Associations between abdominal fat and body mass index on vitamin ...

European Journal of Clinical Nutrition (2010) 64, 461–467

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ORIGINAL ARTICLE

Associations between abdominal fat and body mass index on vitamin D status in a group of Spanish schoolchildren E Rodrı´guez-Rodrı´guez, B Navia-Lombań, AM Lo´pez-Sobaler and RM Ortega. Research group: 920030 Departamento de Nutricioń, Facultad de Farmacia, Universidad Complutense, Madrid, Spain

Background/Objectives: To analyze the association between different anthropometric variables and vitamin D status in a group of Spanish schoolchildren. Subjects/Methods: Study subjects were 102 children aged 9–13 years. Records were made of their height, body weight, body mass index (BMI), waist and hip measurements (to determine the quantity of visceral or abdominal fat), and the thickness of the tricipital and bicipital skinfold (to determine the quantity of subcutaneous fat). Diets were analyzed using a 3-day weighed food record and vitamin D intakes compared with those recommended. Serum 25-hydroxyvitamin D (25(OH)D) concentrations were measured using chemiluminescent assay. Results: The mean serum 25(OH)D concentration was 49.6±15.9 nmol/l. The mean serum 25(OH)D in the ID subjects (that is, those with insufficient vitamin D levels, 25(OH)D of o70 nmol/l) was 46.6±13.4 nmol/l and in the AD subjects (that is, those with adequate vitamin D levels, 25(OH)D of X70 nmol/l) was 77.5±8.4 nmol/l (Po0.001). No significant difference was observed between both groups in vitamin D intake. However, the ID subjects had higher body weight, BMI, waist measurement and waist/height ratio than the AD subjects. Using a multiple linear regression analysis, only weight and BMI were found to independently influence 25(OH)D values. Children with a body weight, BMI, bicipital skinfold thickness, waist measurement and waist/height ratio above the 50th percentile for each variable were at a greater risk of having a low serum 25(OH)D concentration (o70 nmol/l). Conclusions: BMI and abdominal obesity influence the appearance of vitamin D insufficiency in children.

European Journal of Clinical Nutrition (2010) 64, 461–467; doi:10.1038/ejcn.2010.26; published online 10 March 2010 Keywords: vitamin D; body fat; central obesity; BMI; schoolchildren

Introduction In recent years there has been an increase in the prevalence of overweight/obesity among infants and young people (Alexander et al., 2009); indeed, the problem now affects some 26.3% of the Spanish population aged between 2 and 24 years (Serra et al., 2003). At the same time, concern has been growing over the high number of cases of vitamin D deficiency detected among the younger population (Konradsen et al., 2008; Bener et al., 2008a, b; Bener et al., 2009), a situation that could lead to an increased risk of bone

Correspondence: Dr E Rodrı´guez-Rodrı´guez, Departamento de Nutricioń, Facultad de Farmacia, Universidad Complutense, 28040-Madrid, Spain. E-mail: [email protected] Received 28 June 2009; revised 19 January 2010; accepted 22 January 2010; published online 10 March 2010

disease, cancer, high blood pressure, diabetes and heart disease (Holick, 2004; Poduje et al., 2008; Lee et al., 2008a). Vitamin D deficiency has traditionally been associated with an inappropriate diet and a lack of exposure to the sun (Bener et al., 2008a, b), but some studies have also associated it with excess body weight (Bischof et al., 2006; Reinehr et al., 2007). Body fat could exert an effect as a sink for vitamin D (which is fat soluble), reducing its bioavailability (Wortsman et al., 2000). The results available are, however, conflicting. Epstein et al. (1986) and Nesby-O’Dell et al. (2002) reported no relationship between body mass index (BMI) or obesity and serum 25-hydroxyvitamin D (25(OH)D) levels, whereas Parikh et al. (2004) found a negative significant correlation between BMI and serum 25(OH)D in African Americans. In addition, few studies have been undertaken in children (Alemzadeh et al., 2008; Rajakumar et al., 2008) and none has studied the relationship

Vitamin D status and anthropometric variables E Rodrı´guez-Rodrı´guez et al

462 between the distribution of body fat and vitamin D status in children (Alemzadeh et al., 2008). The aim of this work was to study the association between different anthropometric variables on vitamin status in a group of Spanish schoolchildren.

Materials and methods Subjects Sample recruitment. The study subjects were 102 schoolchildren aged between 9 and 13 years from two schools in the Madrid Region of Spain (latitude 401230 N). The directors were contacted by phone to arrange an interview during which the characteristics and the importance of the study were explained. Permission was requested to meet with the parents of the children in the 9–13 years age group. Once permission was given the parents were explained the details of the study and all questions were answered. Signed permission was then sought to include their children in the study. All subjects took part voluntarily. Parents of 214 children between 9 and 13 years were contacted. Only 123 parents signed permission to include their children in the study. Parents of 91 children did not agree to take part in the study because of different reasons: they did not agree to blood samples being taken of their children, they were not interested in the study and so on. The exclusion criteria were: A lack of authorization to take part or the non-acceptance of any of the conditions required for the study to proceed. Non-attendance on days when tests or interviews were performed. Clinical problems that advised against inclusion or that might modify the results. In all, 1 boy was excluded because he had celiac disease, 1 girl was excluded because she had fish allergy and 19 children were excluded because they did not attend on days when tests were performed. The study was approved by the human research review committee of the Pharmacy Faculty, Complutense University of Madrid.

Methods Dietary survey The subjects’ diets were examined prospectively using a ‘weighed food record’ followed for three consecutive days, including a Sunday (from Sunday to Tuesday) (Ortega et al., 2006a). Parents were instructed to record the weights of food and drink consumed by their children if possible, and if not, to record household measurements (spoonfuls, cups, and so on). In addition, trained researchers monitored the food eaten by the children in the school canteen on the Monday and Tuesday of the food recording period. The ingredients European Journal of Clinical Nutrition

used in the preparation of their meals were noted, as were the quantities served to—and that left unconsumed by— each child. The energy and nutrient contents of these foods were then calculated using Food Composition Tables (Department of Nutrition, 2008a). The values obtained were compared with those recommended (Department of Nutrition, 2008b) to determine the adequacy of the diets. Special attention was paid to the intake of energy and vitamin D. DIAL software (http://www.alceingenieria.net/nutricion.htm; Alce Ingenierıá, 2004) was used to process all data (Ortega et al., 2004). To validate the results of the dietetic study, the total energy intake recorded was compared with the theoretical energy expenditure, taking into account body weight, age and physical activity (Ortega et al., 2006b) using equations proposed by the Institute of Medicine (Food and Nutrition Board; Institute of Medicine, 2005). The percentage discrepancy was determined using the following equation: ðEnergy expenditure energy intake100Þ Energy expenditure

A negative value indicates the total energy intake recorded to be greater than the theoretical energy expenditure (indicating a probable overestimation of energy intake), whereas a positive value indicates the total energy intake to be smaller than the energy expenditure (indicating a probable underestimation of intake; Ortega et al., 1995).

Physical activity The subjects’ physical activity was examined with a questionnaire, in which the length of time spent sleeping, eating, playing sport, and so on, was registered. An activity coefficient was established for each subject (Institute of Medicine, 2005). This questionnaire was also used to measure the exposure time to the sun (Ortega et al., 2006b).

Anthropometric survey All measurements were made at the schools in the morning and by following norms set out by the World Health Organization (WHO, 1995). Weight and height were determined using a digital electronic balance (Seca Alpha, GmbH & Co., Igni, France; range 0.1–150 kg, precision 100 g) and a Harpenden digital stadiometer (Pfifter, Carlstadt, NJ, USA; range 70–205 cm, precision 1 mm), respectively. For these measurements, subjects were barefoot and wore only underwear. Subject BMI was calculated as weight (kg)/height2 (m2). Waist and hip measurements were determined using a Holtain flexible metallic tape (Holtain Ltd., Dyfed, UK; range 0–150 cm, precision 1 mm). These were measured in triplicate while the subject was standing relaxed and with the tape


463 held snugly around the body, although not tight enough to compress the subcutaneous adipose tissue. The waist was measured midway between the inferior margin of the last rib and the crest of the ilium, in a horizontal plane. The hip circumference was measured at the horizontal plane of maximum circumference encircling the buttocks and the pubic symphysis. An assistant helped to hold the tape on the side of the subject’s body opposite to the measurer. The mean of the three measurements was used for analysis. The waist/hip ratio and the waist/height ratio were then calculated. The skinfold thicknesses of triceps and biceps were measured on the right side in triplicate to the nearest millimeter using a Holtain skinfold caliper (Holtain Ltd, Crymych, Wales, UK). All calipers were calibrated each day before taking measurements. Tricipital skinfold thickness (Simon et al., 1985) and the sum of two skinfold thickness (triceps and biceps) (Freedman et al., 2009) were used as an overall measure of subcutaneous fat. The percentage of body fat (%BF) was determined using the equation of Parizkova (Parizkova´ and Roth, 1972): girls : %BF ¼ 39:032Y 30:084

The study subjects were then divided into two groups: ID group (subjects with o70 nmol/l 25(OH)D (insufficient levels)) and AD group (subjects with X70 nmol/l (adequate levels)). This threshold was the 90th percentile for the serum 25(OH)D concentration in the present population and was chosen as the most beneficial concentration for metabolic health because it is thought to be 70–100 nmol/l (Talwar et al., 2007; Vieth et al., 2007; McGill et al., 2008) and it is also in accordance with different studies that have defined as vitamin D insufficiency values from o25 nmol/l to o80 nmol/l (Rovner and O’Brien, 2008).

Statistical analysis Means and s.d. were calculated for all variables. Those for the ID and AD group results were compared using Student’s t-test (or the Mann–Whitney test if the distribution was not homogeneous). Comparisons between proportions were performed using the w2 test. Relationships between serum 25(OH)D and anthropometric variables were quantified using multiple linear regression controlling potential confounders. Logistic regression analysis was used to identify risk or protection factors, expressing the odds ratio and the 95% confidence interval. All calculations were made using RSIGMA BABEL Software (Horus Hardward, Madrid, Spain). Significance was set at Po0.05.

boys : %BF ¼ 32:914Y 21:973 in which Y is the log (sum of skinfold thicknesses: biceps þ triceps) and %BF is the percentage of body fat. Using the value for the percentage of body fat and subject body weight, the fat mass and fat-free masses were then calculated: Fat mass ðFMÞ ðkgÞ ¼ % BFbody weight ðkgÞ=100 Fat mass ðFFMÞ ðkgÞ ¼ body weight FM in which FM is the fat mass, %BF is the percentage of body fat and FFM is the fat-free mass. Biochemical survey 25(OH)D levels were measured using chemiluminescent assay (Sackrison et al., 2002; Wootton, 2005). Serum was incubated anti-vitamin D-coated microparticles and isoluminol derivative-conjugated 25(OH)D before measurement of the chemiluminescent signal. The study was undertaken during winter (specifically on February) and blood was taken in that season. Sunlight exposure was measured using a physical activity questionnaire (Ortega et al., 2006b), in which the time spent outdoors (walking, playing, practicing exercises, sports, and so on) was registered.

Results The study subjects were 102 children (49 boys and 53 girls) between 9 and 13 years (10.9±1.00 years) from Madrid. We collected dietetic information from 99 children and anthropometric and serum vitamin D information from all of them. The study was carried out in winter and all data were collected during February. Mean time exposure to the sun was 8.78±3.18 h/week and mean physical activity coefficient was 1.47±0.12 (low active). Vitamin D intake (2.83±3.27 mg/day) was lower than the recommended 5 m/day (Department of Nutrition, 2008b) in 87.9% of the children studied, and was similar in both sexes (2.69±3.40 mg/day in boys and 2.94±3.17 mg/day in girls). No sex differences were observed with regard to serum 25(OH)D concentration (51.24±15.58 and 48.13± 16.26 nmol/l, respectively). A positive, significant relationship was found between vitamin D intake and the serum concentration of 25(OH)D (r ¼ 0.199; Po0.05). Regarding anthropometric data, girls had greater thickness in the tricipital (16.4±5.6 vs 13.8±7.2 mm; Po0.01) and bicipital (8.3±2.9 vs 7.6±4.7 mm; Po0.05) skinfolds, the sum of biceps and triceps (24.8±8.3 vs 21.4±11.7 mm; Po0.05), hip circumference (80.9±9.3 vs 77.2±8.8 cm; Po0.05) and percentage of body fat (23.3±6.0 vs 19.9±7.4%, Po0.05) and less percentage of fat-free mass (76.7±6.0 vs 80.1±7.4%, Po0.05) than boys. European Journal of Clinical Nutrition


464 Table 1 Dietary characteristics of the schoolchildren with respect to their serum 25(OH)D concentrations ID group (n ¼ 89) Mean

s.d.

AD group (n ¼ 10) Mean

Table 2 Personal and anthropometric variables measured with respect to serum 25(OH)D concentration ID group (n ¼ 92) AD group (n ¼ 10) P-value*

P-value*

Age (years) Energy Intake (kcal/day) Discrepancy intake/ expenditure (kcal) Discrepancy intake/ expenditure (%) Energy profile Proteins (% energy) Carbohydrates (% energy) Lipids (% energy) Food groups (servings/day) Cereals and pulses Greens and vegetables Fruits Milk products Meat, fish and eggs Vitamin D intake (mg/day) Intake o67 RI (%) Calcium (mg/day)

2007 332 1903 307 15.1 476.0 149.6 340.4

0.345 0.503

3.48 23.37

9.25 18.41 0.586

15.79 40.20 42.59

2.30 4.92 4.52

16.31 41.04 41.39

4.43 1.85 1.30 2.33 3.47

1.47 1.11 0.89 0.74 1.37

3.71 1.47 1.30 2.36 3.46

2.63 2.86 80.4 881.21 204.23

3.14 0.513 5.63 0.616 4.43 0.426

1.20 1.03 0.55 0.55 1.40

0.141 0.309 0.997 0.892 0.987

4.61 5.69 0.094 60 886.10 102.02 0.871

Abbreviations: 25(OH)D, 25-hydroxyvitamin D; AD group, subjects with 25(OH)D of X70 nmol/l (adequate levels); ID group, subjects with 25(OH)D of o70 nmol/l (insufficient levels); RI, recommended intake. *P-values of o0.05 indicate significant differences between ID and AD group.

No significant differences in either physical activity coefficient (1.47±1.22 vs 1.41±0.08; P ¼ 0.08) or time exposure to the sun (9.61±3.07 vs 9.83±3.44 h/week; P ¼ 0.269) were observed between the ID and AD subjects. Tables 1 and 2 show the dietary, personal and anthropometric variables of the ID and AD subjects. The mean serum 25(OH)D concentration of the ID subjects was 46.6±13.4 nmol/l, and it reached 77.5±8.4 nmol/l in the AD subjects (Po0.001). Despite these differences, no significant difference was observed between the groups in terms of vitamin D intake (Table 1). However, the ID subjects had a significantly higher body weight, BMI, waist measurement and waist/height ratio than the AD subjects (Table 2). Using a multiple linear regression analysis with serum 25(OH)D values as the dependent variable and with confounding variables taken into account, only weight and BMI were found to independently influence these values (Table 3). The children with a body weight, BMI, bicipital skinfold thickness, waist measurement and waist/height ratio above the 50th percentile for each variable were at a greater risk of having a low serum 25(OH)D concentration (op90 or 70 nmol/l; Table 4). Particularly, children with weight higher than 38.3 kg, BMI higher than 16.68 kg/m2, bicipital skinfold thickness higher than 7.15 mm, waist higher than 65.9 cm and waist/height ratio higher than European Journal of Clinical Nutrition

Mean

s.d.

Mean

s.d.

10.9

1.0

11.1

1.1

0.655

3.2 0.1 10.2 8.5 3.7 7.1 4.8 7.1 6.3 6.8 4.0 10.5 9.6 0.07 0.06

50 8.1 1.4 34.6 144.3 16.6 19.0 6.7 81.0 27.9 12.1 6.0 18.1 61.7 0.83 0.43

3.5 0.1 5.0 6.65 1.7 3.6 1.9 3.6 3.4 2.7 1.6 4.2 4.8 0.03 0.03

0.458 0.09 0.035 0.836 0.007 0.129 0.072 0.129 0.059 0.158 0.113 0.120 0.031 0.381 0.024

s.d.

Sex Boys (%) 47.8 Sun exposure (h/week) 8.9 Physical activity coefficient 1.5 Weight (kg) 41.3 Height (cm) 144.8 2 BMI (kg/m ) 19.5 BF (%) 22.0 BF (kg) 9.5 FFM (%) 78.0 FFM (kg) 31.7 Triceps (mm) 15.5 Biceps (mm) 8.2 Triceps þ biceps (mm) 23.7 Waist (cm) 67.8 Waist/hip 0.85 Waist/height 0.47

Abbreviations: 25(OH)D, 25-hydroxyvitamin D; AD group, subjects with 25(OH)D of X70 nmol/l (adequate levels); BF, body fat; BMI, body mass index; FFM, fat-free mass; ID group, subjects with 25(OH)D of o70 nmol/l (insufficient levels). *P-values of o0.05 indicate significant differences between ID and AD group.

Table 3 Regression results using serum 25(OH)D concentration value as the dependent variablea

Weight (kg) Height (m) BMI (kg/m2) %BF %FFM Triceps (mm) Biceps (mm) Triceps þ biceps (mm) Waist (cm) Waist/hip ratio Waist/height ratio

Constant

Standard error

P-value

0.32 10.1 0.93 0.01 0.01 0.05 0.20 0.05 0.21 1.3 30.2

0.16 19.87 0.43 0.24 0.24 0.25 0.42 0.16 0.17 24.6 27.4

0.046* 0.612 0.032* 0.969 0.969 0.854 0.634 0.765 0.222 0.958 0.267

Abbreviations: 25(OH)D, 25-hydroxyvitamin D; BF, body fat; BMI, body mass index; FFM, fat-free mass. *P-values of o0.05 indicate significance. a Confounding variables (vitamin D intake, underestimation of energy intake, sunlight exposure, age and sex) have been taken into account in the statistical analysis.

0.45 had 16.4, 4.7, 4.9, 5.1 and 5.3 times more risk, respectively, than children with weight lower than 38.3 kg, BMI lower than 16.68 kg/m2, bicipital skinfold thickness lower than 7.15 mm, waist lower than 65.9 cm and waist/ height ratio lower than 0.45.


465 Table 4 Risk of having a serum 25(OH)D concentration of o70 nmol/l with respect to being above the 50th percentile for the anthropometric variables measured Variable measured Weight (p50 ¼ 38.3 kg) Height (p50 ¼ 1.45 m) BMI (p50 ¼ 18.68 kg/m2) %BF (p50 ¼ 21.88 %) %FFM (p50 ¼ 78.11%) Triceps (p50 ¼ 14.8 mm) Biceps (p50 ¼ 7.15 mm) Triceps þ biceps (p50 ¼ 21.5 mm) Waist (p50 ¼ 65.9 cm) Waist/hip ratio (p50 ¼ 0.84) Waist/height ratio (p50 ¼ 0.45)

Odds ratio (95% CI)a 16.4 1.9 4.7 2.7 0.37 1.7 4.9 2.7 5.1 1.1 5.3

(1.5–177) (0.48–7.7) (0.93–24.0) (0.53–13.8) (0.07–1.90) (0.44–6.7) (0.96–24.5) (0.64–11.3) (1.0–25.9) (0.28–4.7) (1.1–26.9)

P-value* 0.002 0.199 0.037 0.527 0.527 0.228 0.033 0.115 0.029 0.310 0.025

Abbreviations: 25(OH)D, 25-hydroxyvitamin D; BF, body fat; BMI, body mass index; FFM, fat-free mass; p50, 50th percentile for each variable. a Confounding variables (vitamin D intake, underestimation of energy intake, sunlight exposure, age and sex) have been taken into account in the statistical analysis. *P-values of o0.05 indicate significance.

Discussion Some 87.9% of the studied children failed to take in the quantity of vitamin D recommended for their age. This partly explains the high percentage (90.2%) who showed serum 25(OH)D concentrations of o70 nmol/l (that is, below the minimum value recommended for the maintenance of good metabolic health and considered as insufficient; Talwar et al., 2007; Vieth et al., 2007; McGill et al., 2008). This finding agrees with that reported in other studies with children, the researchers of which indicate that irrespective of whether their country is sunny, children’s exposure to the sun would seem to be low and the dietary intake of vitamin D inadequate (Gordon et al., 2008; Mark et al., 2008; Bener et al., 2008a, b). Although exposure to the sun is essential for the cutaneous manufacture of vitamin D (Millen and Bodnar, 2008), exposure times were not different between ID and AD group. It could be because of the fact that the subjects studied were children and all followed the same school timetable, and thus their levels of sun exposure were very similar. In addition, the study was undertaken during winter, a season during which the diet, rather than ultraviolet light, has been reported to be the main source of vitamin D (Cashman, 2007). In addition, sufficient time since the summer had elapsed for ultraviolet-light-induced vitamin D levels to have fallen (Rucker et al., 2002), and above 351 north latitude, little or no vitamin D3 is produced from November to February because of sun exposure (Webb et al., 1988; Holick et al., 2005). The serum 25(OH)D concentrations were significantly different in the ID and AD groups, although vitamin D intake was similar in both (although below that recommended in both; Table 1). No significant differences

were observed between the groups in terms of the consumption of milk products, meat, fish or eggs—the main dietary sources of vitamin D (Gannage´-Yared et al., 2005; LambergAllardt, 2006; Lu et al., 2007; Lee et al., 2008b). There were not any differences observed in calcium intake (Table 1), despite the fact that a low calcium intake has been associated with inadequate vitamin D status (Heaney, 2008). The differences in serum vitamin D levels between the groups might be explained by their members’ different amounts of body fat (Table 2). A number of studies have reported a negative association between serum 25(OH)D concentration and body fat (Alemzadeh et al., 2008; McKinney et al., 2008; Kremer et al., 2009), perhaps due to the sequestration of the vitamin by the fat (Liel et al., 1988). Several studies performed on adults have reported a negative relationship between BMI and serum levels of vitamin D (Need et al., 2005; Konradsen et al., 2008; Kremer et al., 2009; Rodrı´guez-Rodrı´guez et al., 2009), and the same has been reported for children and adolescents (Alemzadeh et al., 2008; Bener et al., 2008a, b). In a group of 127 children and adolescents, Alemzadeh et al. (2008) observed that those with serum 25(OH)D concentrations of o75 nmol/l had a greater BMI than those with higher concentrations (38.2±8.9 vs 33.9±6.0 kg/m2; Po0.02). The same was observed in the present work (Tables 2–4). Although several studies have detected a relationship between whole body obesity (defined by the BMI) and serum vitamin D levels (Need et al., 2005; Konradsen et al., 2008), few have analyzed the relationship between serum levels of the vitamin and the distribution of body fat, and none have examined this in schoolchildren. In a study involving women aged 19.4±1.5 years, it was found that the serum 25(OH)D concentration was not only inversely correlated with total fat, but also with visceral fat and subcutaneous fat, suggesting that this relationship was independent of the site of fat accumulation (Kremer et al., 2009). However, the present results showed the amount of visceral or abdominal fat, reflected by the waist measurement (Pajuelo et al., 2004), and the waist/height ratio (Ashwell et al., 1996a, b) to be greater in the ID than in the AD subjects, whereas no differences were observed between these groups in terms of the amount of subcutaneous fat, as reflected by the tricipital skinfold thickness and the sum of tricipital and bicipital skinfold thickness (Tables 2 and 4). This result is similar to that reported by McGill et al. (2008) in adults; these researchers also found an inverse relationship between waist measurement and serum vitamin D levels (r ¼ 0.14, P ¼ 0.03). The present results suggest that it is the amount of visceral and not subcutaneous fat that determines the serum level of vitamin D in children. In fact, the children with the highest waist and waist/height values (450th percentile) were at a greater risk of having a serum 25(OH)D concentration of o70 nmol/l (Table 4). Visceral adipose tissue may have a greater metabolic activity than its subcutaneous counterpart (Matsuzawa, 2008); the sequestration of vitamin D by the former is therefore likely to be European Journal of Clinical Nutrition


466 greater. More studies are needed to test this hypothesis and to confirm the present findings. The present study suffers from the limitation that no information was recorded on the degree of sexual maturity of the children studied (Tanner-stage; Tanner, 1962). This could act as a confounding factor, as puberty may have started in some but not all children. In conclusion, the results of the present work suggest that the BMI and visceral or abdominal obesity influence the appearance of vitamin D insufficiency in children. Children should be monitored for this insufficiency, which might help in preventing the appearance of associated disease (Holick, 2005).

Conflict of interest The authors declare no conflict of interest.

Acknowledgements This work was supported by the FISS project (PI060318).

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