Professional Documents
Culture Documents
doi: 10.1111/j.1467-789X.2011.00931.x
Obesity Treatment/Management
obr_
931
68..9168..91
Summary
It is increasingly recognized that the location of excess adiposity, particularly
increased deposition of visceral adipose tissue (VAT), is important when determining the adverse health effects of overweight and obesity. Exercise therapy is an
integral component of obesity management, but the most potent exercise prescription for VAT benefit is unclear. We aimed to evaluate the independent and
synergistic effects of aerobic exercise (AEx) and progressive resistance training
(PRT) and to directly compare the efficacy of AEx and PRT for beneficial VAT
modulation. A systematic review and meta-analysis was performed to assess the
efficacy of exercise interventions on VAT content/volume in overweight and obese
adults. Relevant databases were searched to November 2010. Included studies
were randomized controlled designs in which AEx or PRT in isolation or combination were employed for 4 weeks or more in adult humans, where computed
tomography (CT) or magnetic resonance imaging (MRI) was used for quantification of VAT pre- and post-intervention. Of the 12196 studies from the initial
search, 35 were included. After removal of outliers, there was a significant pooled
effect size (ES) for the comparison between AEx therapy and control (-0.33, 95%
CI: -0.52 to -0.14; P < 0.01) but not for the comparison between PRT therapy
and control (0.09, 95% CI: -0.17 to -0.36; P = 0.49). Of the available nine
studies which directly compared AEx with PRT, the pooled ES did not reach
statistical significance (ES = 0.23, 95% CI: -0.02 to 0.50; P = 0.07 favouring
AEx). The pooled ES did not reach statistical significance for interventions that
combined AEx and PRT therapy vs. control (-0.28, 95% CI: -0.69 to 0.14;
P = 0.19), for which only seven studies were available. These data suggest that
aerobic exercise is central for exercise programmes aimed at reducing VAT, and
that aerobic exercise below current recommendations for overweight/obesity
management may be sufficient for beneficial VAT modification. Further investigation is needed regarding the efficacy and feasibility of multi-modal training as a
means of reducing VAT.
Keywords: Aerobic training, obesity, physical activity, strength training.
obesity reviews (2012) 13, 6891
68
obesity reviews
Introduction
The increased risk of cardiovascular and metabolic morbidity and mortality as result of obesity has been well
described. However, it is increasingly recognized that
the location of excess adiposity, particularly increased
deposition of visceral adipose tissue (VAT), is of greater
importance in determining the adverse health effects of
overweight and obesity. VAT volume is an independent
predictor of elevated blood pressure (1), myocardial infarction (2) and insulin resistance (24). Lifestyle interventions
incorporating restriction of caloric intake and/or increased
energy expenditure via exercise reduce VAT content,
thereby ameliorating this risk. Serial quantification of VAT
content/volume by computed tomography (CT) and magnetic resonance imaging (MRI) has shown that the synergy
of aerobic exercise training and calorie restriction positively affects VAT content when weight loss approximating
49% of body weight is achieved (5), and larger reductions
in VAT have also been shown following a mean 10%
reduction in body weight (6).
Current physical activity recommendations suggest that
~250 min of weekly aerobic-type exercise is required for
body weight management (7) (8). The actual reduction of
weight (and body fat) with this dose of regular exercise in
overweight and obese individuals is often small (~23 kg)
but increases (~57.5 kg) with exercise levels up to
420 min/week (911). However, there is an emerging
acceptance that even with intensive programmes, weight
loss in excess of 34 kg is difficult to sustain (1214),
highlighting the need for alternative strategies and further
rationale for promotion of VAT reduction as opposed to
weight loss per se. A systematic review of the available
randomized control trials to 2006 suggested that interventions involving increased aerobic exercise can beneficially
alter VAT in overweight and obese individuals, and that
this may occur independent of weight loss (5). Recent
evidence has shown that aerobic exercise training (AEx)
programmes of lower energy expenditure than current
guidelines can induce a clinically significant reduction in
VAT, even in the absence of weight loss (15). Although
there are currently no guidelines for progressive resistance
exercise training (PRT) in the management of obesity, PRT
is known to positively affect insulin sensitivity and other
processes associated with VAT accumulation (16), and
there is evidence that despite incurring a significantly lower
energy expenditure than aerobic exercise therapy, PRT may
directly reduce VAT (5).
The aim of this study was to conduct a systematic review
with meta-analysis of randomized controlled trials to assess
the efficacy of exercise interventions on visceral adiposity in
adults. Specifically, we aimed to evaluate the effect of (i)
aerobic exercise therapy vs. control; (ii) PRT therapy vs.
control; (iii) aerobic exercise vs. PRT therapy; and (iv)
I. Ismail et al. 69
Methods
Design
Electronic database searches were performed in AMED,
MEDLINE, MEDLINE Daily Update, PREMEDLINE (via
OvidSP), SPORTDiscus, CINAHL (via EBSCO), EMBASE
and Web of Science from earliest record to November
2010. The search strategy combined terms covering the
areas of strength training, aerobic exercise training and
visceral fat (Fig. 1).
The database searches were performed using the keywords: (strength training, weight training, resistance training, progressive training, progressive resistance, weight
lifting) or (aerobic exercise, endurance exercise, aerobic
training, endurance training, cardio training, exercise,
physical endurance, physical exertion) and (visceral,
abdominal fat, abdominal adiposity, abdominal lipid,
regional adiposity, intra-abdominal, adipose tissue distribution). Reference lists of all retrieved papers were manually
searched for potentially eligible papers. Randomized controlled trials (RCTs) were reviewed while non-RCTs, uncontrolled trials and cross-sectional studies were excluded
from analysis. Manuscripts published in all languages were
included. Theses were not included in this systematic review.
Interventions
Studies were included if the exercise intervention was of 4
weeks or more. This cut-off was established to differentiate
studies examining the acute effects of exercise from those
examining training adaptations. Trials where participants
were randomized to an intervention involving either AEx
or PRT, or both, were included. Studies involving dietary
control/intervention were included only if the diet was the
same between the exercise and control groups.
Participants
Studies with adult participants greater than or equal to 18
years were considered. Studies of individuals with type 2
diabetes were included but those of HIV-infected populations were excluded because of specific medications affecting abdominal fat (5).
obesity reviews
I. Ismail et al.
Outcome measures
Selection of studies
obesity reviews
I. Ismail et al. 71
analyses were conducted using Comprehensive Metaanalysis, version 2 (Biostat Inc, Englewood, NJ).
Results
Analyses
The between-trial standardized mean difference, or effect
size (ES) and 95% confidence intervals (CIs) were calculated. Between-study variability was examined using the I2
measure of inconsistency. This statistic, expressed as a percentage between 0100, provides a measure of how much
of the variability between studies is due to heterogeneity
rather than chance. Publication bias was assessed by examining asymmetry of funnel plots (precision vs. ES) using
Eggers test. Relationships were analyzed using simple
linear regression.
Meta-analyses
Pooled estimates of the effect of exercise on VAT, using ES,
were obtained using fixed- and random-effects models. We
presumed a correlation of 0.5 between outcomes measured
within each comparison group. If we identified studies
where there were two interventions of different exercise
intensity, the intervention of higher intensity was selected.
If we identified studies where there were two interventions
of identical exercise intensity, the intervention of highest
volume (exercise duration x weekly frequency) was
selected. We performed four analyses to compare the effect
of i) AEx vs. Control; ii) PRT vs. control; iii) AEx vs. PRT;
iv) combined AEx and PRT vs. control on VAT change. All
Cohort characteristics
When combined, 2145 individuals (702 male; 1422 female;
21 not reported) participated in the trials (Table 1). Seventeen studies exclusively recruited female participants
(1733), five studies exclusively recruited male participants
(3438), with 11 studies recruiting both men and women
(9,3948). Sex was not reported in one study (49). The mean
age of participants ranged from 2883 years, and 11 studies
did not report mean age. On the basis of body mass index
(BMI) classification criteria (50), 18 studies had participants
who were classified on average as obese, 15 as overweight
and two within normal range. Fourteen studies specifically
recruited obese participants, nine studies recruited participants with type 2 diabetes, three studies with metabolic
syndrome and two studies recruited Asian-only cohorts.
Exercise characteristics
Cycle ergometry was the most common mode of AEx while
resistance training on a weight machine was most commonly used for PRT (Table 2). Within the 27 studies that
conducted AEx training, the frequency of AEx was most
commonly 3 d per week (10 of 27 studies) followed by 5 d
per week (7 of 27 studies). The frequency for PRT was
most commonly 3 d per week (9 of 13 studies), with three
studies training with PRT 2 d per week (20,21,33). Six
studies combined AEx and PRT training, three of which
conducted training on 3 d per week (18,46,48) and one
study conducted on 4 d (25), 5 d (23) and 6 d per week
(30), respectively.
Aerobic exercise intensities, expressed as a percentage
of maximal heart rate, percentage of heart rate reserve or
peak rate of oxygen consumption (VO2peak) ranged from
4055% in initial weeks progressing to 6090% in the final
weeks of the programmes. The most commonly prescribed
intensity was 6075% of maximal heart which is classified
as moderate intensity. Rating of Perceived Exertion (RPE)
and metabolic equivalents (METs) were also used to
express intensity. The intensity of PRT, quantified as a
percentage of one-repetition maximum (1-RM) in most
obesity reviews
I. Ismail et al.
Subjects
% Male
BMI
C: 45%
C: 55
C: 83.0(4.0)
C: 26.0(4.0)
PRT: 53
PRT: 83.0(3.0)
PRT: 27.0(5.0)
45.4(7.2)
29.6(4.6)
100.0
Age
PRT: 47
% Female
0.0
100
C: 58.0(4.7)
C: 32.2(4.6)
C: 53.1
C: 46.9
56.5(10.2)
C: 26.6(2.5)
A: 40
A: 60
50
50
100
18.8
81.3
A: 25.7(4.5)
71.0(4.2)
30(4.2)
C: 60.0(8.7)
C: 36.7(6.0)
A + PRT: 33.3(4.7)
A: 59.4 (5.7)
A: 32.5(4.2)
73.0(4.0)
C: 73.0(5.3)
A: 27.7(7.1)
41.9
58.1
100
100
100
100
100
50
100
Women: 24.0(5.0)
Women: 28.7(3.2)
5070
34.6(3.3)
C: 34.8(5.6)
C: 23.9(1.1)
A: 34.7(8.4)
A: 23.5(1.0)
PRT: 34.1(7.2)
PRT: 23.9(1.0)
C:54.4(5.5)
C: 34.6(3.4)
PRT: 48.6(6.4)
PRT: 35.0(3.1)
51.0(9.0)
34.0(6.0)
C: 60.6(7.1)
C: 30.6(3.8)
A + PRT: 61.0(6.9)
A: + PRT 30.5(4.3)
C: 40.1(6.7)
C: 33.7(4.1)
A: 37.5(6.0)
A: 36.0(7.1)
PRT: 34.8(5.8)
PRT: 31.6(4.3)
100
56.4 (7.1)
27.4(2.5)
100
56.6(8)
27.3(2.7)
202; Sedentary
21; NIIDM
32.0
68.0
50
C: 47.3(9.5)
31.1(2.9)
100
>75
C: 25.7(2.8)
100
C: 57.8 (8.1)
C: 27.4(2.8)
A: 55.7(7.0)
A:27.1(2.4)
PRT:55.7(6.2)
PRT: 27.1(2.3)
A + PRT: 26.0(2.4)
50.5
49.5
NR
0
100
100
postmenopausal women
100
100
45.0(9.8)
30.2(4.4)
C: 58.4(6.0)
C: 33.9(4.0)
A: 59.0(5.0)
A: 32.9(3.7)
C: 43.1(1.7)
C: 25.5(0.9)
A: 42.2(1.9)
A: 25.3(1.7)
A + PRT: 43.4(1.0)
A + PRT: 25.8(1.4)
C:28.0(4.0)
C: 22.0(2.0)
A:29.0(5.0)
A: 22.0(2.0)
PRT: 28.0(3.0)
PRT: 22.0(2.0)
C: 44.4(6.1)
C: 31.9(2.8)
A: 47.4(6.1)
A: 32.2(3.7)
PRT: 39.8(13.2)
PRT: 33.8(4.2)
obesity reviews
I. Ismail et al. 73
Table 1 Continued
Reference
Subjects
% Male
100
% Female
100
100
52
100
48
Age
C: 46.0 (10.9)
C: 30.7(1.9)
A: 45.0 (7.5)
A:32.3(1.9)
C: 43.7(6.4)
C: 32.4(2.8)
A:43.2(5.1)
A: 32.8(3.9)
C: 46.8(7.6)
C: 31.6(2.7)
A: 47.6(6.4)
A: 32.6(3.6)
PRT: 39.0(12.9)
PRT: 33.5(4.1)
C: 36.0(6.0)
C: 29.4 (0.4)
PRT: 37.0(5.0)
2187
women
Sigal et al. 2007 (46)
BMI
C: 25.7(2.4)
A:26.6 (1.8)
63.7
52
104;
49
36.3
48
51
C: 54.8(7.2)
C: 35.0(9.5)
A: 53.9(6.6)
A: 35.6(10.1)
PRT:54.7(7.5)
PRT: 34.1(9.6)
A + PRT: 53.5(7.3)
C: 52.7(6.5)
C: 29.6(3.0)
A: 51.5(5.3)
A: 29.1(2.4)
63.6(5.7)
100
C: 46.0(10.7)
C: 30.7(1.7)
A: 45.0(7.6)
A: 32.3(2.0)
All data reported as means SD. Studies reporting age and BMI as range only are reported in that format.
BMI, body mass index; A, aerobic exercise training; PRT, progressive resistance training; C, controls; NR, not reported.
Methodological quality
Assessment of the study quality is presented in Table 3. All
included studies specified their hypotheses, main outcomes,
participant characteristics, interventions, main findings,
variability estimates, statistical tests, accuracy of measures
and randomization procedure. Eight studies did not report
adverse events while five studies did not provide an
adequate description of the control group. Eighteen studies
reported the reliability of the VAT measure. Only two
studies made an attempt to blind study participants to the
intervention they received (15,49), and only two studies
made an attempt to blind those measuring the main
outcome of the intervention (15,46).
Study outcomes
All studies provided sufficient data to enable calculation
of mean differences, ES and 95% CIs (Table 4). For AEx,
Brochu et al.
2009 (17)
Boudou et al.
2003 (34)
C: n = 71
A: n = 8; bicycle ergometer
60 rpm
C: n = 8; bicycle ergometer at
C: n = 38; 9 of 22 exercises in
phase 1, primary focus on
flexibility.
Binder et al.
2005 (39)
Nutritional intervention
Mode
Reference
3/7
3/7
3/7
3/7
1/7
sessions/each phase.
3/7 for 36
23/7
Frequency
70% HRR
NR
NR
at 65% of 1 RM to progress to 3
sets of 812 at 85100% of initial
1 RM
Intensity
60 min
NR
Continuous: 45 min;
Intermittent: NR
20 min
Session duration
24 months
6 months
8 weeks
months/phase
6 months: 3
6 months
Intervention
duration
I. Ismail et al.
-1.8(2.7)
0.6 (2.8)
-5.8(4.9)
-5.1(4.7)
-1.9(19.2)
-1.7(16.1)
0.0(0.0)
0.0(0.0)
Weight
change
(kg)
obesity reviews
Giannopoulou
et al. 2005 (19)
Donnelly et al.
2003 (7)
DiPietro et al.
1998 (42)
testing period
3/7
3.6(27.2)
-5.5(27.2)
C: n = 11; Hypocaloric
monounsaturated fat diet (40%
fat (30% monounsaturated, 5%
polyunsaturated, 5% saturated),
40% CHO (15% simple, 25%
complex) and 20% protein with
600 kcal/d deficit.
A: n = 11 walking
40% fat, 40% CHO, 20%
protein
M: -5.2(15.8)
F: 0.6(17.1)
NR
M: -0.5(16.3)
F: 2.9(12.3)
C: n = 33;
4/7
4/7
-1.2(2.1)
0.0(15.0)
3/7
-2.9(4.1)
45/7
Maintain habitual
physical activity
Frequency
2.0(3.6)
-1.0(19.2)
NR
A: n = 9; mini trampoline
C: n = 9
NR
A: n = 6; cycle ergometer
NR
C: n = 6
Weight
change
(kg)
Nutritional intervention
Mode
Reference
Table 2 Continued
6570% VO2peak
A: 6075% HRR;
PRT: 2 sets of 12 reps.
A: 6075% HRR
75% of VO2peak
Caloric expenditure matched at
1,000 kcal/7
Intensity
50 min
20 min at baseline to
45 min at 6 months
60 min
75 min
75 min
NR
Session duration
14 weeks
16 months
4 months
16 weeks
12 weeks
Intervention
duration
obesity reviews
Exercise for visceral fat
I. Ismail et al. 75
Janssen et al.
1999 (43)
Ibez et al.
2010 (21)
5/7
3/7
M: -11.4(3.8)
F: -11.5(3.2)
M: -12.7(3.8)
F: -10.0(2.8)
5085% MHR
NR
30 min
15 min progressing to
maximum of 60 min.
45 min
45 min
4560 min
NR
2040 min
Session duration
16 weeks
12 months
16 weeks
16 weeks
1 year
Intervention
duration
I. Ismail et al.
NR
M: -11.7(3.5)
F: -10.7(3.8)
1/7
5/7
0.1 (NR)
-1.3 (NR)
Intensity
2/7
NR
23/7
NR
Frequency
-0.9(15.4)
-3.5(24.0)
NR
-7.1(16.7)
-5.7(20.7)
3.9(11.5)
3.1(8.8)
6.4(9.4)
(kg)
Weight
change
A: n = 9; Walk/run on indoor or
outdoor track
C: n = 7;
C: Diet only
C: n = 30
Hunter et al.
2010 (20)
Nutritional intervention
Mode
Reference
Table 2 Continued
obesity reviews
Ku et al. 2010
(26)
Johnson et al.
2009 (15)
Janssen et al.
2002 (24)
5/7
-1.1(1.3)
-1.9(1.2)
A: n = 15; walking
Maintain sedentary
lifestyle
-0.6(1.7)
4/7
NR
3/7
3/7
3/7
5/7
-0.3(8.8)
NR
C: n = 10
Intensity
4050% max
3.65.2 METs
fatigue
Frequency
0.57(8.8)
-0.2(16.2)
-0.3(19.2)
C: n = 7; stretching
-10.0(3.0)
-11.1(4.4)
-10.0(3.9)
Weight
change
(kg)
A: n = 11; dietary
Nutritional intervention
Mode
Reference
Table 2 Continued
60 min
30 min
Approx. 30 min
15 min progressing to
60 min.
Session duration
12 weeks
12 weeks
4 weeks
16 weeks
Intervention
duration
obesity reviews
Exercise for visceral fat
I. Ismail et al. 77
Nicklas et al.
2009 (53)
Mourier et al.
1997 (49)
McTiernan et al.
2007 (44)
A: n = 38; Calorie
restriction + treadmill walking
-12.3(4.9)
-11.8(4.1)
-1.5(17.3)
0.2(21.4)
C: n = 11
A: n = 10; Ergocycle
M: -1.8(21.0)
F: -1.4(24.9)
M: -0.1(25.2)
F: 0.7(18.6)
C: n = 102
NR
NR
C: n = 14
0.7(10.5)
1.1(6.4)
Weight
change
(kg)
A: n = 13; Walking
NR
NR
C: n = 15
PRT: n = 13; Bicep curls, triceps
extensions, upright rows,
Nutritional intervention
Mode
Reference
Table 2 Continued
3/7
1/7
intermittent
Pre-training 3/7
1/7
6/7
5/7
No exercise
3/7
Frequency
7075% HRR
Intermittent
85% V02peak
for 2 min 50% V02peak
for 3 min x five exercises
Pre-training
75%
Continuous: 75%V02peak
Low intensity
6085% HR max
Anaerobic threshold
4050% 1 RM
Intensity
NR
Continuous: 45 min
NR
20 min45 min
60 min
60 min
Session duration
20 weeks
2 weeks
pre-training
8 weeks
12 months
12 weeks
12 weeks
Intervention
duration
obesity reviews
Poehlman et al.
2000 (31)
-13.6(4.1)
-11.5(3.9)
-12.1(3.4)
A: n = 10; diet
intervention + treadmill walking,
stationary cycle or stair stepping
2.0(8.5)
1.0(10.6)
0.0(7.1)
C: n = 20
A: n = 14; jogging
-6.4(6.6)
-4.7(4.7)
0.6(2.3)
(kg)
Weight
change
double kick
NR
NR
C: n = 10
Nutritional intervention
Mode
Reference
Table 2 Continued
3/7
5/7
NR
3/7
NR
6/7
6/7
NR
Frequency
6070% HR max
Intensity
~30 min
50% progressing to
85%HR max
80% 1 RM
60 min
Session duration
16 weeks
6 months
24 weeks
Intervention
duration
obesity reviews
Exercise for visceral fat
I. Ismail et al. 79
Schmitz et al.
2007 (33)
A: n = 11; Diet
intervention + stationary cycle,
treadmill or stair stepping
PRT: n = 11; Diet
intervention + leg extension, leg
flexion, superpullover, chest
press and cross, shoulder press,
triceps extension and biceps curl
on Nautilus weight training
stations and Sit ups
700 kcal/d
No changes to diet
Nutritional intervention
Mode
Reference
Table 2 Continued
1.4(0.6)
3/7
-13.2(4.1)
2.0(0.7)
5/7
NR
NR
7/7
7/7
NR
Frequency
-11.6(3.7)
-11.4(3.5)
0.5(11. 0)
-5.9(15.3)
-7.5(NR)
0.1(NR)
Weight
change
(kg)
Moderate intensity
1 set of 12 reps
NR
80% of HRmax
Intensity
Year 1: 1 h
Year 2: 45 min
30 min
NR
15 min progressing to
60 min.
Session duration
2 years
16 weeks
14 weeks
12 weeks
Intervention
duration
obesity reviews
C: n = 8
7/7
80% HR max
A: 45 min
PRT: NR
Expend 23 kcal/kg/week
12 weeks
6 months
8 months
6 months
26 weeks
16 weeks
Intervention
duration
n, number of subjects; mg, milligram, kcal, kilocalorie, BMI, body mass index; A, aerobic training; PRT, progressive resistance training; C, controls; NR, not reported; HRR, heart rate reserve; HR, heart rate; RM, maximal repetition; CHO,
carbohydrates; PRO, proteins; FAT, fats; VO2peak, peak oxygen consumption.
-7.6(0.4)
NR
3/7
M: -2.2(2.7)
F: -2.3(3.4)
A: 6090% HR max
PRT: 2 sets, 1015 reps of 50%
1 RM
M: -0.63
F: -0.5(2.3)
6580% VO2peak
0.1(0.8)
NR
1545 min
20 min progressing to
40 min
Session duration
23 sets of 79 reps
6075% HR max
HR max
C: n = 53
A + PRT: n = 51; aerobic:
treadmill, stationary cycle, stair
stepper; PRT: bench press,
shoulder press, seated
mid-rowing, lat-pulldown, leg
extension, leg curl, leg press
Equivalent to jogging
20 miles/week
NR
3/7
activity levels
Revert to pre-study
Stewart et al.
2005 (48)
0.87(NR)
Intensity
Frequency
-2.3(NR)
-2.6(43.0)
Not to diet/change their diet
-0.8(43.0)
-2.6(43.3)
-0.3(39.9)
A + PRT: n = 64
C: n = 47
C: n = 63
-1.5(18.2)
0.3(17.3)
Weight
change
(kg)
C: n = 37
Nutritional intervention
Mode
Reference
Table 2 Continued
obesity reviews
Exercise for visceral fat
I. Ismail et al. 81
1. Hypothesis
stated
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Study
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
2. Main
outcomes
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
3. Participants
characteristics
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
4. Interventions
described
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
6. Main
findings
described
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
7. Variability
estimates
Y
N
N
N
N
N
N
Y
N
N
N
N
N
N
N
N
N
N
N
N
Y
N
Y
N
Y
N
Y
N
N
N
N
Y
N
Y
N
8. Adverse
events reported
Y
N
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
9. Patients
lost to
follow up
Y
Y
Y
Y
N
N
N
Y
N
N
N
Y
Y
N
N
Y
Y
Y
Y
Y
Y
N
Y
N
N
N
N
N
N
N
N
Y
Y
N
N
10. Actual
P value
reported
obesity reviews
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
N
Y
N
N
N
N
N
Y
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
Y
Y
N
N
N
N
N
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
14. Participants
blinded
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
18. Statistical
tests
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
20. Accurate
measures
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
U
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
21. Same
population
recruited
U
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
U
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
U
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
24. Randomized
to groups
Y
Y
Y
Y
Y
N
Y
Y
Y
N
Y
Y
Y
Y
Y
Y
N
Y
Y
Y
Y
Y
Y
N
N
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
25. Adequate
description of
control
Y
Y
Y
N
Y
N
N
N
Y
Y
Y
Y
N
N
Y
Y
N
N
N
N
Y
Y
Y
N
Y
N
N
N
Y
N
N
N
Y
Y
N
26. Reliability
of VAT measure
reported
11. Representative
participants
Study
Table 3 Continued
obesity reviews
I. Ismail et al. 83
obesity reviews
I. Ismail et al.
Mode
Measure
Region
Change Score
Binder et al.
2005 (39)
C (n = 38)
MRI
(20 C,
34 PRT)
NR
-3.8(29.0)
NR
-7.0(43.0)
MRI
Umbilicus (L4-L5)
NR
PRT (n = 53)
Boudou et al.
C: n = 8
2003 (34)
A: n = 8
Brochu et al.
2009
PRT: n = 36
C: n = 71
C: n = 32
CT
CT
C: n = 6
A: n = 6
A + PRT: n = 10
C: n = 9
CT
CT
Donnelly et al.
2003 (7)
C: n = 33
A: n = 41
CT
Giannopoulou
et al. 2005 (19)
C: n = 11
MRI
CT
A: n = 11
CT
A: n = 18
PRT: n = 21
Ibez et al.
2010 (21)
C: n = 12
MRI
PRT n = 13
C: n = 7
CT
A: n = 9
C: n = 86
NR
NR
cm2
-23.0(30.0) cm2
-23.0(34.0) cm2
112.7(58.8)
cm2
87.2(40.0) cm2
75.0(43.3) cm2
NR
NR
-1.6(39.0) cm2
-10.6(19.2) cm2
C: 5(14.7)
-0.4(36.0) cm2
NR
A: n = 9
C: n = 30
DiPietro et al.
1998 (42)
Hunter et al.
2010 (20)
84.20(21.30) cm2
A: -39.0(26.9)cm2
A: n = 9
C: n = 7
150.35(23.25) cm2
112.3(56.0)
A: n = 30
CT
136.0(74.1)cm2
118.0(71.4)cm2
116.0(93.0)cm2
106.0(72.0)cm2
85.4(39.7)
66.0(13.9)
75.5(18.3)
57.4(28.4)
4785.0(1,592.0) cm3
4425.0(1,442.7) cm3
NR
cm3
5152.0(1,456.0) cm3
-12.8%
50.0(20.8) cm2
62.4(28.2) cm2
12.4 cm2,
48.0(17.7) cm2
48.8(20.1) cm2
0.8 cm2,
43.7(14.4) cm2
43.3(15.5) cm2
5912.0(1,605.2)
NR
cm2
cm2
cm2
cm2
NR
3340.0(977.0) cm
2724.0(1,052.0) cm
157.0(71.0) cm2
155.0(71.0) cm2
cm2
cm2
173.0(73.0)
147.6(57.7) g/cm2
148.0(59.0)
NR
147.6(63.5) g/cm2
A + PRT: n = 87
NR
-2.0 cm2
-24.0 cm2
0.1(31.5) g/cm2
-8.5(40.7) g/cm2
cm2
cm2
cm2
cm2
cm2
cm2
Janssen et al.
1999 (43)
C: n = 20
A: n = 20
PRT: n = 20
MRI
Male: 188.0(69.6)
Female: 142.0(53.8)
Male: 159.0(37.9)
Female: 128.0(31.6)
Male: 149.0(123.3)
Female: 89.0(28.5)
NR
-58.0(31.6)
-51.0(22.1)
-67.0(37.9)
-37.0(22.1)
-50.0(47.4)
-15.0(19.0)
Janssen et al.
2002 (24)
C: n = 13
A: n = 11
PRT: n = 14
MRI
2.3(1.1)kg,
131.0(50.0)cm2
1.9(0.9)kg,
120.0(42.0)cm2
1.50(0.59)kg,
84.0(27.0)cm2
NR
-0.65(0.37) kg,
-51(21) cm2
-0.6(0.4) kg
-39.0(24.0) cm2
-0.4(0.2) kg
-19.0(16.0) cm2
C: n = 7
MRI
154.3(56.1) cm2
158.6(63.2) cm2
NR
164.3(63.4) cm2
143.6(64.8) cm2
Johnson et al.
2009 (15)
A: n = 12
A + PRT: n = 10
Ku et al. 2010
(26)
A: n = 15
C: n = 10
C: n = 16
CT
CT
Abdominal
PRT: n = 13
Kwon et al. 2010
(27)
C: n = 15
C: n = 14
CT
PRT: n = 13
A: n = 13
CT
391.9(206.7)
408.4(189.7)
16.5
387.7(111.3)
356.9(93.0)
-30.80
17 530.0(4,747.0)g
17 362.0(4,728.0)g
-168.0(1,801.0)g
15 890.0(4,593.0)g
15 038.0(3,369.0)g
-852.0(2,839.0)g
15 658.0(4,754.0)g
14 678.0(3,456.0)g
-980.0(2,353.0)g
17 268.7(5,060.9)mm2
17 745.1(4,715.0)mm2
4.4%
15 657.8(4,753.6)mm2
14 677.8(3,455.9)mm2
NR
17 204.5(4,674.4)mm2
17 216.3(4,560.8)mm2
0.9%
16 291.5(4,808.5)mm2
14 682.7(3,494.7)mm2
8.4%
obesity reviews
I. Ismail et al. 85
Table 4 Continued
Reference
Mode
Measure
Region
Change Score
McTiernan et al.
2007 (44)
C: n = 102
A: n = 100
CT
L4-L5 space
170.5(72.2) cm2
-6.2(-3.5)%
1.6(1.6)%
100.1(58.8) cm2
-12.2(7.5)%
-5.8(-5.5)%
NR
Mourier et al.
1997 (49)
Nicklas et el.
2009 (29)
C: n = 11
MRI
A: n = 10
C: n = 34
CT
Poehlman et al.
2000 (31)
2369.0(870.0) cm3
NR
-612.0(338.0)
cm3
-630.0(298.0)
cm3
182.9(16.8) cm3
190.4(15.7) cm3
7.5 cm3
112.4(10.5) cm3
-82.6 cm3
A + PRT: n = 10
201.6(28.0) cm3
108.6(17.9) cm3
-93.0 cm3
C: n = 20
CT
CT
L4 close to umbilicus
36.0(13.0)
cm2
41.0(15.0)
cm2
A: n = 14
40.0(11.0) cm2
41.0(13.0) cm2
PRT: n = 17
36.0(17.0) cm2
36.0(13.0) cm2
4.6(1.6)L
NR
C: n = 9
MRI
A: n = 10
C: n = 8
A: n = 16
A: n = 17
C: n = 10
C: n = 11
MRI
MRI
MRI
A: n = 11
PRT: n = 11
Schmitz et al.
2007 (33)
C: n = 63
C: n = 37
80.4(22.1) cm2
195.0(12.6) cm3
C: n = 10
PRT: n = 10
134.9(33.8) cm2
A: n = 10
139.4(36.8) cm2
156.1(47.4) cm2
2509.0(737.0) cm3
A: n = 38
104.2(59.6) cm2
149.6(76.6) cm2
CT
4.1(2.4)L
Whole body
198.0(71.0) cm2
198.0 cm2
186.0(59.0) cm2
134.0 cm2
-1.8(1.0)L
4.6(1.5)L
-1.5(0.7)L
2.3(0.9)kg
2.2(0.9)kg
NR
1.6(0.7)kg
-0.7(0.5)
4.7(1.6)L
NR
-1.5(0.8)L
-1.8(1.0)L
-1.4(0.7)
3.9(2.3)L
L2-L3 interspace
67.4 (36.5) cm
A: n = 65
81.8
cm2
76.9 cm2
7.05 (5.1) %
122.0(79.1) cm2
121.0(73.0) cm2
NR
133.0(88.7) cm2
124.0(88.7) cm2
250.0(147.0) cm2
244.0(161.0) cm2
PRT: n = 64
228.0(156.0) cm2
218.0(156.0) cm2
A + PRT: n = 64
246.0(159.0) cm2
CT
C: n = 47
CT
L4 pedicle
A: n = 42
Stewart et al.
C: n = 53
2005 (48)
A + PRT: n = 51
C: n = 8
MRI
MRI
Whole body
A: n = 16
21.36 (5.3) %
71.8(36.8) cm2
257.0(161.0) cm2
C: n = 63
A: n = 60
NR
2.3(0.8)kg
4.6(1.4)L
PRT: n = 70
CT
-1.5(0.9)L
Whole body
NR
NR
165.0(68.0)
179.2
8.6(17.2)%
168.0(64.0)
156.4
-6.9(20.8)%
NR
4.1(1.7)kg
NR
3.9(0.8)kg
-0.003(0.3)
-1.1(0.4)
Aerobic exercise
There was a significant pooled ES for the comparison
between aerobic exercise therapy and control (ES = -0.23,
95% CI: -0.35 to -0.12; P < 0.001). Significant heterogeneity among studies was observed (I2 = 71.0%, P < 0.001).
I. Ismail et al.
obesity reviews
Figure 2 Forest plot for AEx studies (n = 29). Graph depicts ES and 95% CI for individual studies and the pooled estimate.
obesity reviews
I. Ismail et al. 87
Figure 3 Forest plot for PRT studies (n = 14). Graph depicts ES and 95% CI for individual studies and the pooled estimate.
I. Ismail et al.
obesity reviews
Figure 4 Forest plot for PRT vs. AEx studies (n = 9). Graph depicts ES and 95% CI for individual studies and the pooled estimate.
Figure 5 Forest plot for combined AEx and PRT studies (n = 6). Graph depicts ES and 95% CI for individual studies and the pooled estimate.
obesity reviews
Discussion
This is the first systematic review with meta-analyses to
investigate the independent and combined effects of aerobic
and resistance training modalities on visceral adiposity in
adults. The data show that when compared with a control
intervention, AEx therapy is effective in lowering VAT.
Resistance training itself failed to induce significant reduction in VAT when compared with the control group. In
studies where AEx and PRT were directly compared, the
effect size favoured AEx training but did not reach statistical significance. From available studies in which combined interventions using both AEx and PRT were
employed, the pooled effect size was not significantly different from a control group.
This systematic review and meta-analyses combined 35
studies involving a total of 2145 adult participants. Of the
studies examined, the majority were conducted in overweight or obese populations, predominantly with female
cohorts. Twelve of the studies specifically included participants with type 2 diabetes or metabolic syndrome. Aerobic
training interventions ranged from four to 52 weeks in
duration and prescribed exercise on one to 7 d per week at
intensities between 49% and 85% of peak aerobic capacity.
Such interventions are consistent with current public health
recommendations for improving cardiorespiratory fitness
(51), but the majority of studies fell below the recommended exercise guidelines for the prevention and management of overweight and obesity (52). Progressive resistance
training interventions ranged from 12 to 104 weeks in
duration and employed resistance exercise on two to 5 d
per week at intensities between 30% and 100% of one
repetition maximum (27,39). Most studies employed PRT
interventions, which were consistent with the minimum
frequency and volume of currently recommended for
improving muscular fitness in adults (51).
Excess visceral adipose tissue is a well-established risk
factor for cardiovascular disease (53), and small differences in VAT area/volume can significantly alter risk
profile (54). The present data demonstrate that AEx itself
is effective in favourably modifying VAT, but that interventions involving PRT do not significantly influence VAT.
It has been suggested that a doseresponse relationship
exists between exercise volume and VAT reduction, which
has been attributed to a greater amount of energy expenditure leading to greater weight loss. However, on the
basis of the present data, although there was a significant
relationship between mean weight loss and VAT reduction
(r2 = 0.17, P < 0.05) as expected, we found no evidence to
suggest a relationship between total weekly AEx volume
or mean intensity and VAT reduction (r2 < 0.15 for both),
and there are a number of examples of RCTs in which
VAT reduction occurred in the absence of significant
weight loss (15,32,47). Other studies have found that,
I. Ismail et al. 89
90
obesity reviews
References
1. Rheaume C, Arsenault BJ, Belanger S, Perusse L, Tremblay A,
Bouchard C et al. Low cardiorespiratory fitness levels and elevated
blood pressure. What is the contribution of visceral adiposity?
Hypertension 2009; 54: 9197.
2. Nakamura T, Tokunaga K, Shimomura I, Nishida M, Yoshida
S, Kotani K et al. Contribution of visceral fat accumulation to the
development of coronary artery disease in non-obese men. Atherosclerosis 1994; 107: 239246.
3. Tulloch-Reid MK, Hanson RL, Sebring NG, Reynolds JC,
Premkumar A, Genovese DJ et al. Both subcutaneous and visceral
adipose tissue correlate highly with insulin resistance in African
Americans. Obes Res 2004; 12: 13521359.
4. Fujioka S, Matsuzawa Y, Tokunaga K, Tarui S. Contribution
of intra-abdominal fat accumulation to the impairment of glucose
and lipid metabolism in human obesity. Metabolism 1987; 36:
5459.
5. Kay SJ, Fiatarone Singh MA. The influence of physical activity
on abdominal fat: a systematic review of the literature. Obes Rev
2006; 7: 183200.
6. Ross R, Rissanen J. Mobilization of visceral and subcutaneous
adipose tissue in response to energy restriction and exercise. Am J
Clin Nutr 1994; 60: 695703.
7. Donnelly JE, Hill JO, Jacobsen DJ, Potteiger J, Sullivan DK,
Johnson SL et al. Effects of a 16-month randomized controlled
exercise trial on body weight and composition in young, overweight men and women: the Midwest Exercise Trial. Arch Intern
Med 2003; 163: 13431350.
8. Haskell WLPF, Lee IMMDS, Pate RRPF, Powell KEMDMPH,
Blair SNPEDFF, Franklin BAPF et al. Physical activity and public
health: updated recommendation for adults from the American
College of Sports Medicine and the American Heart Association.
Circulation 2007; 116: 10811093.
9. Donelly J, Blair S, Jakicic J, Manore M, Rankin J, Smith B.
Appropriate physical activity intervention strategies for weight loss
and prevention of weight regain for adults. Med Sci Sports Exerc
2009; 41: 459471.
10. Diabetes Prevention Program Research Group. Reduction in
the incidence of type 2 diabetes with lifestyle intervention or metformin. New Engl J Med 2002; 346: 393403.
11. Franz MJVJ, Crain AL, Boucher JL, Histon T, Caplan W,
Bowman JD et al. Weight-loss outcomes: a systematic review and
meta-analysis of weight-loss clinical trials with a minimum 1-year
follow-up. J Am Diet Assoc 2007; 107: 17551767.
12. Shaw K, Gennat H, ORourke P, Del Mar C. Exercise for
overweight or obesity (review). Cochrane 2007; (4). DOI:10.1002/
14651858.CD003817.pub3: 185.
13. Hansen D, Dendale P, Berger J, van Loon LJC, Meeusen R.
The effects of exercise trainining on fat-mass loss in obese patients
during energy intake restriction. Sports Med 2007; 37: 3146.
14. Franz MJ, VanWormer JJ, Crain AL, Boucher JL, Histon T,
Caplan W et al. Weight-loss outcomes: a systematic review and
meta-analysis of weight-loss clinical trials with a minimum 1-year
follow-up. J Am Diet Assoc 2007; 107: 17551767.
15. Johnson NA, Sachinwalla T, Walton DW, Smith K, Armstrong A, Thompson MW et al. Aerobic exercise training reduces
hepatic and visceral lipids in obese individuals without weight loss.
Hepatology 2009; 50: 11051112.
16. Albright AFM, Hornsby G, Kriska A, Marrero D, Ulrich I,
Verity L. Exercise and type 2 diabetes. Med Sci Sports Exerc 2000;
32: 13451360.
17. Brochu M, Malita MF, Messier V, Doucet E, Strychar I,
Lavoie JM et al. Resistance training does not contribute to improving the metabolic profile after a 6-month weight loss program in
overweight and obese postmenopausal women. J Clin Endocrinol
Metab 2009; 94: 32263233.
18. Cuff DJ, Meneilly GS, Martin A, Ignaszewski A, Tidesley HD,
Frohlich JJ. Effective exercise modality to reduce insulin resistance
in women with type 2 diabetes. Diabetes Care 2003; 26: 2977
2982.
19. Giannopoulou I, Ploutz-Synder LL, Carhart R, Weinstock RS,
Fernhall B, Goulopoulou S et al. Exercise is required for visceral
fat loss in postmenopausal women with type 2 diabetes. J Clin
Endocrinol Metab 2005; 90: 15111518.
20. Hunter GR, Brock DW, Byrne NM, Chandler-Laney PC, Del
Corral P, Gower BA. Exercise training prevents regain of visceral
fat for 1 year following weight loss. Obesity 2010; 18: 690
695.
21. Ibez J, Izquierdo M, Martnez-Labari C, Ortega F, Grijalba
A, Forga L et al. Resistance training improves cardiovascular risk
factors in obese women despite a significative decrease in serum
adiponectin levels. Obesity 2010; 18: 535541.
22. Irving BA, Davis CK, Brock DW, Weltman JY, Swift D,
Barrett EJ et al. Effect of exercise training intensity on abdominal
visceral fat and body composition. Med Sci Sports Exerc 2008; 40:
18631872.
23. Irwin ML, Yasui Y, Ulrich CM, Bowen D, Rudolph RE,
Schwartz RS et al. Effect of exercise on total and intra-abdominal
body fat in postmenopausal women a randomized controlled
trial. J Am Med Assoc 2003; 289: 323330.
24. Janssen I, Fortier A, Hudson R, Ross R. Effects of an energyrestrictive diet with or without exercise on abdominal fat, intermuscular fat, and metabolic risk factors in obese women. Diabetes
Care 2002; 25: 431438.
25. Kim E, Park S, Kwon Y. The effects of combined exercise on
functional fitness and risk factors of metabolic syndrome in the
older women. Jpn J Phys Fitness Sports Med 2008; 57: 207215.
26. Ku YH, Han KA, Ahn H, Kwon H, Koo B-K, Kim HC et al.
Resistance exercise did not alter intramuscular adipose tissue but
reduced retinol-binding protein-4 concentration in individuals
with type 2 diabetes mellitus. J Int Med Res 2010; 38: 782791.
27. Kwon HR, Han KA, Ku YH, Ahn HJ, Koo B-K Kim KHC
et al. The effects of resistance training on muscle and body fat mass
and muscle strength in type 2 diabetic women. Korean Diabetes J
2010; 34: 101110.
28. Kwon HR, Min KW, Ahn HJ, Seok HG, Koo B-K, Kim HC
et al. Effects of aerobic exercise on abdominal fat, thigh muscle
mass and muscle strength in type 2 diabetic subject. Korean Diabetes J 2010; 34: 2331.
29. Nicklas BJ, Wang X, You T, Lyles MF, Demons J, Easter L
et al. Effect of exercise intensity on abdominal fat loss during
calorie restriction in overweight and obese postmenopausal
women: a randomized, controlled trial. Am J Clin Nutr 2009; 89:
10431052.
obesity reviews
30. Park SK, Park JH, Kwon YC, Kim HS, Yoon MS, Park HT.
The effect of combined aerobic and resistance exercise training on
abdominal fat in obese middle-aged women. J Physiol Anthropol
Appl Human Sci 2003; 22: 129135.
31. Poehlman ET, Dvorak RV, DeNino WF, Brochu M, Ades PA.
Effects of resistance training and endurance training on insulin
sensitivity in nonobese, young women: a controlled randomized
trial. J Clin Endocrinol Metab 2000; 85: 24632468.
32. Ross R, Janssen I, Dawson J, Kungl A-M, Kuk JL, Wong SL
et al. Exercise-induced reduction in obesity and insulin resistance
in women: a randomized controlled trial. Obes Res 2004; 12:
789798.
33. Schmitz KH, Hannan PJ, Stovitz SD, Bryan CJ, Warren M,
Jensen MD. Strength training and adiposity in premenopausal
women: strong, healthy, and empowered study. Am J Clin Nutr
2007; 86: 566572.
34. Boudou P, Sobngwi E, Mauvais-Jarvis F, Vexiau P, Gautier JF.
Absence of exercise-induced variations in adiponectin levels despite
decreased abdominal adiposity and improved insulin sensitivity in
type 2 diabetic men. Eur J Endocrinol 2003; 149: 421424.
35. Rice B, Janssen I, Hudson R, Ross R. Effects of aerobic or
resistance exercise and/or diet on glucose tolerance and plasma
insulin levels in obese men. Diabetes Care 1999; 22: 684691.
36. Ross R, Dagnone D, Jones PJH, Smith H, Paddags A, Hudson
R et al. Reduction in obesity and related comorbid conditions after
diet-induced weight loss or exercise-induced weight loss in men: a
randomized, controlled trial. Ann Intern Med 2000; 133: 92103.
37. Ross R, Rissanen J, Pedwell H, Clifford J, Shragge P. Influence
of diet and exercise on skeletal muscle and visceral adipose tissue
in men (Influence de lalimentation et de lexercice sur les muscles
du squelette et les tissus adipeux visceraux chez lhomme). J Appl
Physiol 1996; 81: 24452455.
38. Thong FSL, Hudson R, Ross R, Janssen I, Graham TE. Plasma
leptin in moderately obese men: independent effects of weight loss
and aerobic exercise. Am J Physiol Endocrinol Metab 2000; 279:
E307E313.
39. Binder EF, Yarasheski KE, Steger-May K, Sinacore DR, Brown
M, Schechtman KB et al. Effects of progressive resistance training
on body composition in frail older adults: results of a randomized,
controlled trial. J Gerontol A Biol Sci Med Sci 2005; 60: 1425
1431.
40. Carr DB, Utzschneider KM, Boyko EJ, Asberry PJ, Hull RL,
Kodama K et al. A reduced-fat diet and aerobic exercise in Japanese Americans with impaired glucose tolerance decreases intraabdominal fat and improves insulin sensitivity but not beta-cell
function. Diabetes 2005; 54: 340347.
41. Coker RH, Williams RH, Kortebein PM, Sullivan DH,
Evans WJ. Influence of exercise intensity on abdominal fat and
adiponectin in elderly adults. Metab Syndr Relat Disord 2009; 7:
363368.
42. DiPietro L, Seeman TE, Stachenfeld NS, Katz LD, Nadel ER.
Moderate-intensity aerobic training improves glucose tolerance in
aging independent of abdominal adiposity. J Am Geriatr Soc 1998;
46: 875879.
43. Janssen I, Ross R. Effects of sex on the change in visceral,
subcutaneous adipose tissue and skeletal muscle in response to
weight loss. Int J Obes 1999; 23: 10351046.
44. McTiernan A, Sorensen B, Irwin ML, Morgan A, Yusui Y,
Rudolph RE et al. Exercise effect on weight and body fat in men
and women. Obesity 2007; 15: 14961512.
45. Short KR, Vittone JL, Bigelow ML, Proctor DN, Rizza RA,
Coenen-Schimke JM et al. Impact of aerobic exercise training on
I. Ismail et al. 91