Open Access

Higher visceral fat area increases the risk of vitamin D insufficiency and deficiency in Chinese adults

  • Meilin Zhang1,
  • Ping Li1,
  • Yufeng Zhu1,
  • Hong Chang1, 2,
  • Xuan Wang1,
  • Weiqiao Liu3,
  • Yuwen Zhang3 and
  • Guowei Huang1Email author
Nutrition & Metabolism201512:50

https://doi.org/10.1186/s12986-015-0046-x

Received: 6 July 2015

Accepted: 19 November 2015

Published: 25 November 2015

Abstract

Background

Visceral fat area (VFA), a novel sex-specific index for visceral fat obesity (VFO) might play a major role in the development of vitamin D deficiency. However, the association between VFA and vitamin D insufficiency and deficiency in Chinese population is less clear. The aim of this study was to explore the population-level association between VFA and vitamin D insufficiency and deficiency among Chinese men and women.

Methods

This cross-sectional study involved 1105 adults aged 20–70 years living in Tianjin who were randomly selected and medically examined. All subjects underwent the bioelectrical impedance analysis (BIA) method to estimate the VFA. Serum 25-hydroxyvitamin D3 (25(OH) D3) level was assayed by the high-performance liquid chromatography (HPLC) method and defined insufficiency and deficiency following recommended cutoffs. The association between VFA and vitamin D insufficiency and deficiency was estimated using binary regression analysis.

Results

The total prevalence of vitamin D insufficiency (25(OH) D3: 20–29 μg/L) and deficiency (25(OH) D3 < 20 μg/L) were 26.60 % and 24.89 %, respectively. Significant negative association was observed for VFA with serum 25(OH) D3 levels in men and pre-menopausal women (P < 0.05), not in post-menopausal women (P > 0.05). Moreover, increased VFA was observed to be associated with higher vitamin D insufficiency or deficiency risk with a positive dose–response trend (P for trend < 0.001). As compared to individuals with the lowest VFA, those who had the highest VFA were at 4.9-fold risk of vitamin D insufficiency and deficiency [95 % confidence interval (95 % CI): 1.792–13.365] in men and 1.8-fold risk of vitamin D insufficiency and deficiency (95 % CI: 1.051–3.210) in pre-menopausal women, but not in post-menopausal women [odds ratio (OR) (95 % CI): 2.326(0.903–5.991)].

Conclusions

These results suggest that higher VFA increases the risk of vitamin D insufficiency and deficiency in men and pre-menopausal women, but not in post-menopausal women. VFA is a better and convenience surrogate marker for visceral adipose measurement and could be used in identifying the risk of vitamin D insufficiency and deficiency in routine health examination.

Keywords

Visceral fat area 25-hydroxyvitamin D3 Vitamin D deficiency Visceral fat obesity

Background

Vitamin D deficiency is now being recognized as a major global public health problem [13]. Approximately 1 billion people worldwide have vitamin D deficiency [4]. In China, vitamin D deficiency is common in the middle-aged and elderly population. The prevalence of vitamin D deficiency was 69.2 % in Beijing and Shanghai [5], and the prevalence of vitamin D deficiency was 75.2 % in the northwestern inland of China [6].

Traditional roles of vitamin D lie within the musculoskeletal system, maintaining calcium homoeostasis and bone metabolism. In recent years, new functional roles of vitamin D have emerged linking the fat-soluble vitamin to various non-communicable diseases. The consequences of vitamin D deficiency include poor bone development and health as well as increase risk of many chronic diseases including insulin resistance, diabetes and cardiovascular disease [7], which is also commonly linked with obesity and visceral fat obesity (VFO).

Anthropometric indices such as body mass index (BMI) have been used widely in the previous studies examining the relationship between obesity and vitamin D [8, 9]. In particular, VFO compared with overall obesity might play a major role in the development of vitamin D deficiency. Therefore, estimating visceral fat accumulation is important to identify individuals at high risk for vitamin D deficiency. Their inability to distinguish visceral fat precludes their ability to accurately assess abdominal fat accumulation. Because fat accumulation in different areas represents different risk for metabolic disorders and visceral adipose tissue may be unique [10], we sought to evaluate visceral fat. Conventionally, the simplest and most widely used method of assessing visceral fat accumulation is measuring the waist circumference (WC) [11]. Although WC is recognized as an independent and powerful risk factor for vitamin D deficiency, there might be substantial variations in the visceral fat amount among persons with a similar WC because WC itself performs poorly in discriminating between visceral and subcutaneous fat. Therefore, it is possible that subjects with a normal WC may be more prone to vitamin D deficiency if they have centrally located body fat. Many sophisticated methods such as dual-energy x-ray absorptiometry (DEXA), computed tomography (CT) and magnetic resonance imaging (MRI) have been developed to provide more precise estimates of the location and amount of adipose tissue in various body regions [12]. However, DEXA, CT and MRI are impractical for screening general population, since they require expensive and specialized equipment, and exposure to radiation. Studies have compared the general usage of bioelectrical impedance analysis (BIA) with one of these more established methods (CT, MRI or DEXA). BIA has been shown to accurately predict DXEA-derived percentage body fat (PBF) in the Chinese population (r = 0.89, P < 0.05) [13]. VFA measured by BIA correlated significantly with that acquired by CT (r = 0.992 for VFA, using data from the Biospace of 332 patients) [14]. Although BIA is not considered a “gold standard”, BIA has been considered a valid alternative for measuring body fat in large studies or clinical practice [15], which has also been validated against reference methods [13, 14].

Visceral fat area (VFA), a novel sex-specific index for VFO, has been proposed recently. One study has examined the association of 25-hydroxyvitamin D3 (25(OH) D3) level and VFO in Chinese men and discovered serum 25(OH)D3 levels were inversely associated with VFA [16]. To our knowledge, serum 25(OH) D3 levels and the distribution of abdominal fat are known to be distinctive between men and women [1719], as well as between pre-memopausal and post-memopausal women. However, the significance of association between VFA and vitamin D insufficiency and deficiency in the Chinese population is less clear. In the present study, a simple method for the measurement of visceral fat accumulation using BIA [20] was performed to explore the population-level association between VFA and vitamin D insufficiency and deficiency in Chinese men and women.

Methods

Subjects

This overall population includes 1130 subjects aged 20–70 years coming to the Health Examination Center of Heping District in Tianjin, China for routine health checkup during November to December in 2013, were enrolled. 1105 subjects were included for analysis according to the following inclusion and exclusion criteria. Inclusion criteria were as follows: 1) aged 20–70 years, 2) written informed consent, 3) willingness to take part in the examination and willingness to provide blood samples. Exclusion criteria were as follows: 1) individuals whose medical data were incomplete (n = 10), 2) individuals who took diuretics (n = 3), 3) individuals who undergone hormone replacement therapy (n = 2), 4) individuals with chronic kidney disease (n = 3), 5) individuals with presence of tumor, infectious diseases or psychiatric disease (n = 3), 6) individuals with severe disability or occurrence of bone fracture within the past six months (n = 2); 7) individuals who have had stents or with history of cardiovascular disease (n = 2).

The study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of Tianjin Medical University. All study participants provided written informed consent prior to enrollment.

Body fat measurements

Body fat measurements, consisting of BMI, WC, waist-to-hip ratio (WHR), fat mass (FM), free fat mass (FFM), PBF and VFA were estimated by the BIA method (Inbody 720 Body Composition Analyzer, Korean).

Anthropometric and biochemical assessments

Systolic blood pressure (SBP) and diastolic blood pressure (DBP) were measured by trained nurses with a mercury sphygmomanometer on the right arm of the subjects in a comfortable siting position after 5 -min rest. After 10-h overnight fasting, blood samples were collected from all subjects to measure serum 25(OH) D3 levels as well as other biochemical parameters. Fasting plasma glucose (FPG) was measured by the glucose oxidase method. Lipid profiles, including total cholesterol (TC) and triglycerides (TG) were determined using the standard enzymatic methods, while low-density lipoprotein cholesterol (LDL-c) and high-density lipoprotein cholesterol (HDL-c) were determined by the direct assay method. All of the above measurements were carried out on a Hitachi 7600–120 auto-analyzer (Tokyo, Japan). Total serum 25(OH) D3 level was assayed by the high-performance liquid chromatography (HPLC) method.

Definition of terms

Obesity was defined as a BMI value exceeding 28 kg/m2 [21]. VFO was defined as WC ≥ 90 cm for men or ≥80 cm for women. Or VFO was defined as a VFA exceeding 130 cm2 in men and 100 cm2 in women [22]. Vitamin D status was defined as follows: A serum level of 25(OH) D3 < 20 μg/L is considered to be vitamin D deficiency, whereas a level 20–29 μg/L is insufficient, and to maximize vitamin D’s effect for health, 25(OH) D3 should be ≥30 μg/L [23].

Lifestyle factors

Smoking behavior, drinking behavior, current daily time spent outdoors, physical activity, menopausal status and vitamin D supplement intake were collected using self-administered questionnaires. The current time spent outdoors (h/d) was used as an indicator for sunshine time. A woman was considered post-menopausal if she reported menses had ceased for 1 year or more, and age at menopause was self-reported as previously reported.

Statistical analysis

According to the sample size, a normal distribution was tested by the Kolmogorov-Smirnov test with the Lilliefors correction for men and women. Normally distributed variables were presented as the mean ± standard deviation, whereas skewed variables were presented as the median (interquartile range). Because of significant sex difference in the amount of total body fat, fat distribution and lifestyle factors, we performed sex-stratified analyses. For continuous variables, the independent sample t-test and the Wilcoxon rank-sum test were used for between-group comparisons of normally distributed and skewed data, respectively. Comparative analyses of categorical variables were carried out using a Chi-square test. Each participant was categorized into one of four subgroups depending on their total VFA. To compare variables between these subgroups, one-way analysis of variance (ANOVA) followed by Scheffé post hoc test or Mann–Whitney U test were used where appropriate. Partial correlation analyses between serum 25(OH) D3 and other variables were adjusted for age. Binary logistic regression was performed to examine the association between body fatness indices and vitamin D insufficiency and deficiency. Data were analyzed using SPSS (Chicago, IL) version 13.0 statistical software. P value less than 0.05 was considered to indicate a statistically significant difference.

Results

Descriptive characteristics of the study population

The characteristics of the study population were shown in Table 1. Overall, the prevalence of visceral fat obesity was higher than obesity. It was showed that the men had a higher age, WHR, BMI, WC, FM, VFA, FFM, SBP, DBP, sunshine time, higher levels of TG, LDL-c, FPG and lower levels of PBF, 25(OH) D3 and HDL-c. But there was no difference in TC and vitamin D supplementation intake between the men and women. The prevalence of obesity, visceral fat obesity and vitamin D deficiency in men was higher than in the women, whereas the prevalence of vitamin D insufficiency in men was lower than in the women.
Table 1

Descriptive characteristics of the study population

Characteristics

Total

Men

Women

P-valuea

n

1105

257

848

 

Age, y

43.82 ± 12.15

45.44 ± 12.18

43.33 ± 12.11

0.015

Body mass index, kg/m2

23.67 ± 3.37

26.18 ± 3.39

22.90 ± 2.97

<0.001

Waist circumference, cm

82.79 ± 9.08

90.42 ± 8.57

80.48 ± 7.90

<0.001

Waist-to- hip ratio

0.87 ± 0.05

0.91 ± 0.04

0.84 ± 0.04

<0.001

Fat mass, kg

20.13 ± 6.06

21.45 ± 6.91

19.73 ± 5.72

<0.001

Free fat mass, kg

44.66 ± 8.96

58.41 ± 6.56

40.50 ± 4.11

<0.001

Percentage body fat, %

30.89 ± 6.06

26.35 ± 5.57

32.27 ± 5.51

<0.001

Visceral fat area, cm2

87.30 ± 35.44

116.13 ± 34.87

78.56 ± 30.68

<0.001

Systolic blood pressure, mmHg

113.79 ± 15.72

120.54 ± 12.72

111.07 ± 16.01

<0.001

Diastolic blood pressure, mmHg

75.52 ± 10.06

80.30 ± 9.34

73.59 ± 9.70

<0.001

Total cholesterol, mmol/L

4.98 ± 0.98

5.03 ± 0.95

4.97 ± 1.00

bNS

Triglycerides, mmol/L

1.03(0.73–1.51)

1.41(0.99–2.00)

0.95(0.69–1.36)

<0.001

High-density lipoprotein cholesterol, mmol/L

1.33 ± 0.28

1.16 ± 0.21

1.38 ± 0.28

<0.001

Low-density lipoprotein cholesterol, mmol/L

2.96 ± 0.80

3.10 ± 0.76

2.92 ± 0.82

0.001

Fasting plasma glucose, mmol/L

5.73 ± 1.03

5.96 ± 1.28

5.66 ± 0.92

<0.001

25(OH)D3, μg/L

36.46 ± 24.70

33.26 ± 19.80

37.44 ± 25.94

0.018

Smoking, % yes

11.86

42.80

2.48

<0.001

Drinking, % yes

38.82

70.04

29.36

<0.001

Doing exercise, % yes

46.06

64.98

40.33

<0.001

Sunshine time, h/day

0.5(0.0,1.0)

1.0(0.0,2.0)

0.5(0.0,1.0)

<0.001

Vitamin D supplement users, % yes

2.26

2.33

2.24

bNS

Obesity, %

13.76

29.18

9.08

<0.001

Visceral fat obesity, %

    

 Men: WC ≥90 cm; women: WC ≥ 80 cm

44.71

50.58

42.92

0.031

 Men: VFA ≥130 cm2; women: VFA ≥ 100 cm2

23.53

35.40

19.92

<0.001

25(OH)D3 status*

    

 Vitamin D insufficiency, %

26.60

18.68

29.00

0.001

 Vitamin D deficiency, %

24.89

33.46

22.29

<0.001

Values are percentages for categorical variables, means ± SDs for continuous variables with a normal distribution, or medians (95 % ranges) for continuous variables with a skewed distribution

Abbreviations: WC, waist circumference; VFA, visceral fat area; 25(OH)D3, 25-hydroxyvitamin D

aComparison among men and women

bNS = no significant at p value > .05

*25(OH)D3 status was defined as follows: A serum level of 25(OH) D3 < 20 μg/L is considered to be vitamin D deficiency, whereas a level 20–29 μg/L is insufficient

Characteristics of the study population according to the quartiles of VFA

The study subjects were also divided into four groups according to the quartiles of VFA in men and women. The analysis revealed a increasing trend in VFA that accompanied increases in BMI, WC, WHR, FM, FFM, PBF and TG in both genders, decreases in 25(OH)D3 in men and pre-menopausal women (Table 2, Table 3). Intergroup comparisons revealed that the Q2, Q3 and Q4 groups had significantly lower 25(OH) D3 than the Q1 group in men (Table 2), whereas the Q4 groups had significantly lower 25(OH) D3 than the Q2 group and Q1 group in pre-menopausal women (Table 3).
Table 2

Characteristics of the study population according to quartiles of visceral fat area levels in men

 

Quartiles of visceral fat area (cm2)

P-valuea

 

Q1 (<89.95)

Q2 (89.95–115.72)

Q3 (115.72–140.46)

Q4 (≥140.46)

 

n

64

65

64

64

 

Age, y

42.36 ± 12.69

45.29 ± 12.03

46.92 ± 12.06

47.17 ± 11.58

bNS

Body mass index, kg/m2

22.87 ± 2.23

25.59 ± 2.21#

26.80 ± 2.51# &

29.45 ± 2.77# & $

0.000

Waist circumference, cm

81.28 ± 5.58

88.36 ± 4.93#

92.48 ± 5.50# &

99.57 ± 5.83# & $

0.000

Waist-to-hip ratio

0.86 ± 0.03

0.90 ± 0.02#

0.92 ± 0.02# &

0.95 ± 0.02# & $

0.000

Fat mass, kg

14.08 ± 3.52

19.90 ± 3.67#

23.35 ± 4.97# &

28.51 ± 5.64# & $

0.000

Free fat mass, kg

55.38 ± 6.43

57.40 ± 6.06#

58.17 ± 5.60# &

62.75 ± 5.93# & $

0.000

Percentage body fat, %

20.14 ± 3.63

25.68 ± 3.39#

28.50 ± 4.28# &

31.08 ± 4.02# & $

0.000

Systolic blood pressure, mmHg

118.89 ± 11.35

121.78 ± 12.12

118.41 ± 11.35

122.93 ± 14.70

bNS

Diastolic blood pressure, mmHg

78.19 ± 7.57

80.22 ± 10.05

80.57 ± 8.16

81.95 ± 10.95

bNS

Total cholesterol, mmol/L

4.71 ± 0.78

4.93 ± 1.08

5.17 ± 0.90#

5.31 ± 0.90# &

0.001

Triglycerides, mmol/L

0.99(0.72–1.46)

1.38(0.94–2.10)#

1.53(1.22–2.11)#

1.69(1.26–2.18)#

0.036

High-density lipoprotein cholesterol, mmol/L

1.22 ± 0.23

1.14 ± 0.21

1.13 ± 0.21

1.15 ± 0.18

bNS

Low-density lipoprotein cholesterol, mmol/L

2.85 ± 0.66

2.91 ± 0.68

3.24 ± 0.76# &

3.44 ± 0.79# &

0.000

Fasting plasma glucose, mmol/L

5.63 ± 0.95

6.10 ± 1.36

5.99 ± 1.13

6.13 ± 1.58

bNS

25(OH)D3, μg/L

42.30 ± 19.59

34.90 ± 20.93#

30.80 ± 20.15#

25.01 ± 14.05# &

0.000

Smoking, % yes

28.13

41.54#

43.75#

57.81#

0.009

Drinking, % yes

57.81

73.85

71.88

76.56

bNS

Doing exercise, % yes

51.56

67.69

67.19

73.44

bNS

Sunshine time, h/day

1.00(0.50–1.00)

1.00(0.00–3.00)

0.50(0.00–1.50)

1.00(0.00–2.00)

bNS

Vitamin D supplement users, % yes

1.56

0.00

6.25

1.56

bNS

Values are percentages for categorical variables, means ± SDs for continuous variables with a normal distribution, or medians (95 % ranges) for continuous variables with a skewed distribution

Abbreviations: 25(OH) D3, 25–hydroxyvitamin D3

aComparison among four groups

bNS = no significant at p value > .05

#Compared with Q1, P < 0.05

&Compared with Q2, P < 0.05

$Compared with Q3, P < 0.05

Table 3

Characteristics of the study population according to quartiles of visceral fat area levels in women

 

Pre-menopausal women

 

Quartiles of visceral fat area (cm2)

P-valuea

Q1 (<53.15)

Q2 (53.15–66.18)

Q3 (66.18–84.47)

Q4 (≥84.47)

n

153

144

163

153

 

Age, y

33.09 ± 6.30

36.54 ± 7.54#

38.35 ± 6.91# &

41.27 ± 7.41# & $

0.000

Body mass index, kg/m2

20.51 ± 1.33

21.54 ± 1.46#

22.44 ± 1.77# &

25.48 ± 3.46# & $

0.000

Waist circumference, cm

73.06 ± 3.74

76.67 ± 3.48#

79.62 ± 3.92# &

88.27 ± 7.90# & $

0.000

Waist-to-hip ratio

0.81 ± 0.02

0.84 ± 0.02#

0.86 ± 0.02# &

0.90 ± 0.04# & $

0.000

Fat mass, kg

14.39 ± 2.71

17.02 ± 2.90#

18.99 ± 3.08# &

24.93 ± 5.80# & $

0.000

Free fat mass, kg

39.65 ± 3.46

39.84 ± 3.69

40.16 ± 3.42

43.23 ± 4.85# & $

0.000

Percentage body fat, %

26.53 ± 3.69

29.85 ± 3.74#

32.01 ± 3.58# &

36.26 ± 4.46# & $

0.000

Systolic blood pressure, mmHg

102.64 ± 12.01

102.31 ± 10.81

106.97 ± 112.46#

110.85 ± 15.45# &

0.000

Diastolic blood pressure, mmHg

69.03 ± 8.46

69.18 ± 7.37

72.13 ± 8.73

74.38 ± 10.18# &

0.001

Total cholesterol, mmol/L

4.42 ± 0.72

4.63 ± 0.77#

4.73 ± 0.87#

4.90 ± 0.87# & $

0.000

Triglycerides, mmol/L

0.66(0.58–0.86)

0.79(0.64–1.07)#

0.94(0.69–1.25)# &

1.16(0.80–1.55)# & $

0.000

High-density lipoprotein cholesterol, mmol/L

1.46 ± 0.29

1.41 ± 0.30

1.32 ± 0.24# &

1.26 ± 0.25# &

0.000

Low-density lipoprotein cholesterol, mmol/L

2.41 ± 0.62

2.64 ± 0.63#

2.81 ± 0.76# &

3.02 ± 0.75# & $

0.000

Fasting plasma glucose, mmol/L

5.29 ± 0.47

5.37 ± 0.45

5.55 ± 0.78# &

5.77 ± 0.90# & $

0.000

25(OH)D3, μg/L

43.25 ± 28.90

42.30 ± 28.02

38.39 ± 24.11

35.80 ± 27.38# &

0.002

Smoking, % yes

0.65

0.69

0.61

0.65

bNS

Drinking, % yes

22.22

25.00

24.54

29.41

bNS

Doing exercise, % yes

44.44

48.61

43.56

47.06

bNS

Sunshine time, h/day

1.00(0.50–0.10)

1.00(0.00–1.00)

1.00(0.50–0.10)

1.00(0.50–0.10)

bNS

Vitamin D supplement users, % yes

1.96

0.69

1.23

0.65

bNS

 

Post-menopausal women

 
 

Quartiles of visceral fat area (cm2)

P-valuea

 

Q1(<71.55)

Q2(71.55–91.97)

Q3(91.97–115.73)

Q4(≥115.73)

 

n

59

59

59

58

 

Age, y

58.17 ± 7.74

59.25 ± 5.49

58.95 ± 5.60

59.38 ± 5.81

bNS

Body mass index, kg/m2

21.43 ± 1.60

22.62 ± 1.22#

24.18 ± 2.00# &

27.64 ± 2.51# & $

0.000

Waist circumference, cm

75.57 ± 4.19

79.47 ± 2.73#

84.24 ± 4.41# &

93.64 ± 6.10# & $

0.000

Waist-to-hip ratio

0.82 ± 0.02

0.86 ± 0.01#

0.89 ± 0.01# &

0.93 ± 0.03# & $

0.000

Fat mass, kg

16.80 ± 2.85

19.42 ± 2.35#

22.66 ± 3.51# &

29.18 ± 4.87# & $

0.000

Free fat mass, kg

38.72 ± 3.89

38.79 ± 2.88

39.66 ± 3.24

42.51 ± 4.45# & $

0.000

Percentage body fat, %

30.18 ± 3.77

33.34 ± 3.03#

36.25 ± 3.45# &

40.55 ± 3.97# & $

0.000

Systolic blood pressure, mmHg

115.14 ± 14.90

120.78 ± 18.67

122.36 ± 13.65

124.88 ± 15.37

bNS

Diastolic blood pressure, mmHg

75.97 ± 9.47

76.72 ± 8.67

77.22 ± 8.23

81.63 ± 10.04# & $

0.029

Total cholesterol, mmol/L

   

5.64 ± 0.93

5.84 ± 0.10

5.88 ± 1.17

5.58 ± 0.82

bNS

Triglycerides, mmol/L

1.10(0.67–1.40)

1.21 (0.93–1.50)#

1.40(1.07–1.94)# &

158(1.16–1.89)# &

0.000

   

High-density lipoprotein cholesterol, mmol/L

1.55 ± 0.30

1.42 ± 0.23#

1.33 ± 0.25#

1.35 ± 0.26#

0.000

   

Low-density lipoprotein cholesterol, mmol/L

3.31 ± 0.80

3.57 ± 0.73

3.54 ± 0.85

3.33 ± 0.81

bNS

   

Fasting plasma glucose, mmol/L

5.75 ± 1.34

6.06 ± 1.13

6.35 ± 1.51

6.10 ± 0.84

bNS

   

25(OH)D3, μg/L

33.04 ± 22.62

33.63 ± 20.89

29.77 ± 20.90

27.78 ± 19.64

bNS

   

Smoking, % yes

3.39

6.78

8.47

10.34

bNS

   

Drinking, % yes

33.90

38.98

40.68

46.55

bNS

   

Doing exercise, % yes

32.20

30.51

22.03

18.97

bNS

   

Sunshine time, h/day

1.00(0.50–0.10)

1.00(0.00–1.00)

1.00(0.50–0.10)

1.00(0.50–0.10)

bNS

   

Vitamin D supplement users, % yes

3.39

5.08

6.78

5.17

bNS

   

Values are percentages for categorical variables, means ± SDs for continuous variables with a normal distribution, or medians (95 % ranges) for continuous variables with a skewed distribution

Abbreviations: 25(OH) D3, 25-hydroxyvitamin D3

aComparison among four groups

bNS = no significant at p value > .05

#Compared with Q1, P < 0.05

&Compared with Q2, P < 0.05

$Compared with Q3, P < 0.05

Prevalence of vitamin D insufficiency and vitamin D deficiency according to the quartiles of VFA

Figure 1a showed that the prevalence of vitamin D deficiency increased in men and in pre-menopausal women according to the quartiles of VFA (P <0.05), but not in post-menopausal women (P >0.05). The prevalence of vitamin D deficiency in the fourth quartile of VFA in men (46.88 %) and in pre-menopausal women (28.10 %) were significantly higher than that in the first quartile (15.63 % in men and 13.07 % in pre-menopausal women), second quartile (35.38 % in men and 16.67 % in pre-menopausal women) and third quartile (35.94 % in men and 17.18 % in pre-menopausal women) (P <0.05) (Fig. 1a). Increased VFA was observed to be associated with higher vitamin D deficiency risk with a positive dose–response trend in men and pre-menopausal women (P for trend < 0.001), not in post-menopausal women. The prevalence of vitamin D insufficiency in the fourth quartile of VFA in men (28.13 %) was significantly higher than that in the first quartile (9.23 %) and second quartile (12.50 %) (Fig. 1b). However, the prevalence of vitamin D insufficiency did not increase with the quartiles of VFA in pre-menopausal women and post-menopausal women (P >0.05) (Fig. 1b).
Fig. 1

Prevalence of vitamin D deficiency (25(OH) D3) <20 μg/L) (a) or vitamin D insufficiency (25(OH) D3: 20–29 μg/L) (b) according to the quartiles of visceral fat area in men and women. Men (Q1: <89.95 cm2, Q2: 89.95–115.72 cm2, Q3: 115.72–140.46 cm2, Q4: ≥140.46 cm2); Pre-menopausal women (Q1: <53.15 cm2, Q2: 53.15–66.18 cm2, Q3: 66.18–84.47 cm2, Q4: ≥ 84.47 cm2); Post-menopausal women (Q1: <71.55 cm2, Q2: 71.55–91.97 cm2, Q3: 91.97–115.73 cm2, Q4: ≥115.73 cm2). *Compared with Q1, P <0.05; #Compared with Q2, P <0.05; &Compared with Q3, P <0.05

Relationship between VFA and vitamin D insufficiency and deficiency

Partial correlation analysis showed that serum 25(OH) D3 levels were negatively correlated with VFA and other body fatness indices in men (Fig. 2a-e) and pre-menopausal women (Fig. 2f-j) (all P < 0.05), not in post-menopausal women (Fig. 2k-o). We also assessed the odds ratios (ORs) and 95 % confidence intervals (CIs) of VFA levels and vitamin D insufficiency and deficiency. After adjusting for age, smoking status, drinking status, exercise status, sun exposure and lipid profiles, as compared to individuals with the lowest VFA, those who had the highest VFA were at 4.9-fold risk of vitamin D insufficiency and deficiency (95 % CI: 1.792–13.365) in men and 1.8-fold risk of vitamin D insufficiency and deficiency (95 % CI: 1.051–3.210) in pre-menopausal women, not in post-menopausal women (Table 4).
Fig. 2

The correlation between serum 25(OH) D3 and fatness indices in men (a-e) and women [pre-menopausal women (f-j); post-menopausal women (k-o)]. Abbreviations: 25(OH)D3, 25-hydroxyvitamin D3; BMI, body mass index; WC, waist circumference; WHR, waist-to-hip ratio; PBF, percentage body fat; VFA, visceral fat area

Table 4

The odd ratios of different fatness indices and vitamin D insufficiency and deficiency in men and women

Gender

Fatness indices

Crude model

Adjusted modela

OR (95 % CI)

P-Value

OR (95 % CI)

P-Value

Men

Visceral fat area

    

Q1(<89.95 cm2)

1.0

 

1.0

 

Q2(89.95–115.72 cm2)

2.059(0.990–4.281)

0.053

1.320(0.476–3.662)

0.594

Q3(115.72–140.46 cm2)

3.987(1.900–8.364)

0.000

2.424(0.916–6.417)

0.075

Q4(≥140.46 cm2)

7.667(3.495–16.817)

0.000

4.894(1.792–13.365)

0.002

Continuous

1.025(1.016–1.034)

 

1.719(1.251–2.361)

 

P-value for trend

0.000

 

0.001

 

Body mass index

    

<28 kg/m2

1.0

 

1.0

 

≥28 kg/m2

3.930(2.162–7.142)

0.000

2.857(1.360–6.001)

0.006

Waist circumference

    

<90 cm

1.0

 

1.0

 

≥90 cm

3.007(1.809–4.998)

0.000

2.199(1.130–4.279)

0.020

Waist-to-hip ratio

    

<0.90

1.0

 

1.0

 

≥0.90

3.802(2.210–6.539)

0.000

2.052(1.010–4.169)

0.047

Pre-menopausal women

Visceral fat area

    

Q1(<53.15 cm2)

1.0

 

1.0

 

Q2(53.15–66.18 cm2)

1.240(0.781–1.968)

0.361

1.097(0.644–1.868)

0.735

Q3(66.18–84.47 cm2)

1.257(0.803–1.068)

0.317

1.215(0.717–2.059)

0.469

Q4(≥84.47 cm2)

2.338(1.478–3.697)

0.000

1.837(1.051–3.210)

0.033

Continuous

1.013(1.008–1.018)

 

1.265(1.037–1.543)

 

P-value for trend

0.000

 

0.030

 

Body mass index

    

<28 kg/m2

1.0

 

1.0

 

≥28 kg/m2

3.921(1.952–7.875)

0.000

3.052(1.430–6.514)

0.004

Waist circumference

    

<80 cm

1.0

 

1.0

 

≥80 cm

1.809(1.297–2.523)

0.000

1.647(1.121–2.419)

0.011

Waist-to-hip ratio

    

<0.85

1.0

 

1.0

 

≥0.85

1.487 (1.081–2.046)

0.015

1.281(0.878–1.871)

0.199

Post-menopausal women

Visceral fat area

    
 

Q1(<71.55 cm2)

1.0

 

1.0

 
 

Q2(71.55–91.97 cm2)

0.813(0.392–1.686)

0.577

0.912 (0.359–2.319)

0.847

 

Q3(91.97–115.73 cm2)

1.153(0.550–2.418)

0.706

1.254(0.506–3.106)

0.625

 

Q4(≥115.73 cm2)

1.800(0.829–3.909)

0.137

2.326(0.903–5.991)

0.080

 

Continuous

1.010(1.001–1.019)

 

1.012(1.002–1.022)

 
 

P-value for trend

0.028

 

0.024

 
 

Body mass index

    
 

<28 kg/m2

1.0

 

1.0

 
 

≥28 kg/m2

1.577(0.691–3.598)

0.279

1.379(0.548–3.470)

0.494

 

Waist circumference

    
 

<80 cm

1.0

 

1.0

 
 

≥80 cm

1.391(0.814–2.377)

0.228

1.522(0.780–2.969)

0.218

 

Waist-to-hip ratio

    
 

<0.85

1.0

 

1.0

 
 

≥0.85

1.413(0.776–2.573)

0.258

1.540(0.732–3.241)

0.255

aAdjusted for age, smoking status, drinking status, exercise status, sunshine time and lipid profiles

Discussion

In this cross-sectional study, we confirmed that visceral fat obesity was an important risk factor of vitamin D insufficiency and deficiency among Chinese men and pre-menopausal women, and discovered the increase of visceral adiposity was positively associated with vitamin D insufficiency or deficiency risk with clear dose–response relationship.

There is evidence that vitamin D metabolism, storage, and action both influence and are influenced by adiposity. Observational studies have reported that an increased risk of vitamin D deficiency in those people with obesity [24]. Active vitamin D (1, 25-dihydroxyvitamin D) may influence the mobilisation of free fatty acids from the adipose tissue [25]. In vitro experiments in rats have also shown that large doses of vitamin D2 lead to increases in energy expenditure due to uncoupling of oxidative phosphorylation in adipose tissues [26]. Consistent with the experimental studies, our result has indicated that serum 25(OH) D3 levels decreased significantly in subjects with visceral obesity and has shown that this decrease was closely correlated with fat distribution [27, 28].

Although the mechanism for the association between obesity and vitamin D insufficiency is not well understood, researches suggested that individuals with obesity were prone to vitamin D insufficiency [2931], possibly as the result of increased sequestration of vitamin D in the increased amounts of visceral adipose tissue in individuals with obesity [30]. This may lead to less vitamin D released into the blood, and consequently these individuals may have lower serum 25(OH) D3 levels. Such individuals may therefore need to increase their vitamin D intake to attain serum 25(OH) D3 levels comparable with individuals with normal BMI [29]. Evidence also suggests that vitamin D insufficiency may stimulate lipogenesis as the result of increased calcium influx into the adipocytes mediated by increased synthesis of parathyroid hormones [32]. This would suggest that vitamin D insufficiency could cause obesity. Minimal outdoor activity and maximum skin covering by clothing among the population with obesity also limits photochemical subcutaneous synthesis of vitamin D [31]. Although we have found an association between VFA and vitamin D insufficiency and deficiency, we used cross-sectional data, and thus, were precluded from establishing a temporal relationship between VFA and vitamin D insufficiency and deficiency. However, clinical trials have failed to conclusively demonstrate the benefits of vitamin D supplementation. Randomized controlled trials testing the effect of vitamin D supplementation on weight loss in individuals with obesity or overweight have provided inconsistent findings [3335]. Dilution related to the greater volume of distribution has been recently proposed as the most likely explanation for the lower 25(OH) D3 concentrations in individuals with obesity [36]. In that study, no evidence was found for reduced bioavailability through increased sequestration of vitamin D in the adipose tissue, which had previously been suggested to contribute to the low 25(OH) D3 concentrations in obesity. Therefore, these results suggested that although increased in vitamin D status were not likely to help with weight regulation, increased risk of vitamin D deficiency could contribute to the adverse health effects associated with obesity. Recent study has showed that higher BMI led to lower vitamin D status, providing evidence for the role of obesity as a causal risk factor for the development of vitamin D deficiency on the basis of a bi-directional genetic approach [37].

Next to common adiposity measures, we also discovered that VFA was inversely associated with serum 25(OH) D3 concentrations in Chinese men and pre-menopausal women, which was similar to the recent study in Northeast Germany and Denmark [38] and China [16]. Differed from Hao’s study among Chinese population, our study population included men and women, and included the participants who were diabetes. Especially, we have observed that the men had the higher risk for vitamin D insufficiency and deficiency. It was because the prevalence of obesity and visceral obesity in men was higher than in women. Obesity is known to be associated with decreased bioavailability of vitamin D, which is sequestered in body fat [30]. Moreover, there was a clear difference in the relationship of VFA and vitamin D insufficiency and deficiency between post- and pre-menopausal women in our study. On one hand, the prevalence of vitamin D insufficiency and deficiency in our study was higher in post-menopausal women. The vitamin D inadequacy is also present in many postmenopausal women in European, North American countries and Eastern Asia [3942]. On the other hand, there was no difference in the vitamin D insufficiency and deficiency across the quartiles of VFA among post-menopausal women. Thus, we did not observe a relationship between VFA and vitamin D insufficiency and deficiency in post-menopausal women.

Still other studies have implicated the decreased level of serum 25(OH) D3 was considered as a risk factor for obesity and its related metabolic disorders including hypertension, high pulse pressure, obesity, hyperlipidemia, diabetes, etc., which increases the chance of cardiovascular disease [4348]. Currently, researches on vitamin D and metabolic syndrome or its components, which are known to increase cardiovascular disease, are being conducted all over the world [4952]. Compared with the non-metabolic syndrome group, serum 25(OH) D3 levels were significantly lower in the metabolic syndrome group [52]. Lu et al. [50] have reported that reduced serum 25(OH) D3 levels were associated with metabolic syndrome and its components, and in particular, obesity was highly associated with insulin resistance and serum 25(OH) D3 when compared to normal weight. Among Korean studies, metabolic syndrome and hypertension were associated with serum 25(OH) D3 levels in a study of middle-aged Koreans [51]. In fact, Forouhi et al. reported a significant interaction between 25(OH) D and BMI on the risk for a 10-year increase in HOMA-IR [52]. Moreover, the release of free fatty acids from adipose tissue can induce insulin resistance, whereas 1, 25-hydroxyvitamin D has been shown to counteract the free fatty acid-induced insulin resistance [53]. The stronger association of vitamin D with insulin resistance among the participants with visceral fat obesity suggests that adequate vitamin D status is more important for the prevention of insulin resistance and metabolic syndrome in these individuals. In addition, a larger VFA was strongly related to a higher prevalence of impaired fasting glucose levels [54], diabetes [54], insulin resistance [54], hypertension [55], abnormality of lipid metabolism [56], and metabolic risk factors [56, 57]. In our study, the prevalence of hyperglycemia and hypertriglyceridemia increased with the quartiles of VFA in both genders (Appendix Table 1), and VFA was closely related with the indices of metabolic disorders (Appendix Table 2). The individuals with the higher VFA levels have the higher risk of hyperglycemia and hypertriglyceridemia in both genders (Appendix Table 3). In accordance with our finding, one study has demonstrated that the VFA rather than the WC itself was a major determinant of metabolic syndrome in premenopausal Korean women [58], whereas the WC and VFA were similarly useful in identifying metabolic syndrome in elderly Korean women [59]. Our study highlights VFA might also be a simple and sensitive index in routine use for screening vitamin D deficiency and vitamin D related disease among general.

This study has several limitations. First, the cross-sectional study design precluded the ability to determine a causal relationship between VFA and vitamin D insufficiency and deficiency. Second, the DEXA, CT and MRI were not used to measure visceral fat mass for our study because the participants in our study from the routine health check-up. The DEXA, CT and MRI were not the regular item of health check-up since they require expensive and specialized equipment, and exposure to radiation. Third, the intact parathyroid hormone (iPTH) is also expected to be a relevant confounder or even the causal factor of the association between VFA and 25(OH) D3, and our study often concentrated exclusively on 25(OH) D3 or iPTH without considering the interaction between both. In addition, menopausal status was based on self-reporting. Therefore, further cohort study will be conducted to observe the causal relations between VFA and vitamin D insufficiency and deficiency.

Conclusion

In conclusion, results of our study revealed that higher VFA increases the risk of vitamin D insufficiency and deficiency in men and pre-menopausal women, but not in post-menopausal women. VFA is a better and convenience surrogate marker for visceral adipose measurement and could be used in identifying the risk of vitamin D insufficiency and deficiency in routine health examination.

Abbreviations

VFO: 

Visceral fat obesity

VFA: 

Visceral fat area

25(OH) D3

25-hydroxyvitamin D3

BMI: 

Body mass index

WC: 

Waist circumference

WHR: 

Waist-to-hip ratio

FM: 

Fat mass

FFM: 

Free fat mass

PBF: 

Percentage body fat

DEXA: 

Dual-energy x-ray absorptiometry

MRI: 

Magnetic resonance imaging

CT: 

Computed tomography

BIA: 

Bioelectrical impedance analysis

FPG: 

Fasting plasma glucose

TC: 

Total cholesterol

TG: 

Triglycerides

LDL-c: 

Low-density lipoprotein cholesterol

HDL-c: 

High-density lipoprotein cholesterol

HPLC: 

High-performance liquid chromatography

ANOVA: 

One-way analysis of variance

Declarations

Acknowledgements

We wish to thank all who participated in the study, the stuff at our Medical Check-up Center who assisted the study. This research was funded by the National Science and Technology Support Program (No. 2012BAI02B02) and National Natural Science Foundation of China (No. 81502809).

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Nutrition and Food Science, School of Public Health, Tianjin Medical University
(2)
Department of Rehabilitation and Sports Medicine, Tianjin Medical University
(3)
Health Education and Guidance Center of Heping District

References

  1. Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, et al. Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2011;96:1911–30.View ArticleGoogle Scholar
  2. Samuel L, Borrell LN. The effect of body mass index on optimal vitamin D status in U.S. adults: the National Health and Nutrition Examination Survey 2001-2006. Ann Epidemiol. 2013;23:409–14.View ArticleGoogle Scholar
  3. Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, et al. Guidelines for preventing and treating vitamin D deficiency and insufficiency revisited. J Clin Endocrinol Metab. 2012;97:1153–8.View ArticleGoogle Scholar
  4. Holick MF. Vitamin D deficiency. N Engl J Med. 2007;357:266–81.View ArticleGoogle Scholar
  5. Lu L, Yu Z, Pan A, Hu FB, Franco OH, Li H, et al. Plasma 25-hydroxyvitamin D concentration and metabolic syndrome among middle-aged and elderly Chinese individuals. Diabetes Care. 2009;32:1278–83.View ArticleGoogle Scholar
  6. Zhen D, Liu L, Guan C, Zhao N, Tang X. High prevalence of vitamin D deficiency among middle-aged and elderly individuals in northwestern China: Its relationship to osteoporosis and lifestyle factors. Bone. 2015;71:1–6.View ArticleGoogle Scholar
  7. Reis AF, Hauache OM, Velho G. Vitamin D endocrine system and the genetic susceptibility to diabetes, obesity and vascular disease. A review of evidence. Diabetes Metab. 2005;31:318–25.View ArticleGoogle Scholar
  8. Lagunova Z, Porojnicu AC, Vieth R, Lindberg FA, Hexeberg S, Moan J. Serum 25-hydroxyvitamin D is a predictor of serum 1,25-dihydroxyvitamin D in overweight and obese patients. J Nutr. 2011;141:112–7.View ArticleGoogle Scholar
  9. Rodríguez-Rodríguez E, Navia B, López-Sobaler AM, Ortega RM. Vitamin D in overweight/obese women and its relationship with dietetic and anthropometric variables. Obesity (Silver Spring). 2009;17:778–82.View ArticleGoogle Scholar
  10. Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu CY, et al. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risl factors in the Framingham Heart Study. Circulation. 2007;116:39–48.View ArticleGoogle Scholar
  11. WHO. Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep Ser. 2000;894:i–xii. 1-253.Google Scholar
  12. Cornier MA, Després JP, Davis N, Grossniklaus DA, Klein S, Lamarche B, et al. Assessing adiposity: a scientific statement from the American Heart Association. Circulation. 2011;124:1996–2019.View ArticleGoogle Scholar
  13. Xu L, Cheng X, Wang J, Cao Q, Sato T, Wang M, et al. Comparisons of body composition prediction accuracy: a study of 2 bioelectric impedance consumer devices in healthy Chinese persons using DXA and MRI as criteria methods. J Clin Densitom. 2011;14:458–64.View ArticleGoogle Scholar
  14. Kang SH, Cho KH, Park JW, Yoon KW, Do JY. Association of visceral fat area with chronic kidney disease and metabolic syndrome risk in the general population: analysis using multi-frequency bioimpedance. Kidney Blood Press Res. 2015;40:223–30.View ArticleGoogle Scholar
  15. Kotler DP, Burastero S, Wang J, Pierson Jr RN. Prediction of body cell mass, fat-free mass, and total body water with bioelectrical impedance analysis: effects of race, sex, and disease. Am J Clin Nutr. 1996;64(3 Suppl):489S–97S.Google Scholar
  16. Hao Y, Ma X, Shen Y, Ni J, Luo Y, Xiao Y, et al. Associations of serum 25-hydroxyvitamin D3 levels with visceral adipose tissue in Chinese men with normal glucose tolerance. PLoS One. 2014;9:e86773.View ArticleGoogle Scholar
  17. Kuk JL, Lee S, Heymsfield SB, Ross R. Waist circumference and abdominal adipose tissue distribution: influence of age and sex. Am J Clin Nutr. 2005;81:1330–4.Google Scholar
  18. Gundberg CM, Looker AC, Nieman SD, Calvo MS. Patterns of osteocalcin and bone specific alkaline phosphatase by age, gender, and race or ethnicity. Bone. 2002;31:703–8.View ArticleGoogle Scholar
  19. Looker AC. Body fat and vitamin D status in black versus white women. J Clin Endocrinol Metab. 2005;90:635–40.View ArticleGoogle Scholar
  20. Shoji K, Maeda K, Nakamura T, Funahashi T, Matsuzawa Y, Shimomura I. Measurement of visceral fat by abdominal bioelectrical impedance analysis is beneficial in medical checkup. Obes Res Clin Pract. 2008;2:I–II.View ArticleGoogle Scholar
  21. Li R, Lu W, Jia J, Zhang S, Shi L, Li Y, et al. Relationships between indices of obesity and its cardiovascular comorbidities in a Chinese population. Cir J. 2008;72:937–8.Google Scholar
  22. Kim TN, Park MS, Kim YJ, Lee EJ, Kim MK, Kim JM, et al. Association of low muscle mass and combined low muscle mass and visceral obesity with low cardiorespiratory fitness. PLoS One. 2014;9:e100118.View ArticleGoogle Scholar
  23. Holick MF. High prevalence of vitamin D inadequacy and implications for health. Mayo Clin Proc. 2006;81:353–73.View ArticleGoogle Scholar
  24. Earthman CP, Beckman LM, Masodkar K, Sibley SD. The link between obesity and low circulating 25-hydroxyvitamin D concentrations: considerations and implications. Int J Obes (Lond). 2012;36:387–96.View ArticleGoogle Scholar
  25. Shi H, Norman AW, Okamura WH, Sen A, Zemel MB. 1alpha, 25- Dihydroxyvitamin D3 modulates human adipocyte metabolism via nongenomic action. FASEB J. 2001;15:2751–3.Google Scholar
  26. Fassina G, Maragno I, Dorigo P, Contessa AR. Effect of vitamin D2 on hormone-stimulated lipolysis in vitro. Eur J Pharmacol. 1969;5:286–90.View ArticleGoogle Scholar
  27. Rodríguez-Rodríguez E, Navia-Lombán B, López-Sobaler AM, Ortega RM. Associations between abdominal fat and body mass index on vitamin D status in a group of Spanish school children. Eur J Clin Nutr. 2010;64:461–7.View ArticleGoogle Scholar
  28. Nam GE, Kim do H, Cho KH, Park YG, Han KD, Choi YS, et al. Estimate of a predictive cut-off value for serum 25-hydroxyvitamin D reflecting abdominal obesity in Korean adolescents. Nutr Res. 2012;32:395–402.View ArticleGoogle Scholar
  29. Hatfield DP, Sweeney KP, Lau J, Lichtenstein AH. Critical assessment of high-circulation print newspaper coverage of the Institute of Medicine report Dietary Reference Intakes for Calcium and Vitamin D. Public Health Nutr. 2014;17:1868–76.View ArticleGoogle Scholar
  30. Wortsman J, Matsuoka LY, Chen TC, Lu Z, Holick MF. Decreased bioavailability of vitamin D in obesity. Am J Clin Nutr. 2000;72:690–3.Google Scholar
  31. Compston JE, Vedi S, Ledger JE, Webb A, Gazet JC, Pilkington TR. Vitamin D status and bone histomorphometry in gross obesity. Am J Clin Nutr. 1981;34:2359–63.Google Scholar
  32. McCarty MF, Thomas CA. PTH excess may promote weight gain by impeding catecholamine-induced lipolysis-implications for the impact of calcium, vitamin D, and alcohol on body weight. Med Hypotheses. 2003;61:535–42.View ArticleGoogle Scholar
  33. Sneve M, Figenschau Y, Jorde R. Supplementation with cholecalciferol does not result in weight reduction in overweight and obese subjects. Eur J Endocrinol. 2008;159:675–84.View ArticleGoogle Scholar
  34. Zittermann A, Frisch S, Berthold HK, Götting C, Kuhn J, Kleesiek K, et al. Vitamin D supplementation enhances the beneficial effects of weight loss on cardiovascular disease risk markers. Am J Clin Nutr. 2009;89:1321–7.View ArticleGoogle Scholar
  35. Salehpour A, Shidfar F, Hosseinpanah F, Vafa M, Razaghi M, Hoshiarrad A, et al. Vitamin D3 and the risk of CVD in overweight and obese women: a randomized controlled trial. Br J Nutr. 2012;108:1866–73.View ArticleGoogle Scholar
  36. Drincic AT, Armas LA, Van Diest EE, Heaney RP. Volumetric dilution, rather than sequestration best explains the low vitamin D status of obesity. Obesity (Silver Spring). 2012;20:1444–8.View ArticleGoogle Scholar
  37. Vimaleswaran KS, Berry DJ, Lu C, Tikkanen E, Pilz S, Hiraki LT, et al. Causal relationship between obesity and vitamin D status: bi-directional Mendelian randomization analysis of multiple cohorts. Plos Med. 2013;10:e1001383.View ArticleGoogle Scholar
  38. Hannemann A, Thuesen BH, Friedrich N, Völzke H, Steveling A, Ittermann T, et al. Adiposity measures and vitamin D concentrations in Northeast Germany and Denmark. Nutr Metab (Lond). 2015;12:24.View ArticleGoogle Scholar
  39. Holick MF, Siris ES, Binkley N, Beard MK, Khan A, Katzer JT, et al. Prevalence of Vitamin D inadequacy among postmenopausal North American women receiving osteoporosis therapy. J Clin Endocrinol Metab. 2005;90:3215–24.View ArticleGoogle Scholar
  40. Isaia G, Giorgino R, Rini GB, Bevilacqua M, Maugeri D, Adami S. Prevalence of hypovitaminosis D in elderly women in Italy: clinical consequences and risk factors. Osteoporosis Int. 2003;14:577–82.View ArticleGoogle Scholar
  41. Lips P, Duong T, Oleksik A, Black D, Cummings S, Cox D, et al. A global study of vitamin D status and parathyroid function in postmenopausal women with osteoporosis: baseline data from the multiple outcomes of raloxifene evaluation clinical trial. J Clin Endocrinol Metab. 2001;86:1212–21.View ArticleGoogle Scholar
  42. Lim SK, Kung AW, Sompongse S, Soontrapa S, Tsai KS. Vitamin D inadequacy in postmenopausal women in Eastern Asia. Curr Med Res Opin. 2008;24:99–106.View ArticleGoogle Scholar
  43. Yin X, Sun Q, Zhang X, Lu Y, Sun C, Cui Y, et al. Serum 25(OH) D is inversely associated with metabolic syndrome risk profile among urban middle-aged Chinese population. Nutr J. 2012;11:68.View ArticleGoogle Scholar
  44. Benetos A, Rudnichi A, Safar M, Guize L. Pulse pressure and cardiovascular mortality in normotensive and hypertensive subjects. Hypertension. 1998;32:560–4.View ArticleGoogle Scholar
  45. Yoon H, Kim GS. The association of Vitamin D and Pulse pressure in Korean Adults: Korea National Health and Nutrition Survey, 2010. J Korea Acad Industr Coop Soc. 2013;14:2735–42.View ArticleGoogle Scholar
  46. Gasowski J, Fagard RH, Staessen JA, Grodzicki T, Pocock S, Boutitie F, et al. Pulsatile blood pressure component as predictor of mortality in hypertension: a meta-analysis of clinical trial control groups. J Hypertens. 2002;20:145–51.View ArticleGoogle Scholar
  47. Franklin SS, Khan SA, Wong ND, Larson MG, Levy D. Is pulse pressure useful in predicting risk for coronary heart disease? The Framingham heart study. Circulation. 1999;100:354–60.View ArticleGoogle Scholar
  48. Baker JF, Mehta NN, Baker DG, Toedter G, Shults J, Von Feldt JM, et al. Vitamin D, metabolic dyslipidemia, and metabolic syndrome in rheumatoid arthritis. Am J Med. 2012;125:1036.e9-1036.e15.View ArticleGoogle Scholar
  49. Kim J. Association between serum vitamin D, parathyroid hormone and metabolic syndrome in middle-aged and older Korean adults. Eur J Clin Nutr. 2015;69:425–30.View ArticleGoogle Scholar
  50. Kim MK, Il Kang M, Won Oh K, Kwon HS, Lee JH, Lee WC, et al. The association of serum vitamin D level with presence of metabolic syndrome and hypertension in middle-aged Korean subjects. Clin Endocrinol (Oxf). 2010;73:330–8.View ArticleGoogle Scholar
  51. Yoon H, Kim GS, Kim SG, Moon AE. The relationship between metabolic syndrome and increase of metabolic syndrome score and serum vitamin Dlevels in Korean adults: 2012 Korean National Health and Nutrition Examination Survey. J Clin Biochem Nutr. 2015;57:82–7.View ArticleGoogle Scholar
  52. Forouhi NG, Luan J, Cooper A, Boucher BJ, Wareham NJ. Baseline serum 25-hydroxy vitamin d is predictive of future glycemic status and insulin resistance: the Medical Research Council Ely Prospective Study 1990-2000. Diabetes. 2008;57:2619–25.View ArticleGoogle Scholar
  53. Zhou QG, Hou FF, Guo ZJ, Liang M, Wang GB, Zhang X. 1, 25-Dihydroxyvitamin D improved the free fatty-acid-induced insulin resistance in cultured C2C12 cells. Diabetes Metab Res Rev. 2008;24:459–64.View ArticleGoogle Scholar
  54. Goodpaster BH, Krishnaswami S, Resnick H, Kelley DE, Haggerty C, Harris TB, et al. Association between regional adipose tissue distribution and both type 2 diabetes and impaired glucose tolerance in elderly men and women. Diabetes Care. 2003;26:372–9.View ArticleGoogle Scholar
  55. Hayashi T, Boyko EJ, Leonetti DL, McNeely MJ, Newell-Morris L, Kahn SE, et al. Visceral adiposity is an independent predictor of incident hypertension in Japanese Americans. Ann Intern Med. 2004;140:992–1000.View ArticleGoogle Scholar
  56. Nagaretani H, Nakamura T, Funahashi T, Kotani K, Miyanaga M, Tokunaga K, et al. Visceral fat is a major contributor for multiple risk factor clustering in Japanese men with impaired glucose tolerance. Diabetes Care. 2001;24:2127–33.View ArticleGoogle Scholar
  57. Carr DB, Utzschneider KM, Hull RL, Kodama K, Retzlaff BM, Brunzell J, et al. Intra-abdominal fat is a major determinant of the national cholesterol education program adult treatment panel III criteria for the metabolic syndrome. Diabetes. 2004;3:2087–94.View ArticleGoogle Scholar
  58. Hyun YJ, Kim OY, Jang Y, Ha JW, Chae JS, Kim JY, et al. Evaluation of metabolic syndrome risk in Korean premenopausal women: not waist circumference but visceral fat. Circ J. 2008;72:1308–15.View ArticleGoogle Scholar
  59. Seo JA, Kim BG, Cho H, Kim HS, Park J, Baik SH, et al. The cutoff values of visceral fat area and waist circumference for identifying subjects at risk for metabolic syndrome in elderly Korean: Ansan Geriatric (AGE) cohort study. BMC Public Health. 2009;9:443.View ArticleGoogle Scholar

Copyright

© Zhang et al. 2015

Advertisement