
Significant main effect of intervention (P ⫽ 0.05) and of physical activity enhanced efficiency at very low levels of
time (P ⫽ 0.007) were found. The EX and WLEX groups muscular work in overweight subjects. The present study
increased EC significantly more than the WL group. In the a builds on this previous observation by delineating the separate
priori pairwise comparisons, the WLEX group had a greater effects of exercise and weight loss. The increase in efficiency
improvement in EC compared with the WL group (P ⫽ 0.03), but specifically due to exercise training in these overweight to
it was not greater than the improvement with EX (P ⫽ 0.74). obese older subjects is consistent with previous studies con-
ducted in younger normal-weight subjects (14, 18). Moreover,
Predictors of Improved Efficiency our findings indicate that at least part of the decreased effi-
ciency that may occur with age (38) is explained by age-
To examine predictors of change in GE, change in weight,
associated decreases in physical activity. This is in accord with
change in V̇O2peak, change in LBM, change in FM, sex, and
earlier studies suggesting that exercise efficiency and EC may
intervention group were put into a stepwise multivariable
not change with advancing age in well-trained older subjects
regression. When examining all groups together, having less of
(1, 3, 36), or that lower exercise efficiency was reversed in
a change in LBM (R2⫽ 0.19, P ⫽ 0.02) and an improved

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older subjects following training (30).
V̇O2peak (R2 ⫽ 0.11, P ⫽ 0.008) were the only significant
The changes in exercise efficiency and V̇O2 following exer-
predictors of the improvement in GE. cise training could be influenced by both peripheral and central
Changes in Fat Oxidation During Submaximal effects. Exercise training, but not weight loss, increased the
Cycling Exercise physical fitness (V̇O2peak). We did not detect significant
changes in fiber type with exercise in the present study, which
The changes in the proportion of energy derived from fat are is in apparent contrast to two of our laboratory’s previous
presented in Fig. 3. A main effect of time was found (P ⫽ studies in similar subjects (9, 31). However, this could be
0.04). Post hoc analysis revealed that EF increased (P ⫽ 0.048) explained by the more rigorous three-group analysis in this
within the EX group. When we combined all subjects that study, particularly given that the magnitude of these changes
exercised (EX and WLEX), we also found a significant im- were similar across these three studies. The possibility remains
provement in EF with intervention (P ⫽ 0.04). The WL group that alterations in energetics within muscle, including the
did not have an increase in fat oxidation. proportion of type I muscle fibers, may play a role in altered
efficiency. At the cellular level, our laboratory has shown that
DISCUSSION
with a similar exercise intervention and subject population,
The effects of body weight changes and physical activity on mitochondrial activity and density were greatly enhanced by
exercise efficiency have received relatively little attention. In exercise (25). The increased efficiency in the present study was
particular, the separate or distinct effects of intentional, energy related to the improvement in physical fitness but not to the
restriction-induced weight loss and exercise training have not increase in the proportion of type I muscle fibers. Moreover,
until now been examined. The key findings of this study were we did not observe an association between efficiency and fiber
that exercise training with or without weight loss increased type at baseline. Rosenbaum et al. (34) found that the increases
exercise efficiency and the amount of energy derived from fat in efficiency were paralleled by increases in the capacity for
during a bout of moderate exercise. However, weight loss itself oxidative phosphorylation determined by nuclear magnetic
resonance spectroscopy. In addition, in young highly trained
cyclists, a higher percentage of type I muscle fibers has been
associated with higher efficiency (8). Thus the possibility
remains that muscle fiber type, mitochondria activity, or oxi-
dative capacity can account for efficiency at higher levels of
work. It is also possible that changes in other characteristics
within skeletal muscle, for example, capillarization or muscle
blood flow, may contribute to the increased efficiency with
exercise training. This requires further investigation.
Energy restriction-induced weight loss without an increase in
physical activity in our study did not significantly increase
efficiency. Moreover, the effects of weight loss and exercise
were not additive. Body mass has been suggested to be an
important factor in relation to efficiency (4). The changes in
efficiency with weight loss could be attributed to the work of
the moving legs (2) and the extra weight carried in the legs
Fig. 3. Changes in fat oxidation during submaximal exercise. Groups: diet-
induced weight loss (open bar), exercise training (gray bar), combination of
(20). Although these factors might explain the weight loss
both interventions (black bar). Values are mean changes ⫾ SE. *P ⬍ 0.05 effects on improved efficiency, it is highly unlikely that they
preintervention-postintervention comparison (within-subject post hoc test). accounted for the changes in efficiency observed following
J Appl Physiol • VOL 105 • SEPTEMBER 2008 • www.jap.org
830 EXERCISE TRAINING, WEIGHT LOSS, AND MUSCULAR EFFICIENCY

exercise training because this intervention did not promote In summary, moderate increases in physical activity levels,
substantial weight loss. either with or without concomitant weight loss, enhanced
An increase in efficiency may have significant implications exercise efficiency in previously sedentary, overweight to
for older men and women, who are at greater risk for the obese men and women. In contrast, weight loss alone did not
development of functional limitations. An increased efficiency significantly enhance efficiency in these subjects. Moreover,
during moderate levels of physical activity examined in this exercise training, but not weight loss, increased the reliance on
study would imply that activities of daily living would require fatty acids during moderate exercise. Further research needs to
less energy. This could be clinically relevant for older men and be performed to determine whether or not these changes in
women, who typically have low capacity for physical work, energy metabolism due to exercise or weight loss play a role in
that is, they would require proportionately less energy of their modulating cardiometabolic risk or improving functional per-
maximal functional capacity. Another perspective is that a formance in old age or obesity.
decrease in energy required for physical activity (increased
ACKNOWLEDGMENTS
efficiency) may theoretically hinder efforts to lose weight or to
maintain weight loss in obesity. In our study, the mean increase We thank the volunteers for the participation in this study. We also
acknowledge the valuable contributions of Krista Clark for directing the
in efficiency due to the combination of weight loss and exercise diet-induced weight loss programs.
would correspond to a decrease of 0.4 kcal/min expended Part of this work has been presented as a poster at the annual scientific
during the 1 h of moderate exercise. At 3 h of exercise per meeting of the North American Association for the Study of Obesity in
week, this increased efficiency in our subjects would require October 2007 in New Orleans, LA.
them expend an additional 67 kcal/wk, or an additional ⬃16 GRANTS

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min of weekly leisure walking. Therefore, this should not be a
This work was supported by American Diabetes Association clinical Re-
practical concern. search Award (to B. H. Goodpaster), National Institute on Aging Grant R01
Another key finding was that exercise training increased the AG-20128, General Clinical Research Center Grant 5M01 RR-00056, and
relative reliance on fat oxidation during a moderate-intensity Obesity Nutrition Research Center Grant 1P30 DK-46204.
bout of exercise. This response was observed in subjects who
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