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Med Sci Sports Exerc. Author manuscript; available in PMC 2014 July 01.
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Abstract
Purpose—To examine the effects of three different frequencies of combined resistance and
aerobic training on total energy expenditure (TEE) and activity related energy expenditure (AEE)
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Introduction
Total daily energy expenditure (TEE) is an important contributor to metabolic health (11). In
addition, free living activity related energy expenditure (AEE) is related to reduced weight
gain (31, 34) while exercise training reduces weight regain following weight loss (12).
However, on the average, older individuals have lower AEE than younger individuals (36).
The ability to perform daily tasks reaches a peak at 30 years but declines thereafter (14).
This decline seems to be a result of declining physical activity, reduced strength, as well as
the independent effects of aging itself (14).
Corresponding Author: Gary R. Hunter, PhD, Room 205 Education Building, 901 South 13th Street, University of Alabama at
Birmingham, Birmingham, Alabama 35294-1250, Tel. 205 934-8338, Fax 205 975-8040, ghunter@uab.edu.
There is not conflict of interest for any of the authors.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
Hunter et al. Page 2
Lower levels of physical activity in older adults are at least partly explained by lower
maximum oxygen uptake (VO2max) and increased difficulty in performing daily tasks (17).
Additionally, muscular strength is associated with increased physical activity and is
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predictive of reduced one-year weight gain (34). Thus, the maintenance of both aerobic
fitness and strength seem to be important for the maintenance of TEE.
Increased aerobic fitness and strength adjusted for body weight, ease of performing daily
tasks such as walking, stair climbing, and carrying a simulated box of groceries, are related
to increased AEE (35), suggesting increased ease of physical activity may lead to a more
active lifestyle. Indeed, resistance training results in increased ease in walking, stair
climbing, carrying a small load and rising from a chair (16, 19). However, older women who
resistance train intensely three times/week increase less in ease of performing daily tasks
(19) and hypertrophy less (2, 9) than women who resistance train intensely less frequently.
In addition, subjective feelings of fatigue increase and vigor decreases when training volume
increases in competitive swimmers (26, 28). Taken together, these results suggest that
resistance training may be important for maintaining ease during daily tasks such as
walking, stair climbing, carrying, and rising from a chair; however, training too intensely too
frequently may result in increased fatigue and a reduced training adaptation in older women.
Training less than twice a week for any particular modality (strength training once/week or
aerobic training once/week) is usually felt to be sufficient for maintaining fitness but of
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insufficient frequency to improve fitness. However, a program in which older adults aerobic
and resistance trained once/week for 16 weeks resulted in similar increases in strength and
aerobic fitness as twice/week aerobic and resistance training (20), suggesting older adults
may require less frequent training than younger adults.
It is not clear what effect exercise training has on TEE in older adults. TEE and AEE have
been shown to be elevated in chronically active compared to chronically inactive women,
49–70 years old (37). TEE increases following resistance training in younger males (33) and
older women with coronary heart disease (1). However, TEE did not increase following an 8
week high intensity aerobic training program (8) for 58–78 year old men and women,
suggesting a reduction in non-exercise training activity related thermogenesis (NEAT). The
high intensity (85% VO2max), and short duration may have led to reduced NEAT because
of overtraining in the untrained older adults.
Some studies suggest increases in NEAT (23) following exercise training. Resistance
training in non-alcoholic fatty liver disease patients resulted in more steps/day (10). In
addition, 24 weeks resistance training program increased TEE, with a trend toward an
increase in NEAT (18). To our knowledge, no one has examined the effects of combined
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training on TEE and NEAT in older adults. Since training volume and time will be doubled
with combined training compared to either resistance or aerobic training alone, it is possible
that training too frequently may lead to overstress.
Intense exercise can cause muscle damage (3, 4) with an up-regulation of acute
inflammation (29). To frequent training may lead to chronic inflammation and production of
circulating pro-inflammatory cytokines such as interleukin-1β (IL-1β), tumor necrosis
factor-α (TNF-α), and interleukin-6 (IL-6) (32). A growing body of literature suggests that
elevated pro-inflammatory cytokines provide a link between the blood and brain (24),
causing mood changes favoring inactivity.
Consistent with the concept that overstress may lead to mood changes, muscle soreness was
accompanied by increases in depression, anger, and fatigue in collegiate swimmers (26).
Despite an improvement in overall mood resulting from 24 weeks of resistance training in
older adults (25), increased training volume in a combined resistance and aerobic training
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Hunter et al. Page 3
program resulted in increased depression, decreased vigor (27) and increased fatigue (26).
Thus pro-inflammatory cytokine production and changes in mood may explain the reduction
in NEAT in some studies and the inverse relationship between exercise intensity and
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Therefore, the purpose of this study was to examine the effects of three different frequencies
(1 day/week of aerobic and 1 day/week of resistance (1+1) versus 2 day/week of aerobic and
2 day/week resistance (2+2) versus 3 day/week aerobic and 3 day/week resistance (3+3)) of
16 weeks of combined resistance and aerobic training has on pro-inflammatory cytokines,
subjective feelings of fatigue/depression/vigor, TEE, AEE and NEAT in a group of older
women. We hypothesize the 2+2 group will have larger increases in strength, aerobic
fitness, TEE, AEE, and NEAT than either the 1+1 or 2+2 training groups. In addition, we
hypothesize that the 3+3 group will exhibit indicators of increased overstress such as
increased depression and fatigue, reduced vigor, and increased pro-inflammatory cytokines
while the 2+2 and the 1+1 groups will not.
Methods
Subjects
Seventy-two women, 60 – 74 years old, participated in a 16 week combined aerobic and
resistance training program. All subjects were healthy, free of any metabolic disorders, not
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taking medications that may affect energy expenditure, non-smokers, and sedentary (defined
as exercising less than once per week for the past year). Institutional Review Board
approved informed consent was obtained prior to participation in the study in compliance
with the Department of Health and Human Services Regulations for Protection of Human
Research Subjects. Subjects were evaluated before and after 16 weeks of combined
resistance and aerobic training. Subjects were randomly assigned to one of three training
groups (1+1, 26 subjects; 2+2, 26 subjects; or 3+3, 22 subjects).
Exercise Training
Training sessions lasted 50 minutes in a facility dedicated to research and under the
supervision of exercise physiologists. Each session began with a three to four minute warm-
up on a cycle ergometer or treadmill, and three to four minutes of stretching.
increased to 71% maximum heart rate at week six but duration decreased to 30 minutes.
Week seven duration increased to 40 minutes. Exercise heart rate increased to 75%
maximum heart rate at week eight but duration decreased to 30 minutes. Week nine exercise
duration increased to 40 minutes. Exercise heart rate increased to 80% maximum heart rate
at week ten but duration decreased to 30 minutes. Week eleven duration increased to 40
minutes. The subjects then trained at 80% maximum heart rate for 40 minutes each training
session for the remainder of the study. Exercise modalities included both cycle ergometer
and treadmill exercise. At least 50% of the training time was done on the treadmill.
Resistance Training—Strength exercises included leg press, squats, leg extension, leg
curl, elbow flexion, lateral pull-down, bench press, military press, lower back extension, and
bent leg sit-ups. Each exercise consisted of two sets of 10 repetitions with a 1.5–2-minute
rest between sets. The intensity began at 60% of the maximum weight the subject could lift
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at one time (1RM) and was gradually increased to 80% of 1RM at week 8. Subject 1RM was
determined every fifth week to ensure that intensity was increased appropriately.
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Aerobic Capacity
Maximal aerobic exercise testing was physician-supervised and conducted using the
modified Balke treadmill test protocol. A metabolic cart, calibrated prior to testing (Max-1
Cart, Physio-Dyne Instrument Corporation, Quogue, NY), was used to evaluate ventilatory
expired gases. Monitoring consisted of 12-lead electrocardiogram and BP measurements
taken every two minutes (Omron Blood Pressure Monitor, model HEM-780; Omron
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Healthcare, Inc 1200 Lakeside Dr. Bannockburn, IL). The testing commenced with treadmill
walking at two mph for two minutes. Treadmill grade was increased 3.5% every 2 minutes
until minute 12 at which time grade was decreased to 12% and speed was increased to 3
mph. The grade then increased 2.5% each minute until exhaustion. Blood pressure, heart rate
and oxygen uptake were recorded during the last 20 seconds of each level. Participants were
encouraged to exercise to fatigue. Termination criteria for testing followed American Heart
Association/American College of Cardiology guidelines (5); (6). Maximum oxygen uptake
(VO2max in mL · kg−1 · min−1), maximum respiratory exchange ratio (RER), and maximum
heart rate were defined as the highest 20-second averaged value. Criteria for obtaining
maximum oxygen uptake were heart rate within 10 beats of age predicted maximum,
plateauing of oxygen uptake, and RER 1.1 or larger.
REE
REE was measured between 6:00 and 8:00 AM after a 12 hour fast. Subjects were not
allowed to sleep and measurements were made in a quiet, softly lit, well ventilated room.
Temperature was maintained between 22 and 24 degrees centigrade. Measurements were
made supine on a comfortable bed, with the head enclosed in a plexiglass canopy. Post
training REE was measured 41 hours after the last resistance exercise session. After resting
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for 15 minutes, REE was measured for 30 minutes with a computerized, open-circuit,
indirect calorimetry system with a ventilated canopy (Delta Trac II, Sensor Medics, Yorba
Linda, CA). The last 20 minutes of measurement was used for analysis. Oxygen uptake
(VO2) and carbon dioxide production (CO2) were measured continuously and values were
averaged at one-minute intervals. Energy expenditure and RER were calculated from the
VO2 and CO2 data.
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of exercise, between 20th and 25th minutes of exercise and between 35th and 40th minutes of
exercise and averaged. Oxygen uptake was converted to kcal/session (5 kcal × liters O2/min
× 40 minutes).
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We measured the energy cost of the resistance training and 15 minutes of recovery on a
subset of 25 subjects (COSMED K4 b2 portable metabolic system (COSMED S. r. l., Rome,
Italy)). Based on these measured values we developed a regression equation for estimating
energy expenditure for the rest of the subjects based upon the amount of weight lifted in
each of the exercises use in the resistance training. We then validated the equation using a
different set of older women (n =14) and found that the R2 between predicted and actual
energy expenditure to be 0.95 (standard error of estimate of 11 kcal) using methods we have
previously described(21). Actual measured resistance training energy expenditures were
used for the 25 subjects that had measured resistance training energy expenditures while
estimated energy expenditures were generated from the regression equation for those
remaining subjects.
DXA
Dual-energy X-ray absorptiometry (Lunar DPX-L densitometer; LUNAR Radiation,
Madison WI) in the Department of Nutrition Sciences at UAB was used to determine total
fat and lean mass. Adult Software, version 1.33, was used to analyze the scans.
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TEE
TEE was measured prior to and during the last 2 weeks of resistance training using the
doubly labeled water technique as previously described (34). Four timed urine samples were
collected after oral dosing of the doubly labeled water: two urine samples were taken in the
morning after dosing and two more urine samples were taken 14 days later with a loading
dose of 1 gram of pre-mixture (10% H2 18O and 8% 2H2O) per kilogram of body weight.
The isotopic dilution spaces were calculated from the H2 18O and 2H2O enrichments in the
body by the extrapolation of the log enrichments back to zero time using the following
equation: Dilution space (liters) = d/20.02 • 18.02 • 1/R • E where: d is grams of H2 18O
and 2H2O given, R is the standard ratio for 18O:16O (0.002005) and 2H:1H (0.00015576), E
is the enrichment of the H2 18O and 2H2O at the extrapolated zero time (the % above
background). The rate of carbon dioxide production (rCO2) was calculated from the
equation by Schoeller (30): rCO2 = 0.4554 • N (1.01 K0 – 1.04 Kh) where rCO2 is the
amount of CO2 produced (mol/day) corrected for fractionation, N is total body water (mol)
K0 and Kh are the turnover rates of H2 18O and 2H2O (days −1) respectively. TEE was then
calculated from CO2 production using the equation from de Weir [de Weir 1949 1769/id]:
TEE (kcal/day) = 3.9 (rCO2/FQ) + 1.1 rCO2, where TEE is total energy expenditure (kcal/
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day), rCO2 is the rate of carbon dioxide production (l/day where 1 mol of CO2 is equivalent
to 22.4 l) and FQ is the food quotient. Samples were analyzed in triplicate for H2 18O
and 2H2O by isotope ratio mass spectrometry at the University of Alabama at Birmingham
as previously described (7). Samples for H2 18O and 2H2O were re-analyzed in seven
subjects, the values of TEE between days were in close agreement (coefficient of variation =
4.3%) thus, demonstrating a high level of reproducibility.
AEE
AEE was estimated by subtracting REE from TEE after reducing total energy expenditure
by 10% to account for the thermic response to meals. NEAT was calculated as NEAT =
AEE − energy cost of exercise training (23).
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TNF-α was analyzed using the high-sensitivity ELISA kit (Quantikine HSTA00C, R&D
Systems, Minneapolis, MN). IL-6 was assayed using the high-sensitivity ELISA kit
(Quantikine HS600B, R&D Systems). CRP was assayed with the high-sensitivity ELISA kit
(030-9710s, ALPCO, Windham, NH). We were not able to obtain data in either the pre- and
post-training states for twenty-four subjects. Therefore, we have cytokine data for only 50
subjects.
subjects in either the pre- or post-training time points. Therefore, questionnaire data includes
only 55 subjects.
Statistics
The purpose of this investigation was to evaluate the effects of three frequencies of
combined resistance and aerobic training on TEE, AEE, and NEAT in older adults. Two-
way repeated measures ANOVA (training by group), with repeated measures for the training
factor, were run for all variables except for age and height for which a one-way (group)
ANOVA was run. Tukey post-hoc tests were used to determine pre/post differences in
energy expenditure variables for each of the 3 groups for variables in which there were
significant time by group interactions. Significance was set at 0.05 for all statistical tests.
Results
Descriptive data are presented in table 1. No group differences were observed for height or
age. There was a significant time effect showing a significant loss of weight (not more than
1.2 kg for any group, p < 0.04), %fat (varying from −0.5% to −1.9%, p < 0.01), and fat mass
(varying from −0.6 to −1.8 kg, p <0.01), but no time by group interaction. Fat free mass
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increased significantly (varying from +0.4 kg to +0.7 kg, p < 0.01) with no time by group
interaction. Strength in the leg press (p < 0.0.01) and bench press (p < 0.01) as well as
VO2max (p < 0.0.01) increased significantly pre to post-test but there was no time by group
interaction. No time or time by group interactions were observed for fatigue or depression
but vigor (p < 0.01) did increase significantly with no time by group interaction. No time,
group, or time by group interactions were observed for any of the cytokines.
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Because of the different training frequencies average daily exercise energy expenditure
(total exercise energy expenditure per week/7 days) during exercise training was
significantly different between the 3 groups (p < 0.01). No time effect was observed for
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NEAT (AEE - average daily energy expenditure during exercise training), however there
was a significant time by group interaction (p < 0.01). Post-hoc tests showed that the 1+1
group did not significantly change, but a significant increase for the 2+2 group (p < 0.01)
and significant decrease for the 3+3 group (p< 0.05) was observed.
Discussion
We are not aware of any previous studies that have evaluated the effects of different
frequencies of combined aerobic and resistance training on TEE in older adults. Consistent
with our hypothesis, we found TEE increased more following the 2+2 combined training
than either the 1+1 or 3+3 combined training (Figure 1). This was especially the case for
NEAT with the 3+3 group actually decreasing NEAT -192 kcal/day during the last two
weeks of exercise training while the 1×1 showing a non-significant increase of +127 kcal/
day and the 2+2 group significantly increasing NEAT +224 kcal/day (Figure 1). 14
Subjects were asked to maintain weight, but as often happens with aerobic exercise training
studies a small weight loss occurred suggesting that appetite was not increased proportional
to the small increase in energy expended. Similar to other resistance training programs in
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older women (2, 13) fat free mass increased modestly (0.4 to 0.7 across the 3 groups)
suggesting a blunted hypertrophic response when compared to older men (14). However,
there was no time x group interaction, suggesting all groups changed similarly. The
combination of the small weight loss and increased FFM induced a decrease in %fat.
Despite increased training frequency and volume the 3+3 group did not increase FFM more
than the other groups, suggesting that in older women 1+1 training is as sufficient a stimulus
for hypertrophy as 2+2 or 3+3 training. Interestingly, there was also no difference in weight
or FFM decreases across the 3 groups despite the increased training frequency/volume and
approximately tripled exercise training daily energy expenditure in the 3+3 compared to the
1+1 group, probably because the 3+3 group compensated by reducing NEAT.
We originally hypothesized that the 1+1 group would have lower increases in fitness and
TEE because of insufficient training frequency/volume and the 3+3 group would have lower
increases in fitness and TEE because of too frequent training frequency/volume. We also felt
that the 3+3 group would have increased feelings of fatigue and depression and decreased
vigor. Our original thinking on this topic was that the increased strength and aerobic fitness
adaptations in the 2+2 group would lead to increased NEAT and the increased feelings of
fatigue in the 3+3 group would lead to a reduction in NEAT. Contrary to our hypothesis
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strength and aerobic fitness increased similarly in the three groups. None of our measures of
increased stress, i.e. cytokines and feelings of fatigue and depression changed with training.
Vigor not only did not decrease in the 3+3 group, but it increased similarly in all 3 groups. It
is unlikely the 3+3 day/week training overstressed these older women. Therefore overstress/
fatigue does not seem to be the reason for the reduced NEAT found with the 3+3 training.
However, the 3+3 day/week training was very time consuming. The most consistent
complaint for the 3+3 group was the very large time commitment needed for 6 exercise
training sessions each week. It is possible the 3+3 group reduced NEAT during the week
because of time restraints rather than fatigue. The 3+3 group should have experienced an
increase in TEE if they simply decreased the time spent in being physically active in their
free time (producing NEAT) for the extra time spent in aerobic and resistance training,
likely due to the energy cost for each minute of exercise training being larger than the
energy cost per minute during NEAT. NEAT was reduced more than the extra cost of
training in the 3+3 group. This appears likely since the 3+3 group had 376 kcal/day lower
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Hunter et al. Page 8
NEAT than the 2+2 group but only 40 kcal/day higher energy cost of training. It is possible
the 3+3 group perceived that the training was taking more of their time than it really was and
thus overcompensated in time spent in NEAT. However, this is just speculation and offers
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an alternative hypothesis for explaining the decreased NEAT, since our cytokine and
perception of fatigue data do not support overstress and fatigue as the cause of the reduced
NEAT for the 3+3 group. Future work should be conducted to test this hypothesis.
It is important to point out that the results of this study only apply to women aged 60–74
years who have done combined training for a period of 16 weeks. In addition, all the training
was done in our research gym which adds to the time commitment by requiring transport
time to and from the gym for each workout. It is possible results may have been different if
men instead of women, older or younger subjects had been used or if home exercise that
presumably would have been less time consuming was used.
combined aerobic and resistance training program is to increase TEE, twice per week
training is more successful than more frequent or less frequent training.
Acknowledgments
This work was supported by the NIH grants R01AG027084-01, R01 AG027084-S, P30 DK56336, P60 DK079626,
UL 1RR025777.
The authors thank David Bryan, Bob Petri, and Paul Zuckerman for help in data acquisition.
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Figure 1.
Pre and post 16 weeks training energy expenditure data. Total energy expenditure/day (TEE)
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is divided into average aerobic/resistance exercise training energy expenditure (AREE), non-
exercise activity thermogenesis (NEAT), thermogenesis of food, and resting energy
expenditure (REE). A significant increase in TEE and NEAT was observed for group 2 (p <
0.01) while group 3 had a significant decrease in NEAT (p<0.05). No other significant
changes in EE occurred.
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Table 1
Body composition, fitness, cytokine, and subjective feelings of fatigue, depression, and vigor. Seventy-four subjects except for the VO2max,
psychometrics, and cytokines. Sample size for each group included for those variables.
Hunter et al.
Weight (kg) 78.1±14.3 77.5±12.8 74.2±9.4 73.0±8.8 68.3±9,6 68.2±9.6 T < 0.04
G < 0.02
TxG=0.33
Fat Mass (kg) 35.5±11.4 34.4±10.0 32.4±6.8 30.5±6.0 27.5±7.4 27.0±7.3 T < 0.01
G < 0.01
TxG=0.25
Fat Free Mass (kg) 42.5±4.2 43.1±4.5 41.8±4.7 42.5±4.6 40.8±3.4 41.2±3.6 T < 0.01
G = 0.32
TxG=0.82
Leg Press St (kg) 90.9±25.7 109.5±32.7 95.1±20.6 112.3±29.1 93.5±25.9 116.3±26.2 T < 0.01
G = 0.84
TxG=0.57
Bench Press St (kg) 22.2±4.9 25.4±6.7 24.3±6.3 28.5±6.5 24.2±5.6 29.2±6.9 T < 0.01
G = 0.15
TxG=0.39
VO2max (ml/kg/min) 21.8±4.5 22.3±4.7 (N=24) 22.6±4.7 24.4±3.7 (n=24) 23.7±4.3 24.7±5.1 (n=21) T < 0.01
G = 0.20
TxG=0.26
IL-6 2.0±1.4 1.7±1.1 (n=16) 1.5±0.6 1.5±0.6 (n=18) 2.4±2.3 2.3±2.8 (n=16) T = 0.41
Med Sci Sports Exerc. Author manuscript; available in PMC 2014 July 01.
G = 0.30
TxG=0.73
CRP 2.5±2.2 2.7±2.5 (n=16) 2.6±3.0 2.1±2.3 (n=18) 3.7±3.6 3.6±3.6 (n=16) T = 0.75
G =0.38
TxG=0.71
TNF-α 6.3±2.1 6.1±2.3 (n=16) 6.9±2.4 6.7±2.3 (n=18) 6.7±2.3 6.7±2.4 (n=16) T =0.56
G =0.71
TxG=0.90
Fatigue 4.5±6.0 3.7±3.3 (n=20) 4.7±2.9 4.5±3.6 (n=17) 4.1±3.8 3.4±3.4 (n=18) T = 0.27
G = 0.79
TxG=0.86
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Vigor 19.4±4.2 21.0±4.7 (n=20) 16.6±4.9 18.6±4.9 (n=17) 19.4±5.5 21.0±5.4 (n=18) T < 0.01
G = 0.14
TxG=0.97
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Table 2
Means and standard deviations of total energy expenditure (TEE), resting energy expenditure (REE), activity related energy expenditure (AEE), average
aerobic/resistance exercise energy expenditure (AREE, daily rate averaged over one week), and non-exercise training activity thermogenesis (NEAT) for
74 women aged 60 to 74 years.
Hunter et al.
REE kJ/d (kcal/d) 5381±887 (1286±212) 5058±682 (1209±163) 5192±699 (1241±167) 5104±845 (1220±202) 5079±602 (1214±144) 4937±661 (1180±158) T = 0.11
G = 0.57
TxG= 0.47
AEE kJ/d (kcal/d) 2364±1192 (565±285) 2803±1435 (670±343) 2481±1490 (593±356) 3678±1644** (879±393) 2372±1339 (567±320) 2272±1195 (543±286) T < 0.02
G = 0.07
TxG< 0.03
AREE kJ/d (kcal/d) 176±33.5 (44±8) 360±59 (86±14) 515±88 (126±21) G < 0.01
NEAT kJ/d (kcal/d) 2364±1130 (565±270) 2648±1573 (626±376) 2481±1443 (593±345) 3310±1594** (793±381) 2372±1314 (567±314) 1741±1065* (417±254) T = 0.31
G < 0.03
TxG< 0.01
*
Tukey post hoc test, significantly different from pre-test value (p < 0.05).
**
Tukey post hoc test, significantly different from pre-test value (p < 0.01).
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