Introduction

Obesity has been a global epidemic public health issue during the past decades that imposes a large burden to the healthcare system [1]. Epidemiological studies have shown that 55% of adult population in US are overweight or obese [2]. In Iran, it has been estimated that about half of adult population are affected [3]. Obesity is a known risk factor for diabetes, hypertension, osteoarthritis, coronary heart disease (CHD) and some cancers [1, 4, 5]. In addition to general obesity, distribution of fat in body is also important. Abdominal obesity has been associated with a greater risk of metabolic diseases and mortality [6, 7]. Therefore, the assessment of contributing factors for general and abdominal obesity is of great importance.

It seems that genetic and environmental factors contribute to the obesity epidemic [8]. Several studies have focused on micronutrients deficiencies [9,10,11]. Among micronutrients, vitamin D has received a great attention [12,13,14]. Serum 25(OH)D concentrations have been reported to be inversely associated with impaired glucose regulation, insulin resistance, β-cell dysfunction, and risk of metabolic syndrome [15, 16]. Vitamin D may provide mentioned favourable effects by affecting on adipose tissue. In an experimental study, it had been shown that vitamin D intake led to the activation of calcium-mediated apoptotic pathway in adipose tissue and counteraction of body and fat weight gain [17]. In another similar study, vitamin D up-regulated genes involved in fatty acid oxidation and mitochondrial metabolism, followed by a significant rise in energy expenditure [18]. Therefore, vitamin D deficiency may have a role in the obesity epidemic. On the other hand, in parallel in the increasing prevalence of vitamin D deficiency, the prevalence of obesity also is rising [19, 20]. Therefore, to shed light facts on the association between vitamin D deficiency and obesity, further studies are required.

Despite of 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 [21, 22], while others failed to find any significant relationship [23]. Moreover, prior studies are mostly from western countries and few data are available from Asian countries, in particular from the understudies region of the Middle Eastern. In mentioned area, the prevalence of vitamin D deficiency has been estimated to be high [24, 25]. Furthermore, assessing obesity is particularly relevant for Middle Eastern population, due to the prevalence of a Middle Eastern pattern of obesity, characterized by abdominal fat accumulation and enlarged waist circumference (WC) [26]. Furthermore, mentioned association might be important among high educated individuals who are socioeconomically different than others. Therefore, current study aimed to assess the association of vitamin D status with general and abdominal obesity among high educated Iranian adults.

Subjects and methods

Participants

Current study was cross-sectional which was performed on all professors (assistant, associate and full faculty members) affiliated to Tarbiat Modares University, Tehran, Iran. First, 500 faculty members, aged 35 years or more, were invited to Health Center of Tarbiat Modares University by sending invitation letter via Email, SMS and post. Among them, 360 persons agreed to take part in the study. Required data on demographic variables along with anthropometric measurements and dietary habits were collected from each participant between December 2016 and March 2017. In addition, fasting blood sample was taken to assess vitamin D status. Participants were excluded if had chronic diseases affecting their diet, followed an arbitrary special dietary regimen such as weight loss diet or were pregnant and lactating during the previous year. In addition, we excluded participants who had a history of vitamin D supplementation or presented incomplete data. Finally, 352 participants (including 295 men and 57 women) remained for the final analysis. All participants were willing to participate in the current study and provided a written informed consent. The study was approved by Board of Directors and the ethics committee of Tarbiat Modares University, Tehran, Iran.

Dietary assessment

We used some questions to assess consumption frequency of some food items affecting the association of vitamin D status with general and abdominal obesity. These questions were about frequency of fruits intake (rarely, < 2 serv/day, 2–4 serv/day, > 4 serv/day), vegetables (rarely, < 3 serv/day, 3–5 serv/day, > 5 serv/day), dairy products (rarely, < 2 serv/day, 2–3 serv/day, > 3 serv/day), meat (rarely, < 2 serv/day, 2–3 serv/day, > 3 serv/day), red meat (daily, < 1 time/day), whole grains (rarely, 1 time/week, 2–3 times/week, ≥ 1 time/day) and refined sugar (rarely, 1 time/week, 2–3 times/week, ≥ 1 time/day). Because of infrequently consumption of whole grains in Iranian food culture [27], we changed the four response categories to two categories as “weekly” and “<1 time/week”. In the current study, whole-grain foods were defined as wheat, diet bread and dark breads including Iranian breads of Sangak and Barbari. In addition, red meat was defined as beef, veal, mutton and lamb, dairy products as milk, cheese, yogurt and dough (yogurt drink) and refined sugar as sweets, cakes and biscuits. To include dietary intakes with the four response categories into the multivariate analysis, we considered two of the first categories as “low intake” and two of the last categories as “adequate intake”.

Biochemical assessment

To quantify serum concentrations of 25(OH)D, we collected blood samples after a 12-h overnight fast. Blood sampling was done in winter. Venous blood samples were drawn into 10-mL syringes and then centrifuged for 10 min at 500 g at 4C within 30 to 45 min of collection. Serum 25(OH)D levels were assessed by a commercial ELISA kit (IDS). Participants were classified into three categories based on serum levels of 25(OH)D: vitamin D sufficient (≥ 30 ng/ml), insufficient (20–29 ng/ml) and deficient (< 20 ng/ml) [28].

Anthropometric assessment

Weight was measured with minimal clothing and without shoes by analogue scale with a precision of 100 g and height was determined in a standing position without shoes by a tape measure with the nearest 0.5 cm. Body mass index (BMI) was calculated as weight in kilograms divided by height in square meters. Obesity was considered as body mass index ≥ 30. To measure waist circumference (WC), we measured the middle of bottom ribs and pelvic bones after a normal exhale using an inelastic tape. Abdominal obesity was defined based on criteria reported by Lean et al. and the National Cholesterol Education Program (NCEP), respectively [29, 30]. Participants were categorized into 2 groups: normal (< 80 cm for women, < 94 cm for men) and abdominaly obese (≥ 80 cm for women and ≥ 94 cm for men).

Assessment of other variables

Data on age, marital status (single/married), smoking (non-smoker/former smoker/current smoker) and sleep pattern was obtained using a pre-tested questionnaire. In terms of sleep pattern, participants were asked two questions as follow: “how is your pattern of sleeping and awaking?” and “how many hours do you sleep in a day?” The response categories for the first question were “regular”, “irregular” and for the second question were as follow: “<6 h/day”, “6–8 h/day”, “8–10 h/day”, >10 h/day. To assess physical activity, we asked a question as follow: “how often do you exercise lasting 30 min?” The response categories of this question was “rarely”, “1–2 times/week”, “3–4 times/week”, “>5 times/week”. We collected no information about economic status of participants due to favourable economic status of faculty members.

Statistical analysis

First, we categorized participants according to quartiles of serum 25(OH)D concentrations and also standard ranges of 25(OH)D levels [sufficiency (≥ 30 ng/ml), insufficiency (20–29 ng/ml), deficiency (< 20 ng/ml)]. One-way analysis of variance (ANOVA) was applied to assess significant differences in continuous variables across categories of serum 25(OH)D concentrations. To assess the distribution of participants in terms of categorical variables across categories of serum 25(OH)D, we used Chi-square test. Binary logistic regression in different models was applied to assess the association of serum 25(OH)D with general and abdominal obesity. In the first model, age (continuous) and gender were controlled. Additionally, adjustment was made for marital status (single/married), physical activity (< 3/> 3 times/week), smoking (non-smoker/former smoker/current smoker) and sleeping pattern (regular/irregular) in the second model. In the final model, further controlling was done for dietary intakes of fruits (< 2/> 2 serv/day), vegetables (< 3/> 3 serv/day), dairy (< 2/> 2 serv/day), red meat (daily/< 1 time/day), whole grains (weekly/< 1 time/week) and refined sugar (< 2/> 2 serv/day). In all analyses, participants in the first quartile of serum 25(OH)D or with the normal levels of 25(OH)D (≥ 30 ng/ml) were considered as the reference group. To determine the overall trend of odds ratios across increasing categories of serum 25(OH)D, we considered these categories as an ordinal variable in the logistic regression models. All statistical analyses were performed using SPSS software (version 19.0; SPSS Inc, Chicago IL). P values were considered significant at < 0.05.

Results

Mean age of study population was 53.03 ± 7.15 years. Vitamin D deficiency was prevalent among 60.5% of participants. In addition, 20.3% of participants were affected by general obesity and 54.5% were abdominally obese.

General characteristics of faculty members across categories of serum 25(OH)D are indicated in Table 1. Compared with the lowest quartile, participants in the highest quartile of serum 25(OH)D were older, more likely to be females and had lower weight and BMI. In addition, the prevalence of smoking was different across quartiles of serum 25(OH)D. In terms of standard ranges of vitamin D, participants with vitamin D deficiency had higher weight, BMI and WC compared with those who were vitamin D sufficient. No other significant difference was found for general characteristics across categories of serum 25(OH)D concentrations.

Table 1 General characteristics and dietary intakes of participants across categories of serum 25(OH)D concentrations
Full size table

Multivariable adjusted odds ratios and 95% confidence intervals for general and abdominal obesity across categories of serum 25(OH)D concentrations are presented in Table 2. Compared with those in the first quartile of serum 25(OH)D, participants in the fourth quartile were less likely to be generally obese (OR 0.46, 65% CI 0.22–0.99); such that after taking potential confounders into account, individuals in the highest quartile of serum 25(OH)D had 60% less odds for having general obesity compared with those in the lowest quartile (OR 0.40, 95% CI 0.17–0.91). In terms of abdominal obesity, when the potential confounders were controlled, a significant inverse association was found between serum 25(OH)D and abdominal obesity; such that participants in the top quartile of serum 25(OH)D had 56% less likely to be abdominally obese compared with those in the bottom quartile (OR 0.44, 95% CI 0.22–0.86). In addition, a significant positive association was found between vitamin D deficiency and both kinds of obesity; such that after controlling for potential confounders, participants with vitamin D deficiency had 2.16 and 2.04 times greater odds for having general (OR 2.16, 95% CI 1.05–4.45) and abdominal obesity (OR 2.04, 95% CI 1.16–3.60), respectively, than those with normal levels of vitamin D.

Table 2 Multivariable adjusted odds ratios and 95% confidence intervals for general and abdominal obesity based on categories of serum 25(OH)D concentrations
Full size table

Discussion

In this study, we found a significant inverse association between serum 25(OH)D concentrations, general and abdominal obesity. Such finding was significant even after adjusting for confounding variables. In addition, participants with vitamin D deficiency were more likely to be generally and abdominally obese compared with those with normal levels of vitamin D when potential confounders were taken into account. To the best of our knowledge, this study was the first in Middle East to examine the association between vitamin D deficiency and obesity among high educated adults.

The World Health Organization has projected that there are approximately 1.5 billion overweight adults around the world [31]. Taking into account the association between vitamin D deficiency and obesity, these two conditions might constitute important health issues in future years. Based on our findings, serum 25(OH)D concentrations were inversely associated with general and abdominal obesity. In line with our findings, Zhang et al. reported a significant inverse association between serum 25(OH)D levels and obesity, particularly abdominal obesity [21]. In a cross-sectional study, an inverse relationship was reported between serum 25(OH)D levels and risk of metabolic obesity among male subjects [13]. In a systematic review and meta-analysis, it had been shown that vitamin D intake improved the cardiovascular risk factors in adults with obesity [32]. Another study, done by Afzal et al. showed that the low plasma 25(OH)D concentrations might be a modest mediator between obesity and increased risk of diabetes [22]. In contrast, Khan et al. failed to find any significant association between vitamin D status and obesity [23]. Finding no significant association in that study might be due to low quality of this study and lack of adjustment for confounding variables.

The prevalence of obesity has been increasing at an alarming rate [20]. Recently, the effects of low concentrations of serum 25(OH)D on imprinting during childhood and adolescence and subsequent occurrence of bone diseases have been assessed, along with the growing risk of development of metabolic syndrome and cardiovascular, respiratory and psychological disorders [33, 34]. On the other hand, vitamin D deficiency predisposes the adults to increased risk of chronic diseases such as hypertension, diabetes, cardiovascular diseases, different types of cancer and excess weight [35,36,37]. In Third National Health and Nutrition Examination Survey (NHANES III), after a median follow-up of 19.1 years, vitamin D deficiency was associated with increased risk of cardiometabolic diseases and mortality in both normal-weight and obese participants [38]. Mentioned findings were confirmed by some clinical trials showing vitamin D supplementation increases insulin sensitivity [39], improves glucose homeostasis [40], decreases the leptin and increases the adiponectin levels [41, 42], and followed by a rise in energy expenditure [18]. Furthermore, in a meta-analysis, it had been shown that vitamin D supplementation decreased the incidence of Type 1 diabetes by 25% [43]. In the current study, the prevalence of vitamin D deficiency was high (60.5%). However, individuals participated in this study was high educated. Therefore, it seems that high education level is not a reason for the lack of nutritional deficiencies.

Different theories can be proposed to explain that vitamin D deficiency might favour greater adiposity. Vitamin D deficiency increases parathyroid hormone levels and greater inflow of calcium into adipocytes. Both conditions induce lipogenesis [44]. Accumulated evidence showed that 1.25(OH)D inhibits adipogenesis by actions modulated by vitamin D-dependent receptors [45]. In an experimental study, murine 3T3-L1 pre-adipocytes exposed to vitamin D and/or alendronate (ALN), showed an increment in vitamin D receptors (VDR) mRNA expression and a significant reduction in levels of peroxisome proliferator-activated receptor gamma (PPARγ), the master gene of adipogenesis [46]. Murine 3T3-L1 pre-adipocytes are one of the best characterized and widely used cellular models to study adipocyte differentiation [47]. Vitamin D deficiency might lead to excessive differentiation of pre-adipocytes to adipocytes [48]. In addition, a study on a diet-induced obesity in mouse models revealed that intake of high doses of vitamin D, especially if associated with high intake of calcium, leads to the activation of calcium-mediated apoptotic pathway in adipose tissue, reduction of body and fat weight gain, and improvement in adiposity markers (plasma concentrations of glucose, insulin, and adiponectin) [17].

Vitamin D is a fat-soluble vitamin that is stored in adipose tissue and released in small amounts from this tissue, depending on the stored quantity [41]. As a consequence, a greater adipose mass decreases the available vitamin D in blood [41]. Therefore, it must be kept in mind that obesity may be a reason for vitamin D deficiency. Prior studies have also shown that obese individuals are more likely to be vitamin D deficient compared with normal-weight people [41]. This finding was also confirmed by studies assessed the effect of sleeve gastrectomy on serum level of 25(OH)D [49,50,51,52]. In a clinical trial, after 3 month weight loss by sleeve gastrectomy in morbidly obese patients, 25(OH)D concentrations were increased significantly [50]. In another similar study, weight loss along with increment in 25(OH)D levels occurred after sleeve gastrectomy improved bone mineral density in obese patients [51]. Søvik et al. reported that weight loss due to gastric bypass not only increased the 25(OH)D concentrations, it also improved cardiovascular risk factors [52]. Beneficial effects on risk factors related to cardiovascular diseases in mentioned study might be due to increased levels of vitamin D. Therefore, it is still unclear that vitamin D deficiency develops obesity or vice versa. Further studies, particularly of a prospective nature, are needed to shed light facts in this regard.

The prevalence of vitamin D deficiency in individuals participated in the current study was high (60.5%). On reason for this high prevalence might be seasonal variation in serum 25(OH)D. Blood sampling in this study was in winter and in this season, sunlight exposure is low. However, sunshine exposure in Middle East is potentially high and the effects of seasonal variation on serum 25(OH)D might be low [19]. In future studies, seasonal variation in serum 25(OH)D should be considered on the association between vitamin D levels and obesity.

This study has several limitations that should be considered when interpreting our findings. The design of our study was cross-sectional that prohibits inferring a causal link between vitamin D status and obesity. Therefore, prospective studies are needed to confirm our findings. In addition, participants with obesity may have reduced their dietary intakes to lose weight that affect intake of foods rich in vitamin D. Therefore, actual results may be even stronger than those obtained. Despite several adjustments, further control for other residual confounding variables such as dietary intake of energy, fish and mushrooms (as sources of vitamin D) intake, skin type, sun exposure and psychological factors might be needed to reach an independent association between vitamin D status with general and abdominal obesity.

In conclusion, serum 25(OH)D concentrations were inversely associated with general and abdominal obesity either before or after controlling for potential confounders. Furthermore, in fully adjusted model, vitamin D deficiency was positively associated with both kinds of obesity.