DIABETICMedicine

DOI: 10.1111/j.1464-5491.2010.03045.x

Short Report
The effects of total energy expenditure from all levels
of physical activity vs. physical activity energy
expenditure from moderate-to-vigorous activity on
visceral fat and insulin sensitivity in obese Type 2
diabetic women

B. K. Koo, K. A. Han*, H. J. Ahn†, J. Y. Jung†, H. C. Kim‡ and K. W. Min*

Department of Internal Medicine, Seoul National University College of Medicine, *Department of Internal Medicine, Eulji University School of Medicine, †Diabetes
Center, Eulji Hospital, ‡Department of Radiology, Eulji University School of Medicine, Seoul, Korea

Accepted 2 June 2010

Abstract
Aims We examined the effects of physical activity with or without dietary restriction for 3 months on regional fat and insulin
sensitivity and compared the effect of total energy expenditure from all levels of physical activity with that of physical activity
energy expenditure from moderate-to-vigorous exercise in obese women with Type 2 diabetes.
Methods In this randomized, controlled trial, we assessed change of body weight, abdominal visceral fat area, subcutaneous
fat area and insulin sensitivity, expressed as KITT, and monitored total energy expenditure and physical activity energy
expenditure using an accelerometer during a 12-week intervention in four groups: control, diet, exercise and diet plus exercise.
Results The mean body mass index was 28.0  2.7 kg ⁄ m2 and the mean duration of diabetes was 8  6 years. Both the diet
and diet plus exercise groups showed significant body weight loss compared with the control group (P < 0.05). However, the
visceral fat area was reduced only in the diet and exercise group (P = 0.017) and the subcutaneous fat area was reduced only in
the diet group (P = 0.009). Mean energy intake was an independent determinant of the change in subcutaneous fat
area (P = 0.020) and mean total anergy expenditure was an independent determinant of visceral fat area (P = 0.002). Insulin
sensitivity KITT was associated with physical activity energy expenditure (P = 0.006), energy intake (P = 0.047) and the
change in fructosamine level (P = 0.016) but not with changes in body weight, subcutaneous fat area, visceral fat area or
adipokine level.
Conclusions Exercise had an additive effect to dietary restriction on visceral fat reduction. Visceral fat area was associated with
total energy expenditure, but insulin sensitivity was associated with physical activity energy expenditure.
Diabet. Med. 27, 1088–1092 (2010)
Keywords exercise, visceral fat and insulin sensitivity

Abbreviations BMI, body mass index; EE, energy expenditure; EI, energy intake; HbA1c, glycated haemoglobin; KITT,
insulin sensitivity; PAEE, physical activity-associated energy expenditure; SFA, subcutaneous fat area; TEE, total fat
area; VFA, visceral fat area

We performed a prospective, randomized, controlled trial to

Introduction
The benefits of exercise for the management of diabetes and
obesity might originate from increased lipid oxidation in
response to training adaptation [1].
Correspondence to: Kyung Wan Min, MD, PhD
Department of Internal Medicine, Eulji University School of Medicine
280-1 Hagye-Dong Nowon-Gu, Seoul 139-711, Korea.
E-mail: minyungwa@yahoo.co.kr
investigate the effects of exercise on regional fat depots and
insulin sensitivity in obese women with Type 2 diabetes. We
monitored physical activity in daily life during an intervention
and compared the effect of total energy expenditure from all
levels of physical activity with that of physical activity energy
expenditure from moderate-to-vigorous activity. Dietary
restriction was applied with or without exercise to distinguish
between the effects of physical activity and weight change.

ª 2010 The Authors.

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 Short report
Patients and methods
We studied Korean women with Type 2 diabetes who were
admitted to the Diabetes Clinic at Eulji Hospital and met the
inclusion criteria: (i) Type 2 diabetes, (ii) body mass index (BMI)
‡ 23 kg ⁄ m2, (iii) a glycosylated haemoglobin (HbA1c) level
£ 10% and (iv) no cardiovascular disease. All medications for
glucose control except thiazolidinedione were permitted and
their dosages were maintained during the intervention, except in
cases of hypoglycaemia. The Institutional Review Board of the
Clinical Research Institute at Eulji Hospital approved the study
protocol and informed consent was obtained from each subject.
All of the subjects were randomly assigned to one of four groups
forthe12-weeklifestyleintervention:control,diet,exerciseordiet
plus exercise. The control and exercise groups were given
conventional education for a mild hypocaloric diet (30 kcal per
kg of ideal body weight per day) at the beginning of the study. The
diet and diet plus exercise groups were asked to reduce their usual
energy intake to 1200 kcal ⁄ day for weight reduction [2] and were
educated individually every 2 weeks based on the self-recorded
3-day diet diary. The recommended dietary macronutrient
composition was the same for all groups; namely, 50–55% of
energy intake as carbohydrate, 15–20% as protein and 20–25%
as fat. Daily entergy intake and nutrient consumption were
determined from a computer-aided nutritional analysis program
(CAN-Pro; Korean Nutrition Society, Seoul, Korea).
The control and diet groups were given conventional exercise
education at the beginning of the study; namely, 150 min or more
per week [2]. The exercise and diet plus exercise groups were
requested to walk briskly for 120 min every day, which
corresponds to an energy expenditure of approximately
500 kcal ⁄ day [3], and this was reinforced by a professional
exercise therapist every 2 weeks based on data from the
accelerometer (Lifecorder; Suzuken Co., Nagoya, Japan). All
subjects were requested to attach an accelerometer to their belts
all day long during the intervention period. Data from the
accelerometers were analysed using physical activity analysis
software v1.0 [4] to determine energy expenditure: physical
activity energy expenditure was defined as energy expenditure
from moderate or vigorous physical activity (‡ 4 metabolic
equivalents) and total energy expenditure from basal metabolism
and light activity (< 4 metabolic equivalents) plus physical
activity energy expenditure [4]. Those who did not visit the
hospital on four consecutive occasions or who could not reach
80% of goal of intervention were excluded from the study.
All subjects were examined in the morning after an overnight
fast at baseline and after conclusion of the lifestyle intervention.
Insulin sensitivity was calculated from the first-order constant for
the disappearance rate of glucose (KITT) during insulin tolerance
test, estimated from the regression line of the logarithm of blood
glucose against time [5]. Computerised tomography was used to
assess the cross-sectional fat distribution in the abdomen at the
L4–5 intervertebral disc level. The total fat area was divided into
a subcutaneous fat area and a visceral fat area as previously
described [6].
ª 2010 The Authors.
Diabetic Medicine ª 2010 Diabetes UK
DIABETICMedicine
Statistical analyses were carried out using SPSS ⁄ Win software
(SPSS Inc., Chicago, IL, USA). To evaluate changes during a 12-
week lifestyle modification, we performed an analysis of
covariance (ancova) for intergroup analysis and a paired t-test
for within-group analysis. A stepwise multiple regression test was
used to identify the main determinants of the change in fat area
and insulin sensitivity, irrespective of intervention group. Post
hoc analysis was conducted using Bonferroni’s test.
Results
Baseline characteristics
Among initial 70 women enrolled in the study, 64 subjects
(control, n = 18; diet, n = 19; exercise, n = 13; diet and
exercise, n = 14) were included in the analysis according to
exclusion criteria. The mean age of the subjects was
56  8 years and mean BMI was 28.0  2.7 kg ⁄ m2. There
was no difference in age, disease duration, HbA1c level and
baseline KITT among the groups. However, there were marginal
differences among the four groups despite the initial
randomization (Table 1): the diet and exercise group had a
higher BMI than the exercise group (P = 0.046) and greater
subcutaneous fat area and baseline total energy expenditure
than the control group (P = 0.036 and P = 0.044, respectively).
There was no difference in the type of anti-diabetic medication
among the groups (data not shown).
Changes in body weight and body fat area according to
intervention group
During the 12-week intervention, the mean energy intake of the
diet group was significantly less than that of the control or
exercise groups (P < 0.001) and the mean physical activity
energy expenditure and total energy expenditure of the exercise
and diet and exercise groups was significantly greater than that of
the control or diet groups (P < 0.01) (Table 1). The percentage
change in body weight in the diet and diet and exercise groups
was significantly greater than in the other two groups (P < 0.05)
and there was no difference in body weight reduction between the
control and exercise groups (Table 1). Only the diet and exercise
group showed a significantly larger percentage change in the
visceral fat area compared with the control group (P = 0.017)
and only in the diet group did the subcutaneous fat area decrease
more than in the control group (P = 0.009) (Table 1). A stepwise
multiple regression test conducted irrespective of group showed
that mean energy intake during the intervention was an
independent determinant of the amount of change in
subcutaneous fat area (P = 0.021) and that the mean total
energy expenditure during the intervention was an independent
determinant of the change in visceral fat area (P = 0.002), even
after adjusting for body weight change and baseline body fat
area. Mean physical activity energy expenditure was also
significantly correlated with visceral fat area (r = –0.284,
P = 0.025). However, this relationship was not statistically
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Table 1 Characteristics of the subjects at the time of enrolment and changes after the 12-week intervention

n (%) or mean  sd
DIABETICMedicine

Diet plus exercise

Characteristics Control (group C) Diet (group D) Exercise (group E) (group DE) Pà

Female sex 18 (100) 19 (100) 13 (100) 14 (100) NS

Age (years) 57  8 57  8 59  4 53  8 NS
Duration of diabetes (years) 86 10  7 86 77 NS
BMI (kg ⁄ m2) 28.5 (24.0–31.5) 27.1 (24.0–31.5) 25.5 (23.5–34.4) 29.4 (25.9–37.8) 0.045
Lifestyle
TEE (kcal ⁄ day) Baseline 1783 (1467–2327) 1779 (1584–2291) 1905 (1612–2401) 2054 (1569–2341) 0.031
12 weeks 1818 (1666–2217) 1823 (1644–2119) 2068 (1756–2621)*  2135 (1904–2564)*  < 0.001
PAEE (kcal ⁄ day) Baseline 215 (61–551) 246 (113–649) 288 (137–779) 333 (156–490) NS
12 weeks 293 (49–584) 246 (127–516) 448 (224–820)*  511 (284–672)*  0.003
EI (kcal ⁄ day) Baseline 1819 (1531–2331) 1894 (1529–2253) 1747 (1368–2458) 2027 (1469–2329) NS
12 weeks 1597 (1373–1919) 1354 (1174–1610)* 1625 (1346–2506)  1483 (1219–1852) < 0.001
Laboratory findings
FPG (mmol ⁄ l) Baseline 7.1  1.7 7.0  1.6 7.8  1.2 6.9  2.0 NS
12 weeks 6.5  2.2 6.2  0.9 7.6  1.8 6.7  1.3 NS
Change in 12 weeks (%) –0.61  1.59 (–7.4) )0.94  1.57 ()9.1) )0.19  1.41 ()1.5) )0.09  2.14 (7.2)
HbA1c (%) Baseline 7.5  1.1 7.5  1.1 7.8  1.0 8.0  1.8 NS
12 weeks 7.0  2.0 7.0  0.8 7.2  1.1 7.2  1.2 NS
Change in 12 weeks (%) )0.43  1.00 (–5.6) )0.59  0.61 ()7.3) )0.56  0.64 ()7.1) )0.78  1.10 ()7.9)
Body weight and abdominal fat area
Body weight (kg) Baseline 66.0 (57.0–73.7) 67.4 (58.9–76.7) 64.0 (60.0–86.8) 69.4 (58.6–89.6) NS
12 weeks 65.8 (53.5–73.1) 62.4* (54.6–70.5) 62.4 (59.4–87.9) 64.8* (50.0–86.0) 0.004
Change in 12 weeks (%) –1.5  1.5 ()2.3) )4.7  1.4 (–7.1) )2.1  2.2  (–3.1) )4.4  1.9 ()6.4)
VFA (cm2) Baseline 172.4 (67.5–276.2) 157.8 (76.1–238.0) 162.4 (104.7–255.8) 152.7 (116.2–391.3) NS
12 weeks 163.4 (51.8–248.8) 151.7 (75.2–206.7) 146.9 (70.1–187.4) 120.0* (64.3–219.9) 0.017
Change in 12 weeks (%) )8.0  30.3 ()2.7) )19.5  28.0 ()10.9) )29.7  23.3 ()17.3) )38.2  26.0 ()22.3)
SFA (cm2) Baseline 208.1 (136.2–312.6) 216.5 (153.5–308.0) 219.0 (149.3–326.5) 263.9 (143.2–434.7) 0.043
12 weeks 204.0 (114.4–301.8) 196.1* (128.1–280.0) 220.0 (138.0–286.4) 231.7 (125.0–403.1) 0.009
Change in 12 weeks (%) 0.1  21.4 (0.0) )27.6  27.0 (–12.8) –16.8  23.6 ()6.7) )26.5  25.2 ()10.2)

Parameters with normal distributions are presented as the mean  standard deviation (sd). Parameters that did not have normal distributions were analysed after log-transformation and
are presented as the median and range.
BMI, body mass index; EI, energy consumption in diet; FPG, fasting plasma glucose; HbA1c, glycated haemoglobin; NS, not significant; PAEE, physical activity energy expenditure; SFA,
subcutaneous fat area; TEE, total energy expenditure; VFA, visceral fat area.
*P-value < 0.05 compared with the control group,  P-value < 0.01 compared with the diet group, àsignificance from analysis of variance (anova); for the analysis of change during intervention,
analysis of covariance (ancova) was performed and adjusted for age, baseline BMI and baseline value of the dependent factor.
Exercise intensity, insulin sensitivity and visceral fat • B. K. Koo et al.

Diabetic Medicine ª 2010 Diabetes UK

ª 2010 The Authors.
 Short report
significant after adjusting for body weight change, mean energy
intake and mean total energy expenditure.
Change in glucose level and insulin sensitivity
All intervention groups but not the control group exhibited an
improvement in HbA1c level after 12 weeks (P < 0.05) and there
was no difference in levels among groups (Table 1). However,
more subjects in the diet and diet and exercise groups could
reduce or stop their anti-diabetic medication compared with the
control group: 45% in the diet group, 57.1% in the diet and
exercise group and 5.6% in the control group (P < 0.01). Only
15.4% of the exercise group could reduce their medication;
which was not statistically different from that of the controls.
KITT improved in all groups (P < 0.05) and there were no
significant differences between groups (data not shown). The
magnitude of change in KITT was significantly associated with
mean physical activity energy expenditure and mean energy
intake during the intervention (P = 0.010 and P = 0.007,
respectively) after adjusting for group, age, medication and
baseline KITT.
Discussion
Dietary restriction is known as the most effective method for
decreasing body weight via a negative energy balance [7–9] and
we confirmed this: only groups subjected to energy restriction,
with or without exercise, showed a significant body weight
reduction. In addition, exercise intervention plus dietary
restriction reduced the visceral fat level significantly, with a
similar amount of change in body weight to that of the diet group.
There has been much debate on the additional effect of the
exercise to dietary restriction, even in the recent two well-
controlled randomized trials [10,11] in which energy intake and
the amount of supervised exercise were objectively measured.
However, few studies examined the energy expenditure during
the free-living state beyond exercise. We monitored all the
activities from daily living to distinguish between physical
activity energy expenditure and total energy expenditure and
found that total, but not physical activity energy expenditure,
was an independent determinant of the change in visceral fat
area, which suggests that uncontrolled energy expenditure
during non-structured activities in the prior studies might have
brought the different results.
Although total energy expenditure was associated with a
reduction in visceral fat area, only physical activity energy
expenditure, corresponding with the amount of moderate-to-
vigorous activity, improved insulin sensitivity along with mean
energy intake during the intervention, which is consistent
with the results of previous studies [12–14]. However, an
epidemiologic study showed that total energy intake estimated
from 1-year recall was correlated with insulin sensitivity in
subjects with diabetes [15]. The metabolic importance of light-
intensity activity needs to be elucidated in studies involving long-
term follow-up.
ª 2010 The Authors.
Diabetic Medicine ª 2010 Diabetes UK
DIABETICMedicine
The limitations of this study were the small study size and the
heterogeneity among groups. The diet and exercise group had a
relatively higher body mass and fat than other groups at baseline,
which might require greater energy expenditure with the same
amount of exercise and might make an over-estimation of the
additive effect of exercise to the dietary restriction. Furthermore,
monitoring of energy intake was only from a self-reported diary
which is well known to be under-reported [16,17].
In conclusion, physical activity had an effect on visceral fat
reduction that was additive to that of dietary restriction, despite
the absence of an additive effect on body weight reduction. Total
energy expenditure reduced levels of visceral fat, but only
moderate-intensity exercise improved insulin sensitivity in
Type 2 diabetes. Although exercise and dietary restriction had
different effects on visceral and subcutaneous fat, both improved
insulin sensitivity in obese women with Type 2 diabetes.
Competing interests
Nothing to declare.
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