Diabetes Research and Clinical Practice 65 (2004) 235–241

Beneficial effect of low carbohydrate in low calorie diets on

visceral fat reduction in type 2 diabetic patients with obesity
Yoh Miyashita a , Nobukiyo Koide a , Masaki Ohtsuka a , Hiroshi Ozaki a , Yoshiaki Itoh a ,
Tomokazu Oyama a , Takako Uetake b , Kiyoko Ariga b , Kohji Shirai a,∗
a Center of Diabetes, Endocrine and Metabolism, Sakura Hospital, School of Medicine, Toho University,
564-1 Shimoshizu, Sakura-City, Chiba 285-0841, Japan
b Department of Nutritione, Sakura Hospital, School of Medicine, Toho University, Chiba, Japan

Received 15 March 2003; received in revised form 9 December 2003; accepted 29 January 2004

Abstract

The adequate composition of carbohydrate and fat in low calorie diets for type 2 diabetes mellitus patients with obesity is not
fully established. The aim of this study was to investigate the effects of low carbohydrate diet on glucose and lipid metabolism, es-
pecially on visceral fat accumulation, and comparing that of a high carbohydrate diet. Obese subjects with type 2 diabetes mellitus
were randomly assigned to take a low calorie and low carbohydrate diet (n = 11, 1000 kcal per day, protein:carbohydrate:fat =
25:40:35) or a low calorie and high carbohydrate diet (n = 11, 1000 kcal per day, protein:carbohydrate:fat = 25:65:10) for 4
weeks. Similar decreases in body weight and serum glucose levels were observed in both groups. Fasting serum insulin levels
were reduced in the low carbohydrate diet group compared to the high carbohydrate diet group (−30% versus −10%, P < 0.05).
Total serum cholesterol and triglyceride levels decreased in both groups, but were not significantly different from each other.
High-density lipoprotein–cholesterol (HDL–C) increased in the low carbohydrate diet group but not in the high carbohydrate
diet group (+15% versus 0%, P < 0.01). There was a larger decrease in visceral fat area measured by computed tomography
in the low carbohydrate diet group compared to the high carbohydrate diet group (−40 cm2 versus −10 cm2 , P < 0.05). The
ratio of visceral fat area to subcutaneous fat area did not change in the high carbohydrate diet group (from 0.70 to 0.68), but it
decreased significantly in the low carbohydrate diet group (from 0.69 to 0.47, P < 0.05). These results suggest that, when restrict
diet was made isocaloric, a low calorie/low carbohydrate diet might be more effective treatment for a reduction of visceral fat,
improved insulin sensitivity and increased in HDL–C levels than low calorie/high carbohydrate diet in obese subjects with type
2 diabetes mellitus.
© 2004 Elsevier Ireland Ltd. All rights reserved.

Keywords: Low carbohydrate diet; Low calorie diet; Type 2 diabetes mellitus; Obesity; Visceral fat

1. Introduction

The distribution of body fat is known to be im-

∗ Corresponding author. Tel.: +81-43-462-8811; portant in the development of obesity-associated
fax: +81-43-489-9770. metabolic disorders. In particular, accumulation of
E-mail address: kshirai@kb3.so-net.ne.jp (K. Shirai). visceral fat is related to the development of insulin

0168-8227/$ – see front matter © 2004 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.diabres.2004.01.008
236 Y. Miyashita et al. / Diabetes Research and Clinical Practice 65 (2004) 235–241
resistance [1,2] and to a high incidence of coronary
heart disease [3,4].
A low calorie diet is recognized to be a fundamen-
tal therapy for type 2 diabetic patients with obesity
to improve insulin sensitivity by weight reduction. A
principle of this diet is to provide an adequate amount
of proteins, vitamins and minerals, and to restrict car-
bohydrates and fats as energy components. There have
been several reports concerning the role of nutrient
composition of the diet for weight reduction in obe-
sity [5–7]. For example, Rabast et al. [5] reported that
low carbohydrate diet is beneficial for weight reduc-
tion, which is associated with low insulin levels and a
suppression of appetite by ketone body formation. On
the other hand, Yong and Werner et al. reported that
low carbohydrate diet is not always superior to high
carbohydrate diet for body weight reduction [6,7]. As
a result, there is no definite evidence for appropriate
ratio of carbohydrate in low calorie diet.
Recently, in rats given a normal calorie diet, Zava-
roni and Reaven et al. [8] reported that a diet composed
of 60% carbohydrates raised glucose levels and de-
creased insulin sensitivity in rats. Furthermore, Coul-
ston and co-workers [9] reported that high carbohy-
drate diet increased serum glucose, insulin and triglyc-
eride levels, and decreased HDL–C in diabetic pa-
tients.
We have previously reported that low calorie diet
composed of low carbohydrate is preferable for an im-
provement of glucose and lipoprotein metabolism in
type 2 diabetes mellitus patients with obesity [10]. In
this paper, to clarify whether high or low carbohydrate
diet is more beneficial for type 2 diabetes mellitus pa-
tients with obesity, the effects of both diets on visceral
fat accumulation as well as parameters of glucose and
lipid metabolism were studied.
2. Subjects and methods
2.1. Subjects
Twenty-two obese subjects with type 2 diabetes
mellitus patients were recruited for the study (16
males, 6 females, mean body mass index 27 kg/m2 ).
The mean age was 52.4 ± 13.0 years old. They were
all hospitalized and took no medication. All of sub-
jects gave informed consent.
2.2. Diet composition
The ratio of the low carbohydrate diet compositions
of protein, carbohydrate and fat was 25:39:35 (%), and
in high carbohydrate diet, the ratio was 26:62:10 (%).
The ratio of saturated fatty acids, monounsaturated
fatty acids and polyunsaturated fatty acids were 3:4:3
in both diets. Palmitic acid constituted about 70% of
the saturated fatty acids, oleic acid about 95% of the
monounsaturated fatty acids, and a linoleic acid about
70% of the polyunsaturated fatty acids. The content
of dietary fibers was about 18 g per day in the low
carbohydrate diet and about 20 g per day in the high
carbohydrate diet.
2.3. Program of diet therapy
The subjects were initially given a 3 day low calo-
rie diet composed of high carbohydrate (1000 kcal per
day, P:F:C = 26:10:62), after which they were divided
into two random groups. One group of subjects was
treated with a low calorie diet composed of low car-
bohydrate (=low carbohydrate diet group, n = 11),
and the other was treated with a low calorie diet com-
posed of high carbohydrate (=high carbohydrate diet
group, n = 11). The clinical profile of the subjects
at the start of the different diet therapies is shown in
Table 1. There were no significant differences between
the two groups. The subjects were treated for 4 weeks
with these diets. During this study, all patients were
without medications and treated with exercise therapy
(walking, 30 min × 2 times per day).
2.4. Blood sampling
Blood samples were taken in the morning after 12 h
of fasting. Serum was obtained within 1 h and samples
were used for measuring of blood sugar (FBS), insulin
(basal IRI), serum total cholesterol (TC), triglyceride
(TO) and HDL–C.
2.5. Measurement of body weight and total body fat
Body weight and total body fat were measured in
the morning after 12 h of fasting. The percent body
fat (%) and lean body mass (LBM) were measured by
impedance method using Serkoimpemeter (SIF-93 1,
Serko, Japan).
 Y. Miyashita et al. / Diabetes Research and Clinical Practice 65 (2004) 235–241 237

Table 1
Clinical profiles of low carbohydrate diet group or high carbohydrate diet group before treatment
High carbohydrate group (n = 11) Low carbohydrate group (n = 11) Significance

Body mass index 27 ± 2 27 ±4 None

V/S ratioa 0.71 ± 0.8 0.69 ± 0.7 None
HbAlc (%) 9.8 ± 2 10.2 ±2 None
Fasting blood sugar (mg/dl) 200 ± 50 207 ± 36 None
Basal IRI (␮U/ml) 5.9 ± 1.0 6.2 ± 0.9 None
Total cholesterol (mg/dl) 193 ± 48 199 ± 35 None
Triglyceride (mg/dl) 173 ± 60 175 ± 89 None
HDL–C (mg/dl) 39 ± 16 38 ± 10 None
a The ratio of visceral fat area/subcutaneous fat area.

2.6. Measurement of adipose tissue distribution 3. Results

To measure visceral and subcutaneous fat mass,
computed axial tomography was performed [1]. The
scan was performed at the position of the navel. Vis-
ceral fat area was measured by drawing a line within
the muscle wall surrounding the abdominal cavity. The
subcutaneous fat was calculated by subtracting the
amount of visceral fat from the total fat area. From
these values, a ratio of visceral fat area to subcuta-
neous fat area (V/S ratio) and an area of visceral fat
was obtained.
2.7. Statistical analysis
Statistical analysis was performed using Student’s
t-test and paired t-test. P values less than 0.05 were
considered significant.
3.1. Change in the body weight, fat (%) and LBM
In the low carbohydrate and the high carbohydrate
diet groups, the body weight decreased from 73 to
64 kg, and from 71 to 64 kg, respectively, after low
calorie diet for 4 weeks (Fig. 1A). During these low
calorie diet therapies, fat (%) decreased in both groups,
with no change in LBM in either group (Fig. 1B).
These changes in body weight, body fat (%) and LBM
were not significantly different between the low and
high carbohydrate diet groups (Fig. 1A and B).
3.2. Change in FBS and basal IRI
In low carbohydrate and high carbohydrate diet
groups, FBS decreased from 207 to 104 mg/dl, and

Fig. 1. Changes in body weight, body fat (%) and lean body mass during low calorie diets in low carbohydrate diet group (䊉) and high
carbohydrate diet group (䊊). (A–C) Show changes of body weight, body fat (%), and lean body mass, respectively. Data are shown as
mean ± S.D.
238 Y. Miyashita et al. / Diabetes Research and Clinical Practice 65 (2004) 235–241
Fig. 2. Effect of the low carbohydrate diet (䊉) and the high car-
bohydrate diet (䊊) on fasting blood glucose levels. Fasting blood
glucose levels were decreased in both groups with no significant
difference between the two groups. Data are shown as mean±S.D.
from 200 to 102 mg/dl, respectively after low calorie
diet for 4 weeks. There was no significant difference
between two groups (Fig. 2).
Basal IRI showed a larger decrease in low carbo-
hydrate diet group compared to the high carbohydrate
diet group (Fig. 3A). The decreasing rate of basal IRI
was significantly high in low carbohydrate diet group
compared to high carbohydrate group (Fig. 3B).
3.3. Change in serum lipids
TC and TG were decreased by about 20%, and
40–50% in low carbohydrate diet group and high
carbohydrate diet group during low calorie diet, but
Fig. 3. Changes in IRI during low calorie diets in low carbohydrate diet group (closed circle and solid bar) and high carbohydrate diet
(open circle and open bar). (A and B) Show change and ratio of decrease of basal IRI. Data are shown as mean ± S.D., ∗ P < 0.05.
no significant difference was observed between both
groups (Fig. 4A and B).
HDL–C was significantly increased in the low car-
bohydrate diet group compared to the high carbohy-
drate diet group (Fig. 4C).
3.4. The change in visceral fat, and V/S ratio
In the low carbohydrate diet group, the amount of
visceral fat area was significantly decreased from 124
to 84 cm2 (P < 0.05) after 4 weeks of diet, and V/S
ratio decreased from 0.47 to 0.69 (P < 0.05) during
the same period (Fig. 5A and B). In contrast, neither
the amount of visceral fat area or V/S ratio changed
significantly during diet in the high carbohydrate diet
group (Fig. 5A and B).
4. Discussion
In this study, we have shown for the first time a dif-
ference in effects of two low calorie diets with low
or high carbohydrate content on visceral fat loss and
serum insulin levels in obese patients with type 2 di-
abetes.
During both diet therapies, the body weights were
decreased without a decrease in LBM, and FBS lev-
els decreased as well as TC and TG levels. However,
although the decrease in FBS were similar between
the high and low carbohydrate diet groups, basal IRI
levels were significantly lower in the low carbohy-
drate diet group compared to the high carbohydrate
 Y. Miyashita et al. / Diabetes Research and Clinical Practice 65 (2004) 235–241 239

Fig. 4. Changes in serum lipids during low calorie diets in low carbohydrate diet group (䊉) and high carbohydrate diet group (䊊). (A–C)
Show changes of total cholesterol, triglyceride and HDL–C. Data are shown as mean ± S.D, ∗ P < 0.05 and ∗∗ P < 0.01.

diet group at the end of the study. The lower lev-
els of insulin with similar levels of blood glucose
indicate a larger improvement of insulin sensitivity
in the low carbohydrate diet group. The homeostasis
model assessment-ratio [11] of the low carbohydrate
diet group and the high carbohydrate diet group were
changed from 3.06 to 0.77, and from 2.96 to 1.21, re-
spectively (data not shown).
HDL–C levels were also significantly increased af-
ter 4 weeks diet in the low carbohydrate diet group
compared with the high carbohydrate diet group but
there were no differences in the reduction of TC or
TO between the two groups. It is known that one of
mechanisms by which the HDL–C is increased is by
enhanced catabolism of very low-density lipoproteins
[12]. Accordingly, it is possible that a diet low in
240 Y. Miyashita et al. / Diabetes Research and Clinical Practice 65 (2004) 235–241
Fig. 5. Changes in adipose tissue distribution measured by computed tomography after low calorie diets for a month in low carbohydrate
diet group (䊉) and high carbohydrate diet group (䊊). (A and B) Show changes of visceral fat and V/S ratio. Data are shown as mean ±S.D.,
∗ P < 0.05.
carbohydrates could stimulate the catabolism of very
low-density lipoproteins. Another possibility is that
the activity of lipoprotein lipase might be improved,
accompanying with the increased insulin sensitivity
[13,14].
There were also differences in the effect on adi-
pose tissue distribution between the two groups. In
low carbohydrate diet group, the visceral fat area and
the V/S ratio were significantly decreased during diet,
but not in high carbohydrate diet group. As for the
mechanisms, there are at least two possible explana-
tions. The first is that the low carbohydrate diet could
stimulate growth hormone secretion from the pituitary
gland [15]. This could explain the different effects of
the two diets on visceral fat mass since it has previ-
ously been shown that the lipolytic activity induced by
growth hormone is higher in visceral fat compared to
subcutaneous fat [16,17]. Consequently, in this study,
the secretion of growth hormone might be enhanced
to a larger extent by the low carbohydrate diet com-
pared to the high carbohydrate diet. Another possibil-
ity is a lower insulin requirement of the low carbohy-
drate diet. Hyperinsulinemia is reported to be associ-
ated with visceral fat [1,2] and a high level of fasting
insulin is reported to predict visceral fat accumulation
[18]. In our study, there was a larger decrease of basal
IRI by the low carbohydrate diet compared to the high
carbohydrate diet. Accordingly, low insulin secretion
in low carbohydrate diet might be beneficial for re-
duction of visceral fat accumulation.
Bjorntorp and co-workers reported that an increased
flux of free fatty acids could cause insulin resistance
[19,20]. Consequently, the levels of free fatty acids
may be important factor during diet therapy. Free fatty
acids would be expected to increase during a low calo-
rie diet due to an increased fat mobilization. In our
study, the homeostasis model assessment-ratio in the
low carbohydrate diet is better compared to that in
the high carbohydrate diet. Hence, increased free fatty
acid levels during weight reduction by low calorie/low
carbohydrate diet did not deteriorate the insulin sensi-
tivity in these subjects. Furthermore, Reaven reported
that high carbohydrate intake would tend to increase
the risk of vascular complications [21,22], and high
carbohydrate diet is reported to increase blood glu-
cose, insulin, and TG levels and decrease HDL–C in
diabetes mellitus patients [9]. In agreement with this,
our data suggest that a high carbohydrate intake would
not always be beneficial. In our study, the amount of
total intake of fat in the low carbohydrate diet was
about 40 g per day, which is not considered to be an
excessive fat intake, and is equal to that of 1600 kcal in
a high carbohydrate diet that is widely recommended.
Consequently, our data suggest that the more favor-
able effect on metabolism induced by the low carbo-
hydrate diet compared to the high carbohydrate diet
would be not due to be over-intake of fat, but rather
restriction of carbohydrate.
It is known that monounsaturated fatty acids is
preferable to saturated fatty acids for the diet therapy
of type 2 diabetes mellitus patients [23,24]. Reaven
also reported that substituting monounsaturated fats
for carbohydrates might be advantageous in reducing
the long-term complications, particularly coronary
 Y. Miyashita et al. / Diabetes Research and Clinical Practice 65 (2004) 235–241
heart disease, in type 2 diabetes mellitus patients [9].
In our study, intake of monounsaturated fats was not
always high, but low carbohydrate diet was more
beneficial than high carbohydrate diet for glucose and
lipid metabolism in type 2 diabetes mellitus. Further
studies regarding fat composition are required.
In summary, it is concluded that for type 2 diabetes
mellitus patients with obesity, low carbohydrate con-
tent in the low calorie diet showed more favorable ef-
fects on reducing visceral fat, lower serum insulin lev-
els and improving serum lipid levels compared to an
iso-caloric high carbohydrate diet.
Acknowledgements
This study is supported partly by a fund from the
Meeting of Obesity and Nutritional Disturbance.
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