Introduction

In recent years, a growing number of studies have been done on vitamin D because of its skeletal and non-skeletal health impacts as well as the high prevalence of its deficiency in all age groups. It is well documented that low levels of vitamin D are associated with an increased risk of various clinical outcomes including type 1 diabetes mellitus [1], colorectal and prostate cancers [2], autoimmune diseases [3, 4], insulin resistance [5], obesity [6], cardiovascular diseases [7], infectious diseases [3], and chronic obstructive pulmonary disease (COPD) [8]. It is estimated that more than 1 billion people have an insufficient level of 25-hydroxyvitamin D (25(OH)D) [9].

On the other hand, the prevalence of weight disorders is increasing in the pediatric population [10]. Some studies proposed that vitamin D deficiency might have a role in the pathogenesis of metabolic syndrome and obesity [11, 12]. Several studies evaluated the association of vitamin D status with cardio-metabolic risk factors [13] and anthropometric indices including body mass index (BMI), waist circumference (WC), waist to height ratio (W/HtR), hip circumference (HC) [12, 14,15,16], wrist circumference (WrC) [17], neck circumference (NC) [18] and in various age groups, however, limited experience exists in the pediatric age group.

Moreover, studies are mostly from Western countries and few data are available from Asian countries, in particular from the Middle East countries, where the prevalence of vitamin D deficiency is found to be high [19,20,21].

This study aims to determine the association between vitamin D status and different anthropometric variables in a large representative sample of Iranian children and adolescents.

Methods and materials

Study population

This study was performed in 2019 as a sub-study of the fifth national survey on school students’ high-risk behaviors and the school-based surveillance system entitled Childhood and Adolescence Surveillance and PreventIon of Adult Non-communicable disease (CASPIAN-V). This school-based nationwide health survey was conducted in both urban and rural regions in 30 provinces of Iran. Protocol details of the study have been explained previously [22].

Ethical concerns

The study protocols were reviewed and approved by ethical committees and other relevant national regulatory organizations. The Research and Ethics Committee of the Isfahan University of Medical Sciences approved the main study (project number: 194049). The current study was conducted on sera of a sub-sample of the main study; it was approved by the National Institute for Medical Research Development (NIMAD) (code: 962514). After a complete explanation of the aim of the study and protocols for students and their parents, written informed consent and oral assent were obtained from the parents and the students, respectively.

Assessment of anthropometric measures

Physical examination and face-to-face interviews were conducted by a team of trained health-care experts in a calm room of the school. Trained health-care professionals measured weight, height, waist circumference (WC), hip circumference (HC), neck circumference (NC), and wrist circumference (WrC) of students using calibrated instruments with standard methods. WC was measured using a non-elastic tape on the distance around the mid-point between the lower margin of the last palpable rib and the top of the iliac crest at the end of normal expiration, to the nearest 0.1 cm. The widest part of the buttocks was measured to obtain HC to the nearest 0.1 cm. Wrist circumference (WrC) was measured by placing the superior border of the tape measure distal to the prominences of radial and ulnar bones, with 0.1 cm accuracy. NC was measured with the most prominent portion of the thyroid cartilage taken as a landmark, with 0.1 cm accuracy. Body mass index (BMI) was calculated by dividing weight (kg) by height squared (m2). Waist-to-height ratio (W/HtR) was calculated as WC (cm) divided by height (cm) [23].

Biochemical assessment

The serum concentration of 25(OH)D was determined among a randomly selected sample of frozen sera (− 70 °C) of participants. They were analyzed quantitatively by direct competitive immunoassay chemiluminescence method applying LIASON®25 OH vitamin D assay TOTAL (DiaSorin, Inc.), with a coefficient of variation of 9.8%. 25(OH)D level of less than 10 ng/ml was considered as vitamin D deficiency and levels between 10 and 30 ng/ml as vitamin D insufficiency [24].

Definition of terms

The physical activity (PA) was measured through a validated questionnaire [25] including weekly frequency of leisure-time physical activity outside the school during the past week, and having sufficient physical activity was defined as at least 30 min of exercise per day that led to sweating or large increases in breathing or heart rate. For the sake of statistical analysis, each weekly frequency received a classification (Low PA was < 2 h/week; moderate, 2 to 4 h/week; and high > 4 h/week.).

To assess screen time (ST) behaviors, the students were asked to report the number of hours per day that they spent watching television and/or videos, using their personal computer or playing electronic games. The total cumulative time spent on ST was calculated accordingly. Low ST was defined as less than 2 h per day, and high ST was defined as spending more than 2 h per day.

Socioeconomic status (SES) included father’s job and education, mother’s job and education, type of home (private/rented), having private car and computer, and type of student’s school (private, governmental) variables using one main component, by principal component analysis (PCA) method. It was categorized into tertiles and the lowest tertile considered as a low SES and the third tertile as a high SES.

Statistical analysis

Data analysis was performed using STATA version 11.0 (STATA Statistical Software: Release 11. StataCorp LP. Package, College Station, TX, USA). The normality of continuous variables was assessed using the Kolomogrov–Smirnov test and due to lack of normality, 25 (OH) D is presented as median (inter-quartile range). T test and Mann–Whitney U test were used to compare continuous variables with and without normal distribution according to gender. Association of vitamin D status with anthropometric measures was assessed using the analysis of variance (ANOVA) test. Correlation between 25 (OH) D concentration and anthropometric measures was assessed using the Spearman correlation test. Linear regression analysis was applied to evaluate the association of 25(OH)D status with anthropometric measures. Three models were defined: Model I represented the crude association, Model II was adjusted for age, gender, and living area, and Model III was additionally adjusted for ST, PA, SES, and vitamin D supplementation. P value of less than 0.05 was considered as statistically significant.

Results

The data of 2596 children and adolescents aged 7–18 years were analyzed. They consisted of 55% (n = 1430) boys and 71.3% urban inhabitant. The mean (SD) age of participants was 12.1 (3.0) years; 33.5%, 41.9%, and 24.5% of participants were in the 7–10, 11–14 and 15–18 age range groups, respectively. Prevalence of vitamin D deficiency, insufficiency and sufficiency were 10.6%, 60.4%, and 29%, respectively. No significant difference existed between boys and girls in terms of vitamin D status.

The anthropometric indices and 25(OH)D of both genders are presented in Table 1. The mean age, weight, height, WC, NC, and WrC were significantly higher in boys (P < 0.05). BMI, W/HtR, HC, and concentration 25(OH)D were not statistically different in terms of gender. The mean values of anthropometric indices according to vitamin D status are presented in Table 2. The mean of BMI and WC was higher in the vitamin D deficient group compared to the sufficient group (P < 0.01). No significant difference was found in the HC, NC, and WrC among groups. Table 3 shows the correlation between 25(OH)D concentrations and anthropometric measures. Among anthropometric indices, WC and W/HtR were negatively correlated with 25(OH)D concentration (P < 0.05).

Table 1 Anthropometric indices and 25(OH)D concentration by gender
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Table 2 Mean (SD) of anthropometric indices according to vitamin D status
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Table 3 Pearson correlation coefficient between anthropometric measures and 25(OH)D concentration
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The association between vitamin D status and anthropometric indices are presented in Table 4. In the multivariate models (model III), vitamin D insufficiency was associated with WC and W/HtR (P < 0.05). Likewise, in the multivariate model, vitamin D deficiency was associated with BMI, WC, and W/HtR (P < 0.05). There was no association between HC, NC, and WrC with vitamin D status.

Table 4 Association of anthropometric indices with vitamin D status in linear regression analysis
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Discussion

To the best of our knowledge, this is the first study of its kind about the association of vitamin D status and anthropometric measures in a nationwide pediatric population of a non-Western country. In addition to a considerably high prevalence of vitamin D deficiency and insufficiency, we found significant associations between hypovitaminosis D and some anthropometric measures, notably the indices of generalized and abdominal obesity. Approximately 70% of participants in our study were vitamin D deficient or insufficient. The mean of BMI and WC in subjects with sufficient vitamin D level were significantly lower than those with deficient vitamin D level. In addition, WC and W/HtR were significantly associated with vitamin D deficiency and insufficiency.

Previous surveys in different cities in Iran showed vitamin D deficiency varies from 41.3% to > 90% [26, 27]. Increased urbanization, air pollution, increased time spent in-doors, sun-protective behaviors, overweight or obesity is the reasons for vitamin D deficiency in children and adolescents [28]. We found no significant difference in vitamin D status between boys and girls. However, some studies found a higher prevalence of undesirable vitamin D status in girls compared with boys. These results were justified by the higher sun exposure and outdoor activities of boys than girls, as well as the pattern of girls’ growth spurt during puberty [27, 29, 30]. Another study found it more prevalent among males than in females [31] and in another one, no difference was found according to gender, rather the age was reported as an important factor for vitamin D status [32]. Our finding on the similar prevalence of low levels of 25(OH)D in boys and girls in a sunny region is confirmatory evidence that environmental factors, mainly air pollution, are important determinants of hypovitaminosis D, as documented in some previous study in Iran [33, 34].

In the present study, the association between the anthropometric obesity-related indices and vitamin D status was documented. Data obtained from 2000 to 2013 studies showed a prevalence rate of 5.5% for obesity and 15.1% for overweight among the Iranian pediatric population [35]. In the current study, the mean of BMI and WC were higher in the vitamin D deficient group compared with insufficient groups. Moreover, 25 (OH) D concentrations had an inverse correlation with indices of abdominal obesity, i.e. WC and W/HtR.

Some previous studies indicated that plasma 25(OH)D concentration was inversely associated with BMI [18] and WC [36, 37] in children. A study on 102 Spanish children, aged 9–13 years, showed that children with insufficient vitamin D had higher body weight, BMI, WC, and W/HtR than those with adequate vitamin D levels. Multiple linear regression analysis showed only weight and BMI were independently associated with 25(OH)D values [37]. In another study in Mexican children, BMI and WC were the predictors of 25 (OH) D concentrations [36]. Despite several studies on the association between vitamin D status and obesity, findings are conflicting. Some studies have shown an inverse association between serum 25(OH)D concentrations and obesity, while others did not [38,39,40]. Despite conflicting results in the pediatric population, it seems that similar to adults, vitamin D status is more strongly associated with abdominal obesity than with generalized obesity. Moy et al. have reported that vitamin D insufficiency was independently associated with greater abdominal obesity in Malaysian adults [41]. Likewise, Cheng et al. reported that lower 25(OH)D levels were strongly associated with greater regional adiposity in the Framingham Heart Study [42]. In parallel with the increasing prevalence of vitamin D deficiency, the prevalence of obesity also is rising [12, 43]. Although mechanisms of association between vitamin D and adiposity are unknown, some studies showed that vitamin D supplementation led to up-regulation genes involved in fatty acid oxidation and the activation of the calcium-mediated apoptotic pathway in adipose tissue, which stimulates lipogenesis in isolated human adipocytes. Thus, vitamin D could influence body weight and energy expenditure through calcium regulation [44]. Among the non-calcemic effects of vitamin D, the significant role is played by its impact on the hormonal regulation of glucose metabolism and the synthesis of adipokines by fat tissue. The accumulation of adipose tissue, impaired adipocyte function, development of adipocyte hypertrophy, and altered adipokine secretion profile result in migration and transformation of macrophages and development of adipose tissue inflammation. As a result of this inflammation, the synthesis of pro-inflammatory cytokines (TNF-alpha, IL-6, and IL-1b) becomes increased and insulin resistance develops [45]. Some in vitro studies have also shown that vitamin D can decrease the expression of peroxisome proliferator-activated receptor-gamma (PRAPγ) and vitamin D receptor (VDR) in adipocytes and therefore inhibits adipogenesis [46]. In addition, the association of obesity with low levels of 25(OH)D might be attributed to decreased exposure to sunlight because of the limited mobility of obese people [47]. A longitudinal study on male students aged 12–16 years did not show any significant association between vitamin D levels changes and anthropometric measurements after 18 weeks of a weight reduction intervention [48]. A review article demonstrated that vitamin D replacement treatment with different formulations had a possible role to restore normal levels of vitamin D in obese subjects and might have positive impacts on obesity and its metabolic consequences [49].

Study limitations and strengths: There are some limitations to our study. It was not possible to provide a causal relationship between variables because of the cross-sectional nature of our study. Moreover, we could not examine the pubertal status, which might affect vitamin D status and anthropometric indices. Some confounding factors such as physical activity, outdoor activities, seasonal change, and sun exposure that could interfere in both vitamin D status and obesity should be considered in future studies. Despite these limitations, our study has novelty in the pediatric population of non-Western countries. The other strengths are including a large sample size and adjustment of associations for confounding factors as sedentary activities and SES.

Conclusion

Our findings on inverse association between vitamin D status and some anthropometric measures, mainly indices of abdominal obesity, serve as confirmatory evidence of the reciprocal interaction of vitamin D and adiposity. This study underscores the importance of providing vitamin D by fortification and supplementation programs of vitamin D for the pediatric population.

What is already known on this subject?

Several studies evaluated the association of vitamin D status with anthropometric in various age groups, however, there are limited evidence in the pediatric age group.

What does this study add?

The inverse association was founded between vitamin D status and some anthropometric measures.