Nutrition 29 (2013) 1204–1208
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Nutrition
journal homepage: www.nutritionjrnl.com
Applied nutritional investigation
Vitamin D status and body fat measured by dual-energy X-ray absorptiometry
in a general population of Japanese children
Katsuyasu Kouda M.D., Ph.D. a, *, Harunobu Nakamura M.D., Ph.D. b, Yuki Fujita Ph.D. a,
Kumiko Ohara B.Sc. b, Masayuki Iki M.D., Ph.D. a
a
b
Department of Public Health, Kinki University Faculty of Medicine, Osaka-Sayama, Japan
Department of Health Promotion and Education, Graduate School of Human Development and Environment, Kobe University, Kobe, Japan
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 25 December 2012
Accepted 6 March 2013
Objective: For a general population of children, data on the relationship between vitamin D status
and adiposity are limited. The aim of this study was to assess the relationships between the serum
concentration of 25-hydroxyvitamin D (25-OH-D) and body fat variables measured by dual-energy
X-ray absorptiometry (DXA) in a general population of Japanese children, including underweight,
normal, and overweight children.
Methods: The source population comprised 521 fifth-grade children who attended either of the two
public schools in Hamamatsu, Japan. Total and regional body fat mass (FM) measured by DXA were
evaluated along with the serum concentration of 25-OH-D.
Results: We were able to analyze the FM and 25-OH-D data of 400 of the 521 children. Among boys,
significant inverse relationships were observed between serum vitamin D levels and body fat
variables (total FM, r ¼ 0.201; trunk FM, r ¼ 0.216; appendicular FM, r ¼ 0.187; P < 0.05 for all
values). Mean values of total FM and trunk FM in the vitamin D-deficient group (25-OH-D <50
nmol/L) were larger than those in the vitamin D-sufficient group (25-OH-D 75 nmol/L) after
adjusting for confounding factors, such as sedentary behavior (P < 0.05). No relationship was
observed between vitamin D status and FM among girls.
Conclusions: Vitamin D deficiency was associated with higher total and trunk adiposities in
a general population of Japanese children, particularly boys.
Ó 2013 Elsevier Inc. All rights reserved.
Keywords:
Adipose tissue
Children
DXA
Epidemiology
Vitamin D
Introduction
Epidemiologic evidence suggests that poor vitamin D status
may be involved in the etiology of chronic diseases such as
autoimmune diseases, type 2 diabetes, and cardiovascular disease
[1,2]. Furthermore, a mechanistic role for vitamin D in the regulation of adiposity and body weight has been suggested [3]. An
inverse association between serum 25-hydroxyvitamin D
(25-OH-D) and body fat measured by dual-energy X-ray absorptiometry (DXA) has been reported in epidemiologic studies of
adulthood [4–6]. A recent double-blind randomized clinical trial
KK and MI designed the research; KK, HN, YF, KO, and MI conducted the
research; KK, HN, and KO provided essential materials; KK and YF analyzed data;
KK, YF, and HN wrote the manuscript. All authors approved the submitted
version of the manuscript.
* Corresponding author. Tel.: þ81-72-365-5559; fax: þ81-72-367-8262.
E-mail address: [email protected] (K. Kouda).
0899-9007/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.nut.2013.03.010
showed that calcium and vitamin D supplementation reduced
visceral adipose tissue in overweight and obese adults [7].
In childhood, several studies have reported a relationship
between vitamin D status and body weight. A study of
adolescents in Boston reported a negative relationship between
25-OH-D and body mass index (BMI) [8]. Another study of
postmenarcheal girls in Ohio also showed a negative correlation
between body weight and serum 25-OH-D levels [9]. A study of
New Zealand children revealed lower 25-OH-D concentrations in
obese children compared with those of normal weight [10].
Furthermore, data obtained from a multiracial U.S. adolescent
population showed an inverse relationship between serum
25-OH-D levels and body weight [11].
However, given that BMI and body weight reflect both lean
mass and fat mass (FM), they are insufficient indexes of adiposity
[12]. Thus, studies that directly evaluate body fat in children are
needed. Using bioelectrical impedance analysis (BIA), Alemzadeh
et al reported a negative relationship between serum 25-OH-D
K. Kouda et al. / Nutrition 29 (2013) 1204–1208
and FM among obese children and adolescents [13]. ElizondoMontemayor et al also reported an inverse association between
serum 25-OH-D concentration and body fat measured by BIA
among obese and non-obese children [14]. However, data from
studies using a more precise technique such as DXA in a population of children are limited. Lender et al reported an inverse
relationship between 25-OH-D and body fat in obese adolescents
in the United States [15]. In contrast, Weng et al reported that
25-OH-D status was not associated with FM in healthy-weight
children and adolescents (BMIs within the 5th to 95th percentiles) in Philadelphia [16].
For a general population of children, including underweight,
normal, and overweight children, data on the relationship
between vitamin D status and body fat measured by DXA are
lacking. To this end, we investigated the relationships between
the serum concentration of 25-OH-D and fat variables measured
by DXA in a general population of Japanese children.
Methods
Study population
The source population comprised all fifth-grade school children attending
one of the two public schools, Aritama Elementary School (November 2010 and
December 2011) or Sekishi Elementary School (December 2010 and November
2011) in Hamamatsu, as previously described (521 children, 268 boys and 253
girls) [17]. Given that most children who lived in the present study area attended
one of these two schools, they were included in the general population of
Hamamatsu, Japan. Parents of the children received printed information on study
procedures, including the DXA radiation dose for the children, and provided
written informed consent before participant enrollment. Children were protected
rights to freedom of nonparticipation in the study. Blood samples (for 25-OH-D
determination) and complete information on body composition, sedentary
behavior, and pubic hair appearance were obtained for 400 of the 521 children
(197 boys and 203 girls; 76.8% of the source population). We analyzed the 400
children. The study was performed in accordance with the ethical standards set
forth in the 1964 Declaration of Helsinki, and was approved by the Ethics
Committee of the Kinki University Faculty of Medicine.
Measurement of body composition components
Body composition components were measured using a single DXA scanner
(QDR-4500A; Hologic Inc., Bedford, MA, USA) in a mobile test room, which was
brought to the schools. Participants wore light clothing without metal objects
during the measurements. Both the total and regional components of body
composition were measured as described previously [18]. Measurements of both
arms, both legs, and the head were separated from trunk measurements using
computer-generated default lines with manual adjustment in the anterior view
planogram. An experienced medical radiology technician handled the adjustment of all subjects using specific anatomical landmarks (chin, center of the
glenohumeral joint, and femoral neck axis). Total, trunk, and appendicular FM
were individually evaluated. Appendicular FM was calculated as the sum of FM
from both arms and legs. FM was evaluated using a fat volume (kg) and a heightnormalized fat volume called FM index (kg/m2) [19]. The FM index was used to
avoid ambiguities of body fat as a percentage of body weight, and is calculated as
FM (kg) divided by height squared (m2).
Measurement of serum 25-OH-D levels
A non-fasting blood specimen was drawnat the same session as the
measurement of body composition components. The serum 25-OH-D concentration was determined using a radioimmunoassay (25-hydroxyvitamin D 125I
RIA Kit; DiaSorin Inc., Stillwater, MN, USA).The intra-assay and inter-assay variances were 5.2% to 9.5% and 6.3% to 10.8%, respectively. Vitamin D status was
classified into one of the following groups: vitamin D-sufficient (75 nmol/L),
vitamin D-insufficient (50, <75 nmol/L), and vitamin D-deficient (<50 nmol/L)
[20].
Other variables
Sedentary behavior, such as media use, and the first appearance of pubic hair
were determined from self-reported responses to a questionnaire. Body weight,
height, and waist circumference were assessed at the same session as the other
measurements. BMI (kg/m2) was calculated as weight (kg) divided by height
1205
squared (m2). The international BMI cut-offs for child overweight (based on the
adult BMI cut-offs of 25 kg/m2) were used [21]. Similarly, the international BMI
cut-offs for child underweight (based on the adult BMI cut-offs of 18.5 kg/m2)
were used [22]. Blood pressure and serum levels of low-density and high-density
lipoprotein cholesterol also were measured at the same session.
Statistical analysis
Either the unpaired t test or the Mann-Whitney U-test was used to compare
characteristics between boys and girls. Pearson’s correlation test was used to
examine the relationships between 25-OH-D concentration and body fat variables, such as total FM, trunk FM, and appendicular FM. The adjusted mean values
for body fat variables stratified by 25-OH-D status were calculated using the
general linear model after adjusting for sedentary behavior and pubic hair
appearance. Analysis of variance or analysis of covariance was used to analyze the
differences between the crude and adjusted means of body fat variables stratified
by 25-OH-D status. Simple or multiple linear regression analysis was used for
trend tests of the crude and adjusted means. The Bonferroni method was used to
compare the mean values of fat variables between the vitamin D-deficient and
vitamin D-sufficient groups. P < 0.05 was considered statistically significant. Data
were analyzed using the SPSS Statistics Desktop for Japan, Version 20.0 (IBM
Japan, Ltd., Tokyo, Japan).
Results
Subject characteristics are presented in Table 1. The mean age
of children was 11.2 y. Subjects included 38 (9.5%) overweight
children and 56 (14%) underweight children. Height and bone
mineral content were significantly higher in girls than in boys.
Table 1
Characteristics of the study population
Characteristics
Boys (n ¼ 197) Girls (n ¼ 203) P-value*
Age (years)
Height (cm)
Weight (kg)
Body mass index (kg/m2)
Waist circumference (cm)
Overweighty, N (%)
Underweighty, N (%)
Bone mineral content (kg)
Fat-free soft tissue mass (kg)
Total FM (kg)
Total FM index (kg/m2)
Trunk FM (kg)
Trunk FM index (kg/m2)
Appendicular FM (kg)
Appendicular FM index (kg/m2)
Systolic blood pressure (mm Hg)
Diastolic blood pressure (mm Hg)
High-density lipoprotein
cholesterol (mmol/L)
Low-density lipoprotein
cholesterol (mmol/L)
Sedentary behavior
(media use), N (%)
<1 h/d
1–2 h/d
2–3 h/d
3–4 h/d
4–5 h/d
Pubic hair appearance, N (%)
No appearance
Grade 5
Grade 4
Grade 3
25-hydroxyvitamin D (nmol/L)
11.2 0.3
141.5 6.2
34.9 7.3
17.3 2.6
63.2 7.7
25 (12.7)
27 (13.7)
0.95 0.14
27.7 4.3
7.18 3.67
3.54 1.67
2.26 1.55
1.11 0.71
4.12 2.11
2.03 0.97
105.6 10.6
58.1 7.4
1.97 0.42
11.2 0.3
143.3 7.0
35.2 7.0
17.0 2.3
62.4 6.4
13 (6.4)
29 (14.3)
0.99 0.19
27.4 4.3
7.71 3.18
3.71 1.33
2.47 1.31
1.18 0.56
4.48 1.88
2.16 0.79
106.6 10.2
59.6 8.2
1.85 0.37
0.413
0.007
0.697
0.221
0.293
0.032
0.867
0.024
0.480
0.125
0.261
0.147
0.244
0.073
0.161
0.343
0.056
0.003
2.41 0.56
2.51 0.52
0.068
0.857
42 (21.3)
97 (49.2)
32 (16.2)
18 (9.1)
8 (4.1)
47 (23.2)
90 (44.3)
50 (24.6)
13 (6.4)
3 (1.5)
187 (94.9)
10 (5.1)
0 (0.0)
0 (0.0)
83.6 20.6
135 (66.5)
55 (27.1)
12 (5.9)
1 (0.5)
73.8 18.7
< 0.001
< 0.001
FM, fat mass; N, number
Values represent mean SD, or N (percentage)
The FM index was calculated as FM divided by height squared
* The unpaired t test or the Mann-Whitney U test was performed.
y
The international cut-offs of body mass index for child overweight and
underweight were used.
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K. Kouda et al. / Nutrition 29 (2013) 1204–1208
Table 2
Relationships between serum 25-hydroxyvitamin D levels and body fat variables
Total FM (kg)
Total FM index (kg/m2)
Trunk FM (kg)
Trunk FM index (kg/m2)
Appendicular FM (kg)
Appendicular FM
index (kg/m2)
Boys (n ¼ 197)
Girls (n ¼203)
r*
P-value
r*
P-value
0.201
0.170
0.216
0.196
0.187
0.154
0.005
0.017
0.002
0.006
0.008
0.031
0.001
0.019
0.013
0.000
0.005
0.025
0.985
0.790
0.849
0.998
0.940
0.722
FM, fat mass
The FM index was calculated as FM divided by height squared
* Pearson’s correlation test was used.
Serum high-density lipoprotein cholesterol and serum 25-OH-D
levels were significantly higher in boys than in girls.
Table 2 shows the relationships between serum 25-OH-D levels
and body fat variables. In boys, significant inverse relationships
were observed between serum vitamin D levels and body fat
variables. However, no significant relationship was observed
between serum vitamin D levels and body fat variables in girls.
Tables 3 and 4 show the crude and adjusted means of body fat
variables stratified by serum 25-OH-D status. Boys exhibited
a significant decrease in crude means of FM with increasing
serum 25-OH-D levels. After adjusting for confounding factors,
such as sedentary behavior, the decrease in FM continued to
exhibit an association with the increase in serum 25-OH-D levels.
Crude and adjusted means of total FM, trunk FM, and trunk FM
index in the vitamin D-deficient group were significantly larger
than the mean values in the vitamin D-sufficient group. Girls did
not exhibit a significant trend or difference between the groups.
Discussion
This is the first report of an association between vitamin D
status and adiposity measured by DXA in a general population of
children. The present cross-sectional and observational study
showed that poor vitamin D status was associated with higher
total and central adiposities. Specifically, the mean values of
body fat variables were larger in boys who were vitamin Ddeficient than in boys who were vitamin D-sufficient. In contrast,
no significant relationship was observed between serum vitamin
D levels and body fat variables in girls. These results from
a general population provide additional evidence supporting the
relationship between vitamin D and adiposity in children.
Several studies have reported an inverse relationship
between vitamin D status and childhood body weight [8–11].
However, information on the relationship between vitamin D
status and precisely measured adiposity in the general population is lacking. Lender et al reported an inverse relationship
between 25-OH-D and body fat measured by DXA in obese
adolescents who were screened for a weight loss trial in the
United States [15]. Weng et al reported no association between
25-OH-D status and body fat measured by DXA in
healthy-weight children and adolescents with BMIs within the
5th to 95th percentiles in Philadelphia [16]. In the present study,
subjects comprised a general population of Japanese children
and included not only healthy-weight children but also overweight children with BMIs >20.55 kg/m2in boys and >20.74
kg/m2in girls [21], and underweight children with BMIs <14.97
kg/m2in boys and<15.05 kg/m2in girls [22]. Consequently, we
observed significant inverse relationships between serum
vitamin D levels and body fat variables in boys.
No significant relationship was observed between vitamin D
status and FM in the girls in the present study. Because previous
studies that performed a direct evaluation of body fat did not
analyze gender differences in the relationship [13–16], we are
unable to compare our results with theirs. However, the gender
differences in the relationship between adiposity and vitamin D
may be explained by a difference in regional fat deposit patterns
between boys and girls. Females store energy in the subcutaneous depot when energy is surfeit, and carry more fat subcutaneously [23]. In the present study, appendicular fat, which
consists of subcutaneous fat, was higher in girls than in boys
(Table 1). Many studies indicate that males have more visceral
adipose tissue than females throughout the ages of 5 to 25 y [24].
A recent randomized controlled trial showed a selective reduction in visceral adipose tissue following calcium and vitamin D
supplementation [7]. Thus, vitamin D status may be better
Table 3
Mean values of body fat variables in boys
25-hydroxyvitamin D status
<50 nmol/L (n ¼ 9)
Crude mean
Total FM (kg)
Total FM index (kg/m2)
Trunk FM (kg)
Trunk FM index (kg/m2)
Appendicular FM (kg)
Appendicular FM index (kg/m2)
Adjusted meanx
Total FM (kg)
Total FM index (kg/m2)
Trunk FM (kg)
Trunk FM index (kg/m2)
Appendicular FM (kg)
Appendicular FM index (kg/m2)
50 , <75 nmol/L (n ¼ 67)
P-value for difference*
P-value for trendy
75 nmol/L (n ¼ 121)
9.63
4.52
3.45
1.61
5.39
2.53
1.90z
0.86
0.91z
0.42z
0.97
0.44
7.86
3.80
2.52
1.22
4.53
2.19
0.48
0.22
0.21
0.10
0.27
0.12
6.62
3.32
2.03
1.01
3.80
1.91
0.29
0.13
0.11
0.05
0.17
0.08
0.010
0.032
0.007
0.016
0.014
0.045
0.003
0.009
0.002
0.005
0.003
0.013
9.80
4.58
3.51
1.63
5.48
2.56
1.19z
0.55
0.50z
0.23z
0.69
0.32
7.72
3.75
2.46
1.19
4.45
2.16
0.44
0.20
0.19
0.09
0.25
0.12
6.69
3.35
2.06
1.02
3.84
1.92
0.33
0.15
0.14
0.06
0.19
0.09
0.015
0.045
0.009
0.021
0.022
0.065
0.005
0.016
0.004
0.009
0.006
0.021
FM, fat mass
The FM index was calculated as FM divided by height squared
Values represent mean standard error
* Analysis of variance or analysis of covariance was used to assess the differences between groups.
y
Simple or multiple linear regression analysis was used for trend tests.
z
P < 0.05 compared with the vitamin D-sufficient group (75 nmol/L) using the Bonferroni method.
x
Adjusted for sedentary behavior and pubic hair appearance.
K. Kouda et al. / Nutrition 29 (2013) 1204–1208
1207
Table 4
Mean values of body fat variables in girls
25-hydroxyvitamin D status
<50 nmol/L (n ¼ 17)
Crude mean
Total FM (kg)
Total FM index (kg/m2)
Trunk FM (kg)
Trunk FM index (kg/m2)
Appendicular FM (kg)
Appendicular FM index (kg/m2)
Adjusted meanz
Total FM (kg)
Total FM index (kg/m2)
Trunk FM (kg)
Trunk FM index (kg/m2)
Appendicular FM (kg)
Appendicular FM index (kg/m2)
50, <75 nmol/L (n ¼ 105)
P-value for difference*
P-value for trendy
75 nmol/L (n ¼ 81)
6.99
3.37
2.15
1.04
4.09
1.97
0.51
0.26
0.21
0.11
0.29
0.15
7.70
3.69
2.48
1.18
4.47
2.14
0.31
0.13
0.13
0.06
0.18
0.08
7.87
3.81
2.52
1.22
4.59
2.22
0.37
0.15
0.15
0.06
0.22
0.09
0.586
0.459
0.556
0.479
0.607
0.477
0.370
0.243
0.395
0.294
0.362
0.239
6.82
3.30
2.09
1.01
3.98
1.93
0.76
0.32
0.31
0.13
0.45
0.19
7.68
3.69
2.47
1.18
4.45
2.14
0.30
0.13
0.13
0.05
0.18
0.08
7.94
3.83
2.55
1.23
4.62
2.23
0.35
0.15
0.14
0.06
0.21
0.09
0.402
0.313
0.398
0.339
0.415
0.326
0.222
0.155
0.246
0.190
0.219
0.153
FM, fat mass
The FM index was calculated as FM divided by height squared
Values represent mean standard error
* Analysis of variance or analysis of covariance was used to assess the differences between groups.
y
Simple or multiple linear regression analysis was used for trend tests.
z
Adjusted for sedentary behavior and pubic hair appearance.
related to visceral adipose tissue than subcutaneous adipose
tissue. The lack of association between vitamin D status and FM
in girls may be explained by the lower amounts of visceral
adipose tissue in girls. Similarly in boys, the relationship
between vitamin D and trunk fat, which consists of visceral and
subcutaneous fat, appears to be stronger than that between
vitamin D and appendicular fat (Table 2).
This study has several limitations worth noting. First, we
could not evaluate an association between visceral adipose tissue
and vitamin D status independently of trunk fat, because DXA
does not specifically measure visceral fat. Further studies
involving visceral fat measurements by computed tomography
and magnetic resonance imaging are needed. Second, the study
was cross-sectional and observational in design, and we did not
determine whether poor vitamin D status was involved in the
etiology of increased childhood adiposity. Third, although the
association between FM and vitamin D is confounded by several
factors, we could not investigate the relationship by considering
other relevant factors, such as biochemical parameters, dietary
intake, and sunlight exposure. Obese children consume
unhealthy high-caloric foods, which are low in mineral and
vitamin content [25]. The contributions of dietary quality and
supplement intake to the relationship between FM and vitamin
D status remain unknown. On the other hand, sedentary
behavior is also a confounding factor. Given that obese children
are usually sedentary, they may have less exposure to sunlight
and may therefore suffer from hypovitaminosis D. Therefore, we
analyzed the association between adipose tissue and vitamin D
status after adjusting for sedentary behavior. However, data on
sunlight exposure will be needed to more clearly interpret the
association. Fourth, data were obtained from only one prefecture
in Japan rather than from the entire country. Additionally, the
study population was 76.8% of the source population. However,
the mean body height and weight of the study population are
similar to those reported in a Japanese national survey (Table 1).
Standard growth charts for the height and weight of Japanese
children aged 11.2 y show mean heights of 142.5 cm and 144 cm
and mean weights of 36.6 kg and 37.3 kg for boys and girls,
respectively [26]. Therefore, the study population is considered
a general population of Japanese children aged 11 y. Fifth, the
cut-off values for 25-OH-D (deficiency, insufficiency, and
sufficiency) used in the present study are somewhat controversial, and there is only a weak rationale for the normal range,
particularly in childhood [20,27,28]. Thus, strong evidence does
not yet exist. Epidemiologic studies, such as randomized
controlled studies, using a general population of children will be
needed to further support the role of vitamin D in regulating
adiposity.
Conclusion
The present cross-sectional study showed inverse relationships between serum vitamin D levels and body fat variables in
a general population of Japanese boys. Poor vitamin D status was
associated with higher total and central adiposities. In girls, no
significant relationship was observed between serum vitamin
D levels and adiposity.
Acknowledgments
The authors would like to thank the teaching staff at Aritama
Elementary School and Sekishi Elementary School and Dr.
Toshiko Okamoto for their support. This work was supported by
Grants-in-Aid for Scientific Research (#21657068 and
#22370092) from the Japan Society for the Promotion of Science.
The authors declared no conflict of interest.
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