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obesity reviews

doi: 10.1111/j.1467-789X.2011.00931.x

Obesity Treatment/Management

A systematic review and meta-analysis of the effect of


aerobic vs. resistance exercise training on visceral fat

obr_

931

68..9168..91

I. Ismail1, S. E. Keating1, M. K. Baker2,3 and N. A. Johnson1,3

Discipline of Exercise and Sport Science,

University of Sydney, Sydney, New South


Wales, Australia; 2School of Exercise and
Health Sciences, Edith Cowan University,
Joondalup, Western Australia, Australia;
3

Boden Institute of Obesity, Nutrition and

Exercise, University of Sydney, Sydney,


New South Wales, Australia

Received 19 June 2011; revised 25 July 2011;


accepted 26 July 2011

Address for correspondence: Dr N Johnson,


Discipline of Exercise and Sport Science,
Faculty of Health Sciences, The University of
Sydney, C42 Cumberland Campus,
Lidcombe, NSW 2141, Australia. E-mail:
nathan.johnson@sydney.edu.au

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

Financial support: none.

68

2011 The Authors


obesity reviews 2011 International Association for the Study of Obesity 13, 6891

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)

Exercise for visceral fat

I. Ismail et al. 69

combined aerobic and PRT therapy vs. control on VAT


change. We hypothesized that, when compared with a
control condition, both aerobic and PRT therapies would
significantly reduce VAT. Secondly, we hypothesized that
aerobic exercise would have a greater effect than PRT
therapy on VAT. We further hypothesized that combined
aerobic exercise and PRT therapy would have a greater
effect on VAT than either therapy in isolation.

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).

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70 Exercise for visceral fat

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I. Ismail et al.

Figure 1 Flowchart of outcomes of search


strategy.

Outcome measures

Selection of studies

Studies were selected if the effect of exercise alone on visceral


fat was presented, and if computed tomography (CT) or
magnetic resonance imaging (MRI) was used for quantification of visceral fat area/volume. Studies providing
outcome measures of visceral fatness/trunk adiposity using
any other method such as ultrasound or dual energy X-ray
absorptiometry (DXA) were excluded.

After eliminating duplications, the search results were


screened by one investigator (II) against the eligibility criteria, and those references which could not be eliminated
by title or abstract were retrieved and independently
reviewed by two reviewers (II, NJ) in an unblinded manner.
Disagreements were resolved by discussion or by a third
researcher (MB). In cases where journal articles contained

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Exercise for visceral fat

I. Ismail et al. 71

insufficient information, attempts were made to contact


authors to obtain missing details.

analyses were conducted using Comprehensive Metaanalysis, version 2 (Biostat Inc, Englewood, NJ).

Data extraction and calculations

Results

Data relating to participant characteristics (age, sex, body


mass index {BMI]} ), exercise details (mode of exercise,
nutritional intervention, exercise frequency, intensity, duration and intervention duration) and visceral fat quantification (measurement technique and region) were extracted
independently by two researchers (II, SK), with disagreements resolved by discussion or by a third researcher (NJ).
For one study which presented data graphically, mean and
standard deviation were estimated in duplicate manually.
One author was contacted and provided standard deviation
data that were missing from the study.

Assessment of methodological quality


Included studies met a minimum quality threshold, defined
as having met all inclusion criteria. Study quality was
further assessed by two researchers (II, SK) in a blinded
manner using a modified assessment scale created by
Downs & Black (17). The scale was modified to include
criteria for adequate description of control and whether
CT/MRI reliability for VAT quantification was reported.

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

Identification and selection of studies


The original search netted 12 196 studies. Three more
studies were found from the reference lists of the manuscripts retrieved. After removal of duplicates and elimination of papers based on the eligibility criteria, 35 studies
remained (Fig. 1).

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

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72 Exercise for visceral fat

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Table 1 Participant characteristics


Reference

Subjects

Binder et al. 2005 (39)

91; Older sedentary with physical frailty

% 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)

Boudou et al. 2003 (34)

16; Men with type 2 diabetes

100.0

107; Postmenopausal women

Carr et al. 2005 (40)

62; Japanese-Americans with impaired


glucose tolerance

Coker et al. 2009 (41)

18; Overweight elderly

Cuff et al. 2003 (18)

28; Postmenopausal with type-2


diabetes

16; Healthy older

Age

PRT: 47

Brochu et al. 2009 (17)

DiPietro et al. 1998 (42)

% 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: 63.4 (7.0)

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)

Donnelly et al. 2003 (7)

74; Sedentary overweight and


moderately obese

41.9

58.1

Giannopoulou et al. 2005


(19)

22; Obese post menopausal women


with type 2 diabetes

100

Hunter et al. 2010 (20)

69; Healthy premenopausal women

100

Ibanez et al. 2010 (21)

25; Obese women

100

Irving et al. 2008 (22)

16; Obese women with metabolic


syndrome

100

Irwin et al. 2003 (23)

173; Overweight postmenopausal


women

100

Janssen et al. 1999 (43)

Janssen et al. 2002 (24)

60; Upper body obese

38; Premenopausal obese women

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)

Male: C: 45.6 (6.6); A: 47.4 (6.6); PRT:


37.9 (13.3)

Male: C: 31.6(2.8); A: 33.0(3.5); PRT:


33.6(4.4)

Female: C: 39.6(7.6); A: 39.0(6.3); PRT:


37.3(4.4)

Female: C: 34.5(4.4); A: 35.5 (6.6);


PRT: 32.5 (4.7)

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)

19; Obese sedentary

Kim et al. 2008 (25)

20; Women of advanced age with


metabolic syndrome

Ku et al. 2010 (26)

44; Overweight Korean women with


type 2 diabetes

Kwon et al. 2010 (27)

28; Overweight type 2 diabetics

100

56.4 (7.1)

27.4(2.5)

Kwon et al. 2010 (28)

27;Obese type 2 diabetics

100

56.6(8)

27.3(2.7)

McTiernan et al. 2007 (44)

202; Sedentary

21; NIIDM

Nicklas et al. 2009 (29)

72; Overweight and obese

Park et al. 2003 (30)

30; Middle-aged obese women

32.0

C: Men: 29.0(3.0), Women: 29.3(2.3)


A: Men29.7(2.9),

Johnson et al. 2009 (14)

Mourier et al. 1997 (49)

68.0

50

C: Men: 24.0(4.0), Women: 21.0(4.0)


A: Men: 22.0(4.0),

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

Poehlman et al. 2000 (31)

Rice et al. 1999 (35)

51; Non-obese younger women

29; Obese men

100

100

C: Men: 56.6(7.6), Women: 53.7(5.6)

C: Men: 30.1(4.8), Women: 28.5(4.8)

A: Men: 56.2(6.7), Women: 54(7.1)

A: Men: 29.7(3.7), Women: 28.9(5.5)

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)

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Exercise for visceral fat

I. Ismail et al. 73

Table 1 Continued
Reference

Subjects

% Male

Ross et al. 2000 (36)

24; Obese men

100

Ross et al. 2004 (32)

Ross et al. 1996 (37)

Schmitz et al. 2007 (33)

Short et al. 2003 (45)

27; Premenopausal women with


abdominal obesity
33; Obese men

133; Overweight or obese

102; Healthy sedentary men and

% 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)

PRT: 29.4 (0.4)

2187

women
Sigal et al. 2007 (46)

Slentz et al. 2005 (47)

Stewart et al. 2005 (48)

251; Type 2 diabetes

BMI

C: 25.7(2.4)
A:26.6 (1.8)

63.7

89; Sedentary overweight with mild to


moderate dyslipidemia

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)

A + PRT: 35.0 (9.6)

C: 52.7(6.5)

C: 29.6(3.0)

A: 51.5(5.3)

A: 29.1(2.4)

63.6(5.7)

C: Male: 29.7(3.8), Female: 29.6(6.1)


A + PRT: Male: 29.7(3.0),

Thong et al. 2000 (38)

24; Obese men

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.

studies (17,20,21,25,27,30,31,39,48) ranged between


30100% 1 RM. Two studies (24,43) prescribed one set of
812 repetitions until volitional fatigue.
Ten studies stated that diet was not controlled, nine
studies required participants to recall/record diet and
analysis was reported, and eight studies required the participants to follow a prescribed diet. Eight studies did not
report on dietary intervention or control.

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,

26 of the 29 studies showed an ES favouring aerobic


exercise therapy, ranging from 0.07 to -6.09. Five of
these studies showed a statistically significant effect
for aerobic exercise. None of the four studies with an
ES favouring the control intervention (ES range: 0.10
0.61) reached statistical significance. For PRT, seven
of the 14 studies showed an ES favouring resistance
exercise training, ranging from -0.04 to -0.58, with only
one of these studies showing a statistically significant
effect for resistance exercise. Five studies favoured the
control intervention vs. resistance exercise (ES range:
0.131.67), with two of these reaching statistical significance. Of the nine studies comparing AEx with PRT,
seven favoured aerobic exercise vs. resistance training,
ranging from 0.02 to 1.02, two of which were statistically
significant. None of the two studies which reported an
ES favouring resistance training vs. aerobic exercise
reached statistical significance. Six of the seven studies
which combined AEx with PRT, reported an ES favouring
the intervention group, half of these reached statistical
significance (range: -0.13 to -4.62). One study showed a
statistically significant ES for control vs. combined AEx
plus PRT.
A linear regression analysis was performed to assess the
relationship between VAT reduction and change in weight
in all of the exercise groups (AEx, PRT and AEx + PRT). A
significant relationship between VAT reduction and weight
loss was found (r = 0.42, P = 0.014).

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Carr et al. 2005


(40)

Brochu et al.
2009 (17)

Boudou et al.
2003 (34)

Isocaloric with 30% fat (<7%


saturated), 50% CHO, 20%
protein with <300 mg
cholesterol/d
Isocaloric with 30% fat (10%
saturated), 55% CHO, 15%
protein with <200 mg
cholesterol/d

A: n = 32; walking or jogging on a


treadmill

55% CHO; 30% fat; 15%


protein

C: n = 32: Stretching exercises

PRT: n = 36; leg press, chest


press, lat pull down, shoulder
press, arm curls, triceps
extensions

C: n = 71

A: n = 8; bicycle ergometer

60 rpm

C: n = 8; bicycle ergometer at

machine. + shortened version of


phase 1.

balance coordination, speed of


reaction. Phase 2: PRT, knee
extension, flexion, seated bench
press, seated row, leg press,
biceps curl on weightlifting

Maintain usual diet (~50%


CHO, 30% lipids, 20%
proteins).

Supplemental calcium and


vitamin D

C: n = 38; 9 of 22 exercises in
phase 1, primary focus on
flexibility.

Binder et al.
2005 (39)

PRT: n = 53; Phase 1: flexibility,

Nutritional intervention

Mode

Reference

Table 2 Exercise details

3/7

3/7

3/7

3/7

1/7

sessions/each phase.

3/7 for 36

23/7

Frequency

70% HRR

NR

Four progressive phases:


1 (3 weeks): 15 reps/65% 1 RM,
23 sets per exercise, 90120 s
rest b/w sets
2 (5 weeks): 12 reps/70% 1 RM,
23 sets per exercise, 90 s rest
b/w sets3 (9 weeks):
10 reps/7580% 1 RM, 24 sets
per exercise, 120180 s rest b/w
sets
4 (8 weeks): 1012 reps/7075%
1 RM, 24 sets per exercise
6090 s rest b/w sets.

NR

Continuous 75% VO2peak 2/7 and


intermittent exercise at 85%:50%
for 2 min:3 min, respectively, 1/7

Low intensity (30 W)

at 65% of 1 RM to progress to 3
sets of 812 at 85100% of initial
1 RM

Phase 2: PRT, 12 sets of 68 reps

Intensity

60 min

NR

Continuous: 45 min;
Intermittent: NR

20 min

Phase 2: 6090 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)

74 Exercise for visceral fat

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Giannopoulou
et al. 2005 (19)

Donnelly et al.
2003 (7)

DiPietro et al.
1998 (42)

testing period

Refrain from any type


of regular physical
activity during study

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

A: n = 41; Treadmill, stationary


bike or elliptical trainer

M: -0.5(16.3)
F: 2.9(12.3)

Maintain usual dietary intake

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

Continue with current


physical activity
patterns
3/7

2.0(3.6)

-1.0(19.2)

NR

Continue with current diet


patterns

A: n = 9; mini trampoline

C: n = 7; stretching, yoga, stretch


bands

A + PRT n = 10 Aerobic exercise


on treadmills, stationary bicycles,
recumbent steppers, ellipitical
trainers and rowing machines.
Resistance training on leg press,
leg curl, hip extension, chest
press, latissimus pulldown
A: n = 9 as above exercise with
low impact low intensity dynamic
movement

C: n = 9

NR

controlled feeding prior to


baseline and post intervention

A: n = 6; cycle ergometer

Cuff et al. 2003


(18)

NR

Mixed diet (35% fat, 20%


protein, 45% CHO) during 4 d

C: n = 6

Coker et al. 2009


(41)

Weight
change
(kg)

Nutritional intervention

Mode

Reference

Table 2 Continued

6570% VO2peak

60% HRR at baseline to 75% at 6


months

Maintain usual physical activity

5560% HR max for 1 month; 75%


HR max for 3 months

HR did not exceed 90 bpm

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

2040 min 1st month


progressing to 60 min for
3 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)

Irwin et al. 2003


(23)

Irving et al. 2008


(22)

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)

1 set of 812 reps to volitional


fatigue

5085% MHR

A: 40% HR max progressing to


6075% HR max by week 8
PRT: 2 sets of 10 reps

NR

RPE 1517 on 3/7 and 1012 on


2/7

30 min

15 min progressing to
maximum of 60 min.

45 min

45 min

Time to expend 300 kcal


in weeks 12, 350 kcal in
weeks 34, and 400 kcal
in weeks 516

4560 min

NR

2040 min

Session duration

16 weeks

12 months

16 weeks

16 weeks

1 year

Intervention
duration

I. Ismail et al.

A: n = 20; brisk walking on a


treadmill, stationary cycling or
stair stepping
PRT: n = 20; Leg extension, leg
flexion, super pullover (latissimus
dorsi), bench press, shoulder
press, triceps extension, bicep
curl and sit ups

NR

M: -11.7(3.5)
F: -10.7(3.8)

Weight maintenance energy


intake reduces by
1,000 kcal/d. Limit dietary fat
intake to <30%.

C: n = 20; Diet only

1/7
5/7

0.1 (NR)

Weeks 12: 3/7


Weeks 34: 4/7
Weeks 516: 5/7

-1.3 (NR)

Maintain usual diet

Week 18: 5070% 1 RM; Week


916: 7080% 1 RM + 20% of leg
extensor and bench press sets
with 3050% 1 RM.

between sets; 80% of 1 RM

Week 14: 1 set of 10 reps then 2


sets of 10 reps. 2 min rest

Week 1: 67% HR max progressing


to 80% HR max in week 8.

Intensity

Maintain current level of physical activity

2/7

NR

23/7

NR

Frequency

A + PRT: n = 87; A: treadmill


walking, stationary bike. PRT: leg
extensions, leg curls, leg press,
chest press, seated dumbbell
row.

C: n = 86; stretching sessions

-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;

PRT: n = 13; Diet + bilateral leg


press, bilateral knee extension,
bench press, and 45 exercises
for main muscle groups of body;
all on resistance machines

C: Diet only

leg sit ups

triceps extension, lateral pull


down, bench press, military
press, lower back extension, bent

PRT: n = 21; squats, leg


extension, leg curl, elbow flexion,

55% CHO, 15% protein, 30%


fat, 500 kcal/d

800 k/cal per day (2022% fat,


1822% protein, 5862%
CHO)

C: n = 30

Hunter et al.
2010 (20)

A: n = 18; walking or jogging on a


treadmill

Nutritional intervention

Mode

Reference

Table 2 Continued

76 Exercise for visceral fat

obesity reviews

2011 The Authors


obesity reviews 2011 International Association for the Study of Obesity 13, 6891

2011 The Authors


obesity reviews 2011 International Association for the Study of Obesity 13, 6891

Ku et al. 2010
(26)

Kim et al. 2008


(25)

Johnson et al.
2009 (15)

Reduce weight maintenance


energy intake by 1,000 kcal/d,
limit dietary fat intake to <30%

C: n = 13; dietary intervention

Janssen et al.
2002 (24)

5/7

-1.1(1.3)

-1.9(1.2)

PRT: n = 13; elastic band


exercises including bicep curl,
triceps extension, upright row,
shoulder chest press, trunk side
bending, seated row, leg press,
hip flexion, leg flexion, leg
extension

A: n = 15; walking

Maintain sedentary
lifestyle

-0.6(1.7)

C: n = 16; diabetes education

4/7

NR

3/7

3/7

3/7

5/7

-0.3(8.8)

Maintain standard calorific


intake (ideal body weight
(kg) 30 kcal/kg/d)

NR

C: n = 10

Intensity

4050% max

3.65.2 METs

Week 1: -4: 4055% HRR, week


58: 5565%, week 912: 6575%
PRT 75% 1 RM

Week 1: 50% VO2peak


Week 2: 60% VO2peak
Week 3&4: 70% VO2peak

fatigue

1 set of 812 reps until volitional

50% progressing to 85% of HR


max

Maintain pre-study physical activity levels.

Frequency

A + PRT: n = 10; A: speedy


walking, V step, Cha cha step,
Mambo step, step aerobics, Gait
training with dance. PRT: Push
up, sit up, sit down and up, leg
raise, leg extension, leg curl, leg
press on free weights. Asana
Yoga

0.57(8.8)

-0.2(16.2)
-0.3(19.2)

Consume habitual diet


for 3 d before and after
intervention provided with diet
(60% CHO, 20% protein, 20%
fat)

C: n = 7; stretching

-10.0(3.0)

-11.1(4.4)

-10.0(3.9)

Weight
change
(kg)

A: n = 12; cycle ergometer

press, shoulder press, triceps


extension, biceps curl, sit ups.

intervention + leg extension, leg


flexion, super pullover, bench

intervention + treadmill, cycle


ergometer or stair stepping.
PRT: n = 14; dietary

A: n = 11; dietary

Nutritional intervention

Mode

Reference

Table 2 Continued

3 sets, 1520 reps

60 min

60 min; 30 min aerobics,


15 min Resistance, 15 min
Yoga

3045 min (15 min bouts


with intervening 5 min
rests)

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)

Kwon et al. 2010


(28)

C: n = 34; Calorie restriction

A: n = 38; Calorie
restriction + treadmill walking

Total calorie deficit of


400 kcal/d, 2530% fat,
1520% protein, 5060% CHO

-12.3(4.9)

-11.8(4.1)

-1.5(17.3)

0.2(21.4)

Maintain usual diet


50% of C and A group
supplemented with BCAA
(46% leucine, 24% isoleucine,
30% valine; protein intake
0.6 g/kg/d)

C: n = 11

A: n = 10; Ergocycle

M: -1.8(21.0)
F: -1.4(24.9)

A: n = 100; Treadmills, stationary


bikes, elliptical machines and
rowers

M: -0.1(25.2)
F: 0.7(18.6)

Asked not to change dietary


habits

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,

Kwon et al. 2010


(27)

shoulder press, chest press,


seated rows, leg press, hip
flexion, leg flexion, leg extension,
side bends with resistance bands

Nutritional intervention

Mode

Reference

Table 2 Continued

3/7

Not to alter sedentary lifestyle

1/7
intermittent

Trial: 2/7 continuous


exercise

Pre-training 3/7

1/7

6/7

Asked not to change


exercise habits

5/7

Maintain routine activity

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

1015 min progressing to


30 min by end of 6th
week

NR

Continuous: 45 min

NR

20 min45 min

60 min

60 min

3 sets 10-15 reps for


40 min plus 10 min warm
up and cool down

Session duration

20 weeks

2 weeks
pre-training
8 weeks

12 months

12 weeks

12 weeks

Intervention
duration

78 Exercise for visceral fat


I. Ismail et al.

obesity reviews

2011 The Authors


obesity reviews 2011 International Association for the Study of Obesity 13, 6891

2011 The Authors


obesity reviews 2011 International Association for the Study of Obesity 13, 6891

Rice et al. 1999

Poehlman et al.
2000 (31)

PRT: n = 10; diet


intervention + leg extension, leg
flexion, super pullover, bench
press, shoulder press, triceps
extension, biceps curl, sit ups

-13.6(4.1)

-11.5(3.9)

-12.1(3.4)

Energy intake reduced by


1,000 kcal/d, limit dietary fat
intake to <30%

C: n = 9; diet intervention only

A: n = 10; diet
intervention + treadmill walking,
stationary cycle or stair stepping

2.0(8.5)

PRT: n = 17; leg press, bench


press, leg extension, shoulder
press, sit up, seated row, tricep
extension, arm curls, leg curls

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

A + PRT: n = 10; Aerobic


programme + bench press, side
raise, tricep push down, barbell
curl, leg curl, leg extension, leg
press, leg raise, abdominal
crunch, latissimus pull down

double kick

scissor double, hop and jump,


jumping jack, side kick, full turn,

turn, Cha cha, Mambo rock,


diamond step, single hamstring
walking, heel touch, sit up, push
up. Week 1324: fast walking,
turn round, heel side, knee up,

NR

NR

C: n = 10

Park et al. 2003


(30)

A: n = 10; Aerobics: week 112:


side by side, step touch, lunge
side, v-step, grape vine, pivot

Nutritional intervention

Mode

Reference

Table 2 Continued

3/7

5/7

NR

3/7

NR

6/7

6/7

NR

Frequency

1 set of 812 reps

19 min progressing to 60 min

3 sets 10 reps, 11.5 min between


sets

Weeks 116: 5% increase in HR


max each week progressing to
90% HR max
Weeks 1728:
Mon: 80% HR max
Wed: 95% HR max
Fri: 7580% HR max.
By last session at 85% HRmax

A (3/7) 6070% HR max


PRT (3/7) Week 112 60% 1 RM,
Week 1324 70% 1 RM

6070% HR max

Intensity

~30 min

50% progressing to
85%HR max

80% 1 RM

Weeks 116: 25 min


progressing to 40 min
Weeks 1728:
Mon: 45 min
Wed: 4 5 min bouts with
3 min rests
Fri: 45 min.
By last session: 60 min

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)

Ross et al. 1996


(37)

Ross et al. 2004


(32)

C: n = 63; Walking programme as


per AHA guidelines
PRT: n = 70; isotonic variable
resistance machines and freeweight exercises for quadriceps,
hamstrings, gluteal, pectoral,
erector spinae, latissimus dorsi,
rhomboid, deltoid, bicpes, triceps

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

C: n = 11; Diet intervention only

C: n = 10; Maintain body weight


A: n = 17; Brisk walking or light
jogging on motorized treadmill;
maintain isocaloric diet and
expend 500 kcal/d with exercise

700 kcal/d

jogging on motorized treadmill.


maintain isocaloric diet and
perform exercise that expended

No changes to diet

Energy intake reduced by


1,000 kcal/d and limit dietary
fat intake to <30% of total
energy intake

Weight maintenance diet


(5060% CHO, 1520%
protein, 2030% fat) for 4- to
5-week baseline period

5-week baseline period

Weight maintenance diet


(5560% CHO, 1520%
protein, 2025% fat) for 4- to

C: n = 8; Maintain body weight

Ross et al. 2000


(36)

A: n = 16; Brisk walking or light

Nutritional intervention

Mode

Reference

Table 2 Continued

1.4(0.6)

Most days of the


week
2/7

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)

Year 1: 3 sets, 810 reps


Year 2: 2 sets and maintain the
highest weight lifted each exercise

Moderate intensity

1 set of 12 reps

NR

80% of HRmax

<70% VO2peak (80% MHR)

Intensity

Year 1: 1 h
Year 2: 45 min

30 min

NR

15 min progressing to
60 min.

Time required to expend


500 kcal.

Time taken to expend


700 kcal

Session duration

2 years

16 weeks

14 weeks

12 weeks

Intervention
duration

80 Exercise for visceral fat


I. Ismail et al.

obesity reviews

2011 The Authors


obesity reviews 2011 International Association for the Study of Obesity 13, 6891

2011 The Authors


obesity reviews 2011 International Association for the Study of Obesity 13, 6891
Weight maintenance diet for
45-week baseline period
consisting of 5560% CHO,
1520% protein, 2025% fat
Matched exercise expenditure
with additional 700 kcal/d

C: n = 8

A: n = 14; Perform exercise that


expended 700 kcal/d; brisk
walking or light jogging on a
motorized treadmill

Thong et al. 2000


(38)

7/7

80% HR max

Time required to expend


700 kcal

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

National Institute of Aging Guidelines for Exercise

M: -0.63
F: -0.5(2.3)

6580% VO2peak

AHA Step 1 diet; Maintain


normal caloric intake

0.1(0.8)

NR

1545 min

20 min progressing to
40 min

Session duration

Combined aerobic and resistance training programmes

23 sets of 79 reps

6075% HR max

HR max

70% HR max progressing to 80%

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

3/7 progressing to 4/7

Stewart et al.
2005 (48)

0.87(NR)

Intensity

Flexibility exercises to perform at home; maintain regular lifestyle

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

intake 90% estimated


weight maintenance
requirement

Recommended diet that would


not cause weight loss.
Prescribed energy

C: n = 47

PRT: n = 64; 7 different machine


weight exercises

A: n = 60; treadmills or bicycle


ergometers

C: n = 63

-1.5(18.2)

0.3(17.3)

Weight
change
(kg)

A: n = 42; treadmills, elliptical


trainers, cycle ergometers

Slentz et al. 2005


(47)

Sigal et al. 2007


(46)

Weight maintaining diet


(55%CHO, 30%fat and 15%
protein)

C: n = 37

Short et al. 2003


(45)

A: n = 65; stationary bicycle

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

Binder et al. 2005 (39)


Boudou et al. 2003 (34)
Brochu et al. 2009 (17)
Carr et al. 2005 (40)
Coker et al. 2009 (41)
Cuff et al. 2003 (18)
DiPietro et al. 1998 (42)
Donnelly et al. 2003 (7)
Giannopoulou et al. 2005 (19)
Hunter et al. 2010 (20)
Ibez et al. 2010 (21)
Irving et al. 2008 (22)
Irwin et al. 2003 (23)
Janssen et al. 1999 (43)
Janssen et al. 2002 (24)
Johnson et al. 2009 (15)
Kim et al. 2008 (25)
Ku et al. 2010 (26)
Kwon et al. 2010 (27)
Kwon et al. 2010 (28)
McTiernan et al. 2007 (44)
Mourier et al. 1997 (49)
Nicklas et al. 2009 (29)
Park et al. 2003 (30)
Poehlman et al. 2000 (31)
Rice et al. 1999 (35)
Ross et al. 2000 (36)
Ross et al. 2004 (32)
Ross et al. 1996 (37)
Schmitz et al. 2007 (33)
Short et al. 2003 (45)
Sigal et al. 2007 (46)
Slentz et al. 2005 (47)
Stewart et al. 2005 (48)
Thong et al. 2000 (38)

Table 3 Quality ratings of 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

82 Exercise for visceral fat


I. Ismail et al.

obesity reviews

2011 The Authors


obesity reviews 2011 International Association for the Study of Obesity 13, 6891

2011 The Authors


obesity reviews 2011 International Association for the Study of Obesity 13, 6891

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

Binder et al. 2005 (39)


Boudou et al. 2003 (34)
Brochu et al. 2009 (17)
Carr et al. 2005 (40)
Coker et al. 2009 (41)
Cuff et al. 2003 (18)
DiPietro et al. 1998 (42)
Donnelly et al. 2003 (7)
Giannopoulou et al. 2005 (19)
Hunter et al. 2010 (20)
Ibez et al. 2010 (21)
Irving et al. 2008 (22)
Irwin et al. 2003 (23)
Janssen et al. 1999 (43)
Janssen et al. 2002 (24)
Johnson et al. 2009 (15)
Kim et al. 2008 (25)
Ku et al. 2010 (26)
Kwon et al. 2010 (27)
Kwon et al. 2010 (28)
McTiernan et al. 2007 (44)
Mourier et al. 1997 (49)
Nicklas et al. 2009 (29)
Park et al. 2003 (30)
Poehlman et al. 2000 (31)
Rice et al. 1999 (35)
Ross et al. 2000 (36)
Ross et al. 2004 (32)
Ross et al. 1996 (37)
Schmitz et al. 2007 (33)
Short et al. 2003 (45)
Sigal et al. 2007 (46)
Slentz et al. 2005 (47)
Stewart et al. 2005 (48)
Thong et al. 2000 (38)

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

22. Same time


recruitment

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

Exercise for visceral fat

Y, Yes; N, No; U, Undeterminable; VAT, visceral adipose tissue.

11. Representative
participants

Study

Table 3 Continued

obesity reviews
I. Ismail et al. 83

84 Exercise for visceral fat

obesity reviews

I. Ismail et al.

Table 4 Outcomes of intervention studies for change in visceral fat


Reference

Mode

Measure

Region

Pre, mean (SD)

Post, mean (SD)

Change Score

Binder et al.
2005 (39)

C (n = 38)

MRI
(20 C,
34 PRT)

Serial images above and below the


L4-L5 interspace

179.0 (85.0) cm2

NR

-3.8(29.0)

195.0 (104.0) cm2

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

Carr et al. 2005


(40)

C: n = 71

C: n = 32

CT

CT

L4-L5 vertebral disc using a scout


image of the body
At level of umbilicus

C: n = 6
A: n = 6

Cuff et al. 2003


(18)

A + PRT: n = 10

C: n = 9

CT

L4-L5 vertebral disc space

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)

Irving et al. 2008


(22)

Irwin et al. 2003


(23)

C: n = 12

MRI

PRT n = 13
C: n = 7

CT

A: n = 9
C: n = 86

NR

183.0 (52.0) cm2

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)

L4/L5 vertebral disc space

259.1 (103.2) cm2

-0.4(36.0) cm2

NR

-26.3 (23.4) cm2

215.7 (77.4) cm2

A: n = 9

C: n = 30

186.0 (56.0) cm2

251.1 (72.4) cm2

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

Coker et al. 2009


(41)

156.85 (23.4) cm2


153.25 (38.55) cm2

CT

-8.8 (16.2) cm2

136.0(74.1)cm2

118.0(71.4)cm2

116.0(93.0)cm2

106.0(72.0)cm2

L4-5 vertebral space

Men: 91.7(29.7) cm2


Women: 62.9(21.8) cm2
Men: 97.9(22.5) cm2
Women: 60.6(25.5) cm2

85.4(39.7)
66.0(13.9)
75.5(18.3)
57.4(28.4)

From superior portion of head of


femur to most superior part of
kidneys

4785.0(1,592.0) cm3

4425.0(1,442.7) cm3

NR

cm3

5152.0(1,456.0) cm3

-12.8%

Supine position with arms


stretched above head; at levels of
L4 and L5

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

4th to 5th lumbar body

Abdominal and thigh; Supine


position with both arms parallel
along sides of the body
L4-L5 intervertebral disc space at
midpoint between inguinal crease
and top of patella
L4-L5 intervertebral space

5912.0(1,605.2)

NR

cm2
cm2
cm2
cm2

NR

0.8 cm2, -0.4 cm2


2

3340.0(977.0) cm

2724.0(1,052.0) cm

3290.0 (1,141.0) cm2

2633.0 (1,000.0) cm2

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

Intervertebral space between L4


and L5 as point of origin

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

5 cm below to 15 cm above L4-L5

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

L4-L5 intervertebral space

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

Kim et al. 2008


(25)

A + PRT: n = 10

Ku et al. 2010
(26)

A: n = 15

C: n = 10

C: n = 16

CT

CT

L4 vertebrae close to umbilicus

Abdominal

PRT: n = 13
Kwon et al. 2010
(27)

C: n = 15

Kwon et al. 2010


(28)

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

10 mm line from lumbar vertebrae


4 and 5 to bellybutton

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

Cross-sectional area of L4-L5


vertebrae

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%

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I. Ismail et al. 85

Table 4 Continued
Reference

Mode

Measure

Region

Pre, mean (SD)

Post, mean (SD)

Change Score

McTiernan et al.
2007 (44)

C: n = 102
A: n = 100

CT

L4-L5 space

Men: 176.7(79.1) cm2


Women: 102.6(55.8)
cm2
Men: 161.8(66.3) cm2
Women: 105.9(60.8)
cm2

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

Level of the umbilicus

A: n = 10
C: n = 34

CT

Within 15 mm centres at L4-L5


level

Poehlman et al.
2000 (31)

Rice et al. 1999


(35)

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

L4-L5 vertebral level

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

Ross et al. 2004


(32)

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

Short et al. 2003


(45)

C: n = 37

Slentz et al. 2005


(47)

80.4(22.1) cm2

195.0(12.6) cm3

C: n = 10

PRT: n = 10

Sigal et al. 2007


(46)

134.9(33.8) cm2

A: n = 10

Ross et al. 2000


(36)

Ross et al. 1996


(37)

139.4(36.8) cm2
156.1(47.4) cm2

2509.0(737.0) cm3

A: n = 38

Park et al. 2003


(30)

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

Two sets from L4-L5 to upper


thorax and one extended from
L4-L4 to approximate level of
femoral head

-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

L4-L5 intevertebral space

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

252.0 (147.0) 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

224.0 (159.0) cm2

CT

Transverse cut at L4-L5

C: n = 47

CT

L4 pedicle

A: n = 42

Stewart et al.

C: n = 53

2005 (48)

A + PRT: n = 51

Thong et al. 2000


(38)

C: n = 8

MRI

One slice below, at and above


umbilicus

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

1 image below and 4 images


above the L4-L5 intervertebral
space

Whole body

NR

NR

165.0(68.0)

179.2

8.6(17.2)%

168.0(64.0)

156.4

-6.9(20.8)%

Male: 162.7(70.3) cm2


Female: 123.4(62.6)
cm2
Male: 186.5(63.4) cm2
Female: 109.6(47.7)
cm2

NR

-7.4 (27.88) cm2


-0.3(23.1) cm2
-40.6(33.0) cm2
-14.5(23.2) cm2

4.1(1.7)kg

NR

3.9(0.8)kg

-0.003(0.3)
-1.1(0.4)

All data reported as means SD.


BMI, body mass index; A, aerobic training; PRT, progressive resistance training; C, controls; NR, not reported.

Effect of exercise therapy on visceral adiposity


(Meta-analyses)
The effect of exercise therapy on visceral adiposity is summarized in Table 4 and Figs 25.

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).

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86 Exercise for visceral fat

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.

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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.

Further examination of these showed that one study was an


outlier with much larger effect size. This study employed
high volume (6 d per week, ~60 min per session). After
re-analysis via random effects model with this outlier
removed, there remained a significant pooled ES (-0.33,
95% CI: -0.52 to -0.14; P < 0.01) (Fig. 2).
Progressive resistance therapies
The pooled ES for the comparison between resistance
exercise therapy and control did not reach significance
(ES = 0.05, 95% CI: -0.10 to 0.20; P = 0.52). Significant
heterogeneity among studies was observed (I2 = 61.7%,
P < 0.01). After re-analysis via random effects model, the
pooled ES was 0.09 (95% CI: -0.17 to 0.36; P = 0.49)
(Fig. 3).
Aerobic exercise vs. progressive resistance therapies
The pooled ES for the comparison between aerobic exercise
and resistance exercise therapies showed a non-significant
effect which tended to favour aerobic training (ES = 0.20,

95% CI: -0.02 to 0.42; P = 0.08). Low heterogeneity


among studies was observed (I2 = 20.1%, P = 0.26). Analysis via random effects model showed that the pooled ES did
not reach statistical significance (ES = 0.23, 95% CI: -0.02
to 0.50; P = 0.07) (Fig. 4).
Combined aerobic exercise and progressive
resistance therapies
There was a significant pooled ES for interventions
that combined aerobic and resistance exercise therapy
vs. control (ES = -0.27, 95% CI: -0.46 to -0.08;
P < 0.01). Significant heterogeneity among studies was
observed (I2 = 87.1%, P < 0.01). Further examination of
these showed that one study was an outlier with much
larger effect size and low precision. It is noteworthy that
this study had a low sample size (10 subjects per
group). After re-analysis with this outlier removed using
random effects the pooled ES did not reach statistical significance (-0.28, 95% CI: -0.69 to 0.14; P = 0.19)
(Fig. 5).

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88 Exercise for visceral fat

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.

2011 The Authors


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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,

Exercise for visceral fat

I. Ismail et al. 89

when caloric expenditure of exercise is matched, higher


intensity exercise is more effective for reduction in VAT22
which has been attributed to the augmented secretion of
lipolytic hormones such as growth hormone (GH) (55).
GH acts to stimulate adipose tissue directly via hormone
sensitive lipase and also indirectly by enhancing insulin
sensitivity (56,57). Although resistance training induces
acute increases in GH secretion, chronic aerobic training
(particularly at higher intensities) can lead to chronic
increases in 24-h GH release (58). This is consistent with
our observation of a significant reduction in VAT following aerobic but not resistance exercise training. However,
our failure to observe a relationship between exercise
intensity and VAT reduction is likely to be due to heterogeneity in study duration, training frequency, modality
and cohort characteristics.
Several limitations exist which should be considered when
interpreting the results of this review. Although the majority
of the cohorts examined were overweight or obese, there
were two studies which included lean participants and others
with known metabolic disease. Furthermore, differences in
exercise prescription (intensity, duration, modality, frequency and intervention length) contributed to heterogeneity.
Only one study in this review (15) attempted to blind the
control group using a sham-exercise design. Blinding of the
researcher/s conducting the baseline and post-intervention
assessment of the main outcome measures occurred in just
two studies (15,46). Other potential confounders included
differences in dietary intake and activity performed outside
of the interventions. Four of the 29 studies examined
reported non-significant or near significant effects of AEx
intervention on VAT and were likely limited by low subject
numbers. Our finding of a strong statistically significant
effect for AEx on VAT highlights the relevance of a pooled
analysis approach for providing clarity on this effect.
Despite these limitations, this systematic review with
meta-analyses provides useful information for the clinical
application of exercise in the management of obesity. There
is strong evidence for the effectiveness of AEx therapy but
not for resistance exercise. However, the goal of reducing
visceral adiposity in isolation is unlikely in most obese
individuals in whom multiple cardiometabolic risk factors
are likely to be present, and PRT has been shown to be
effective for improving risk factors including insulin resistance and dyslipidaemia (59). Although direct comparison
between AEx and PRT is problematic due to differences in
metabolic strain and appropriate dosage/volume, it is clear
from the present results that the aerobic component of
exercise therapy is central to exercise-induced VAT modification. The present study highlights the need for more
research examining the efficacy of combined AEx and PRT
modalities but suggests that combined interventions should
not sacrifice an adequate volume of aerobic training for the
inclusion of PRT. Given that the studies reviewed in this

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obesity reviews 2011 International Association for the Study of Obesity 13, 6891

90

obesity reviews

Exercise for visceral fat I. Ismail et al.

investigation comply with current recommendations for


improvement in cardiorespiratory fitness (150 min/week
of moderate intensity aerobic activity) (51), these recommendations appear sufficient for favourably modifying
VAT despite being lower than specific overweight/obesity
management guidelines.

Conflict of Interest Statement


No conflict of interest was declared.

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