European Journal of Internal Medicine 25 (2014) 197–201

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Original Article

Vitamin D status and seasonal changes in plasma concentrations of 25-hydroxyvitamin D in office workers in Ankara, Turkey Nese Cinar ⁎, Ayla Harmanci, Bulent O. Yildiz, Miyase Bayraktar Department of Endocrinology and Metabolism, Hacettepe University School of Medicine, 06100 Ankara, Turkey

a r t i c l e

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Article history: Received 14 September 2013 Received in revised form 6 November 2013 Accepted 7 November 2013 Available online 21 November 2013 Keywords: 25-Hydroxyvitamin D Parathyroid hormone Office workers Seasonal changes

a b s t r a c t Background: Lack of sun exposure is one of the primary causes of epidemic vitamin D deficiency worldwide. The aim of this study was to investigate vitamin D status and seasonal changes in summer and winter in office workers. Methods: This study was conducted in Ankara located at 39°52 30 N, 32°52 E. The study consisted of 118 premenopausal women and men aged between 21 and 52 years-old. Seasonal changes were evaluated in August and February. Fasting serum was obtained for intact parathyroid hormone (iPTH) and 25-hydroxyvitamin D (25OHD). Additional data were collected by a questionnaire that enquired about age, weight, height, wearing style, dietary calcium intake and sunlight exposure. Serum 25OHD concentration was measured using a precise HPLC assay. Low vitamin D status was defined as a 25OHD concentration less than 30 ng/mL. Results: Mean serum 25OHD concentration in summer was 28.4 ± 10.4 ng/mL and 13.8 ± 6.6 ng/mL in winter (p b 0.001). 35.6% of the subjects were vitamin D insufficient in summer and 12.7% in winter (p b 0.001) while 31.5% were vitamin D deficient in summer and 83.9% in winter (p b 0.001). A significant increase in iPTH levels (33.1 ± 15.9 pg/mL vs 49.6 ± 24.3 pg/mL, p b 0.001) was observed throughout the seasonal change. No significant association was found between 25OHD levels and iPTH, body mass index, age and sun exposure index (p N 0.05 for all) in both seasons. Conclusion: Vitamin D deficiency is very prevalent in office workers even in summer time and this should be accepted as a public health problem. © 2013 European Federation of Internal Medicine. Published by Elsevier B.V. All rights reserved.

1. Introduction There is a new growing interest about vitamin D and its physiological functions nowadays due to the new knowledge about its role in preventing cancer [1], immunomodulation against tuberculosis [2], reversing cardiovasculary events [3] and components of metabolic syndrome [4], reducing the risk of autoimmune diseases [5] and even decreasing all-cause mortality [6]. Its primary role in musculoskeletal system is known for almost two centuries. In many studies, it's shown that low 25-hidroxyvitamin D (25OHD) level is significantly associated with low bone mineral density, increased risk of non-vertebral and hip fracture for both men and women [7]. Human get vitamin D from exposure to sunlight, their diet (milk, shiitake mushrooms, egg yolk or oily fish) or dietary supplements [8]. Solar ultraviolet B radiation (wavelength 290-315 nm) is needed for conversion of 7-dehydrocholesterol to previtamin D3 [9]. 25OHD is the main circulating metabolite of vitamin D and shows the vitamin D status

⁎ Corresponding author at: Department of Endocrinology and Metabolism, Hacettepe University School of Medicine, Hacettepe, 06100, Ankara, Turkey. Tel.: + 90 312 3051707; fax: +90 312 3116768. E-mail address: [email protected] (N. Cinar).

of a person. Although, there is no consensus on optimal levels of 25OHD, its presence is known to be inversely associated with parathyroid hormone levels as reported by several studies. In general, adequate or sufficient vitamin D concentration is accepted as equal or greater than 75 nmol/L (30 ng/mL) at which level parathyroid hormone begins to make plateau [8,10]. Moreover, while concentrations between 20 and 30 ng/mL are considered as vitamin D insufficiency, a 25OHD level less than 20 ng/mL is usually defined as vitamin D deficiency by most experts [8]. According to these figures, it has been estimated that around one billion people worldwide have vitamin D deficiency or insufficiency [10–12]. As an aside, previous studies showed that aging, being female, darker skin pigmentation, not enough sunlight exposure and absence of vitamin D fortification contribute to low levels of 25OHD [13]. The role of indoor working in vitamin D deficiency is another factor mentioned in a number of studies since sunlight exposure is one of the most significant factors for having sufficient vitamin D levels. Indeed, indoor workers were reported to have lower 25OHD levels than outdoor workers [14–16] and serum levels of 25OHD were found to be associated with occupational exposure to sunlight [14]. In a study focusing on office workers in subtropical Australia, Vu et al. reported a rate of 54% and 87% vitamin D insufficiency or deficiency in summer and in winter [17].

0953-6205/$ – see front matter © 2013 European Federation of Internal Medicine. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.ejim.2013.11.004

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In this study, we aimed to investigate vitamin D status of healthy adults working all day in an office and seasonal changes of 25OHD concentrations during summer and winter in Ankara, Turkey. 2. Materials and Methods

(HPLC, Absciex, Foster City, USA). The average intra- and inter-assay coefficients of variation (CV) for 25OHD were ≤4.3% and ≤3.4%, respectively. The concentration of iPTH was determined by use of immunoradiometric assay (Immulite 2000) with a reference range of 9.5–75 pg/mL. The average intra- and inter-assay CV for iPTH were ≤4.3% and ≤3.4%, respectively.

2.1. Subjects 2.4. Statistical analysis A total of 118 premenopausal women and men aged between 21 and 52 years-old, working all day in the office were enrolled in the study. Participants with hepatic, renal or gastrointestinal dysfunction (inflammatory bowel disease and malabsorption), uncontrolled thyroid or parathyroid disease and individuals using calcium or vitamin D supplementation or therapies that interfere with vitamin D metabolism were excluded from the study. The study was approved by the local ethics committees of the Hacettepe University School of Medicine and informed consent was obtained from all subjects. 2.2. Study design The study was designed as a prospective observational study in Ankara. The city is centrally located in Anatolia, at 39°52 30 N, 32°52' E. Ankara has a continental climate, with cold, snowy winters and hot, dry summers. Rainfall occurs mostly during spring and autumn. The average temperature is 28 °C (82 °F) in summer and the temperatures as high as 42 °C (108 °F) were recorded. Furthermore, January is the coldest month with temperatures dropping to an average of -6.6 °C (20.1 °F). In an effort to investigate the effects of coldest and highest temperatures the timespan of the study was selected to cover a period between August (August 1–30, 2008) and February (February 1–28, 2009). In August, at the start of the observations, fasting serum was collected from all subjects for determining intact parathyroid hormone (iPTH) and 25OHD levels. The entire laboratory tests performed in August were repeated at the end of the observation period in February. According to the test results, the participants were classified as vitamin D deficient (if 25OHD b 20 ng/mL), vitamin D insufficient (if 20 ng/mL ≤ 25OHD b 30 ng/mL) and vitamin D sufficient (if 25OHD ≥ 30 ng/mL). In addition, to properly understand other factors that may have a role in vitamin D deficiency, all subjects were enquired about age, weight, height, wearing style, physical activity, dietary calcium intake, current and past smoking habits, alcohol intake and sunlight exposure by a questionnaire. Later, the questionnaire results were used to determine body mass index (BMI) by taking the ratio of weight (kg) over height squared (in m2), physical activity by using subject responses in regard to hours spent on exercise, at work or leisure time and sunlight exposure by calculating the average time spent in the sun per day. Moreover, by referring to the answers to the wearing style questions and the rule of nines [18] which calculates skin sun exposure at front torso, back torso and each leg (18% each), the arms and head (9% each), and the face (5%), a sun exposure index [19] was calculated. This index was employed to estimate the amount and duration of skin sun exposure. Sun exposure index of each subject was then multiplied by the reported average sun exposure per week without sunscreen to calculate per individual sun exposure index. Finally, dietary calcium intake was calculated by using a food-frequency questionnaire (FFQ) that included multiple choices about frequency of intake of calcium containing foods (milk, cheese, kasseri, yogurt) due to the absence of vitamin D fortified foods in Turkey. FFQs were checked by a nutritionist for completeness and accuracy. 2.3. Assays Blood samples were taken through venipuncture and centrifuged within 2 h after withdrawal. Serum was stored at −80 °C. The 25OHD concentrations were measured by high liquid chromatography method

We estimated the prevalence of vitamin D deficiency or insufficiency overall and for each sex group for each season by using chi-squared or Fisher exact test. Mean (±SD) values were used to represent continuous variables such as 25OHD, iPTH, age and dietary calcium intake. While the comparisons between the means of two continuous variables were calculated by using independent samples Student's t-test or Mann–Whitney U test, the comparison of categoric variables was performed by McNemar test. Moreover, for the analysis of the seasonal changes of continuous variables paired sample t-test or Wilcoxon signed-rank test was preferred. On the other hand, the associations between 25OHD, iPTH, dietary calcium intake, sunlight exposure were analysed by using Pearson or Spearman correlation. The statistical analysis also contained a multivariate regression of the vitamin D status by using a number of independent variables including age, sex, BMI and sun exposure index. The entire statistical studies were performed by SPSS Release 15.0 (Statistical Package for Social Sciences for Windows) and P b 0.05 was accepted as the cut-off value for statistical significance. 3. Results The mean age of 118 subjects (65 women and 53 men) that consented to give blood samples is 34.1 ± 7.4 years. Table 1 shows the characteristics of these subjects. A significant decrease in serum 25OHD levels (28.4 ± 10.3 ng/mL in summer vs 13.8 ± 6.6 ng/mL in winter, p b 0.001; Table 2) and a significant increase in iPTH levels (32.9 ± 15.8 pg/mL in summer vs 48.9 ± 24.2 pg/mL in winter, p b 0.001; Table 2) were observed throughout the seasonal change. In general, 39.8% of the subjects had sufficient vitamin D levels in summer whereas this percentage decreased to 3.4% in winter (p b 0.001, Table 2). However, even in summer, 24.6% of subjects had vitamin D deficiency and this share increased to 83.9% in winter (p b 0.001, Table 2). In Tables 3 and 4, we present the comparison of vitamin D status of women and men in summer and winter, respectively. No significant difference was observed in vitamin D status and iPTH levels between the sexes in both seasons (p = NS for all, Tables 3 and 4). The correlations of vitamin D level between age (r: − 0.075, p = NS), BMI (r: −0.60, p = NS), iPTH (r: −0.126, p = NS), and sun exposure index (r: 0.120, p = NS) were all found to be insignificant in summer. Similarly, in winter, the correlations of vitamin D level between BMI (r: 0.015, p = NS) and iPTH (r: − 0.101, p = NS) were

Table 1 Characteristics of the study group. Value Age (years) Women/men BMI (kg/m2) Dietary calcium intake (mg/d) Physical acitivity b2-3 h a week (%) ≥2-3 h a week (%) Smokers (%) Users of alcohol (%) Wearing clothes which restrict exposure to sunlight Sun exposure index (hr/w) Summer Winter

34.1 ± 7.4 65/53 24.3 ± 3.3 648.2 ± 310.1 104 (88.1%) 14 (11.9%) 58 (49.2%) 18 (15.2%) 2 (1.7%) 2.57 ± 2.50 0.29 ± 0.19

N. Cinar et al. / European Journal of Internal Medicine 25 (2014) 197–201 Table 2 25OHD and iPTH levels and vitamin D status in summer and winter.

Serum 25OHD (ng/mL) Serum iPTH (pg/mL) Vitamin D sufficient (n, %) Vitamin D insufficient (n, %) Vitamin D deficient (n, %)

Table 4 Comparison of vitamin D status of women and men in winter.

Summer

Winter

p

28.4 ± 10.4 33.1 ± 15.9 47 (39.8) 42 (35.6) 29 (24.6)

13.8 ± 6.6 49.6 ± 24.3 4 (3.4) 15 (12.7) 99 (83.9)

b0.001 b0.001 b0.001 b0.001 b0.001

also insignificant. Furthermore, sunlight exposure had no significant effect on vitamin D levels in winter (r: 0.102, p = NS), nor change in 25OHD levels throughout the seasonal change was not correlated with change in iPTH levels (r: 0.047, p = NS). To evaluate the effect of obesity on vitamin D levels, the subjects were divided into groups as BMI b 25 kg/m2 (n = 64) and BMI ≥ 25 kg/m2 (n = 54). However, no significant difference was found between nonobese and overweight/obese groups in vitamin D levels both in summer and in winter (27.5 ± 10.1 ng/mL vs 29.1 ± 10.4 ng/mL respectively, p = NS in summer; 13.6 ± 6.8 ng/mL vs 14.1 ± 6.4 ng/mL respectively, p = NS in winter). The multivariate regression analysis showed no significant effect of age, sex, BMI and sun exposure index on vitamin D status (vitamin D sufficiency vs insufficiency) in both seasons (p = NS for all). 4. Discussion Sunlight exposure time is one of the major predictors of vitamin D levels. The results of this study show that even in summer, vitamin D insufficiency (35.6%) and deficiency (24.6%) have a great prevalence among healthy adults working in the office all day in Ankara. While only 39.8% of the subjects have normal vitamin D levels (25OHD N 30 ng/mL) in summer, the prevalence of vitamin D deficiency increases in winter to a great degree that only 3.4% of the subjects have sufficient 25OHD levels. There is no significant association with the degree of sun exposure and vitamin D levels in office workers living in Ankara. Due to differences in dietary intake of vitamin D, different exposure time to sun or use of supplements, the prevalence of vitamin D deficiency shows different patterns across various populations. For instance, in Europe, children and adults were found to be at a high risk [20]; even in sunniest areas, vitamin D deficiency is common due to avoidance from the sun. Furthermore, studies from Saudi Arabia, United Arab Emirates, Australia, Turkey and Lebanon reported that around 30-50% of children and adults have 25OHD less than 20 ng/mL [21,22]. On the other hand, National Health and Nutrition Examination Survey (NHANES), holding across all ages (12-60 years N), found that from 1994 to 2004 the number of subjects with 25OH less than 30 ng/mL nearly doubled in the American population [23] whilst only 20-25% of the NHANES population had a serum 25OHD level of at least 30 ng/mL [24]. This dramatic increase in vitamin D insufficiency is explained with decrease in milk consumption (fortified with vitamin D in USA), increase in sun protection and sun avoidance and upward trend in obesity. In a recently published study evaluating the vitamin D status among adults in the Aegean region of Turkey at the end of winter season, mean serum 25OHD concentration was reported to be 16.9 ± 13.1 ng/mL with 74.9% of the subjects having vitamin D Table 3 Comparison of vitamin D status of women and men in summer.

Serum 25OHD (ng/mL) Serum iPTH (pg/mL) Vitamin D sufficient (n, %) Vitamin D insufficient (n, %) Vitamin D deficient (n, %)

199

Women (n = 65)

Men (n = 53)

P

27.9 ± 11.9 33.9 ± 16.8 24 (36.9) 20 (30.8) 21 (32.3)

28.9 ± 8.1 32.1 ± 14.8 23 (43.4) 22 (41.5) 8 (15.1)

NS NS NS NS NS

Serum 25OHD (ng/mL) Serum iPTH (pg/mL) Vitamin D sufficient (n, %) Vitamin D insufficient (n, %) Vitamin D deficient (n, %)

Women (n = 65)

Men (n = 53)

P

13.4 ± 6.9 50.1 ± 26.3 2 (3.1) 9 (13.8) 54 (83.1)

14.3 ± 6.3 48.9 ± 21.9 2 (3.8) 6 (11.3) 45 (84.9)

NS NS NS NS NS

deficiency, 13.8% having insufficiency and 11.3% having vitamin D sufficiency [25]. Although about one third of the subjects included were above 50 years-old in the study, the results of this study were better than ours and this might result from the choice of specific group in our study. In the literature seasonal variations in 25 OHD levels have generally been reported for healthy young adults [19,26]. Regarding vitamin D status in office workers, Vu et al reported that, 54% of the participants in summer and 87% of the participants in winter had low vitamin D status (25OHD b 30 ng/mL) in a study including 129 office workers in summer and 175 in winter in subtropical Australia [17]. Only, 13% of winter participants had 25OHD levels over 75 nmol/L, which was much lower than the proportions reported in a previous study in the same region (34%) [27]. Despite the high levels of ultraviolet (UV) radiation all year around the city, a wide variation in 25OHD levels during the seasonal change (74 nmol/L in summer vs. 54 nmol/L in winter) was also observed, a compatible figure with our study. Different from our study, half of the participants were over 50 years-old and the participants taking vitamin D supplements were included in the study. In another study including 122 outdoor workers and 104 indoor workers in Israel, outdoor workers had significantly higher 25OHD levels than indoor workers both in summer (29.5 ± 8.9 ng/mL vs 26.3 ± 8.2 ng/mL, p b 0.01) and in winter (25.9 ± 8.5 ng/mL vs 20.4 ± 7.9 ng/mL) [14]. In this study, mean serum 25OHD levels in summer were comparable with our study whereas the decrease in 25OHD levels during the seasonal change was lower than the change in our study, which might be due to latitude difference between Israel and Ankara. In a study focusing on four male indoor daytime workers in Kawasaki City, Japan, Itoh et al. reported 16-56% higher serum 25OHD levels in October than February in association with 15-41% lower iPTH levels in October even after accounting for interday variation [28]. The results of this study were similar to our study. The difference in the vitamin D status in men and women has been evaluated in a number of studies [17,29], while some other studies have failed to show this difference [30,31]. In a study including 327 Turkish residents of Turkey and 566 Turkish immigrants living in Germany, Turkish females had a higher prevalence of 25 OHD deficiency (b 10 ng/mL) than Turkish males (30% vs 8%, respectively) [29]. In this study, sex, BMI, lack of sun exposure, living at a higher latitude and wearing a scarf were found to be the most important predictors for hypovitaminosis. D. Hekimsoy et al. reported higher prevalence rates of vitamin D deficiency in women in the Aegean region of Turkey (78.7% of women vs 66.4% of men, p b 0.05) [25]. In this context, personal factors such as dressing styles and higher body surface area in men may be the source of the sex differences. Moreover, Vu et al. observed that women had a significantly lower mean serum 25OHD levels in summer than men and 60% more likely to have a serum concentration b 30 ng/mL [17]. In our study, we observed that there was no difference in mean serum 25OHD levels and the prevalence of vitamin D deficiency between men and women in both seasons. This might be due to the inclusion of only two veiling women in our study. It's known that photoconversion of 7-dehydrocholesterol to previtamin D is decreased at latitudes above 40° and as latitude rises, summer synthesis of vitamin D is even blunted [32]. Vu et al. found that high 25 OHD values were associated with time spent outdoors in non-peak UV radiation periods, while in winter high levels were associated with

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intake of vitamin D from food or supplements in office workers living in subtropical Australia [17]. On the other hand, the degree of occupational exposure to sunlight was found to be significantly correlated with 25OHD levels in a study including outdoor and indoor workers living in Israel [14]. Opposing these data, we failed to show a significant association with sun exposure index and vitamin D levels in both seasons. This might be due to the small number of subjects included in our study. Second, Ankara's tropospheric ozone might reduce the synthesis of vitamin D in the skin. Lastly, solar radiation is of maximal intensity in summer that shortens the unprotected time in direct sunlight (as short as 15 min/d) for sufficient dermal production of vitamin D. While a significant linear inverse relationship between serum 25OHD and iPTH concentration was reported in many studies [33,34], some failed to show this association [35]. The correlations between iPTH and 25OHD levels show wide individual variability [36]. Genetic differences in the vitamin D receptor polymorphism exist in the amount of vitamin D necessary to maintain optimal physiological function, contributing to the lack of a direct relationship between serum iPTH and 25OHD [37]. In addition, iPTH levels are affected by several other factors such as dietary calcium intake. In our study, we failed to find a significant association between vitamin D level and iPTH in both seasons. On the other hand, despite the lack of correlation between iPTH and 25OHD in our study, in association with the decrease in 25OHD levels, iPTH levels tend to increase during seasonal change. In many studies, a negative correlation between age and 25OHD values was observed [33,38]. Older people are thought be at increased risk due to the reduced capacity of older skin to synthesize vitamin D. However, we could not find such an association, which might be due the narrow range of age of participants (21-52 years-old) in our study. On the other hand, obesity has been found to be associated with lower 25OHD levels. This may be related to the less sunlight exposure due to limited mobility and higher storage of vitamin D in adipose tissue. In a study, the ones with BMI N 40 kg/m2 had 24% lower serum 25OHD levels than those with BMI b 25 kg/m2 [39]. In our study, no significant correlation was observed between vitamin D level and BMI and no significant difference was found between overweight/obese (BMI ≥ 25 kg/m2) and non obese groups (BMI b 25 kg/m2) both in summer and in winter. In our study, mean dietary calcium intake was 648.2 ± 310.1 mg/d. This was low compared to the recommended daily/dietary allowance of Food and Nutrition Board at the Institute of Medicine of the National Academies (1000 mg/d) [40]. This data also suggests that our diet is insufficient in calcium and the quality of the diet has to be improved with enrichment or supplementation of calcium. One of the limitations of our study is the lack of a control group who do outdoor activities as a job, therefore we could not be able to compare the people all day working in an office with the ones doing outdoor activities. Another limitation is the data collection method of sun exposure through self-reporting since incorrectly reported sun exposures are a possibility. Also, we did not obtain data about the sun exposure time on sunny vs. overcast or rainy days. Finally, with regard to calcium intake, participants may not have given accurate information since dietary histories were used instead of direct observations or daily diaries. 5. Conclusions In conclusion, vitamin D deficiency is very prevalent in office workers who spend most of their daylight hours indoors in Turkey and vitamin D supplementation may be indicated to indoor workers. Fortification of foods with vitamin D should seriously be considered as a solution to an important and generally overlooked public health problem. Learning points • Sun exposure is essential for sufficient vitamin D levels. This study presents the vitamin D status in office workers in summer and winter in Ankara.

• The main finding is the high prevalence of vitamin D insufficiency in healthy adults working all day in the office even in summer. • Vitamin D supplementation may be indicated to indoor workers. Conflict of Interest The authors have nothing to disclose. Funding The study was funded by Hacettepe University Scientific Research Projects Coordination Unit. References [1] Holick MF. Calcium plus vitamin D and the risk of colorectal cancer. N Engl J Med 2006;354:2287–8 [author reply 2287-8]. [2] DeLuca HF. Overview of general physiologic features and functions of vitamin D. Am J Clin Nutr 2004;80:1689S–96S. [3] Kendrick J, Targher G, Smits G, Chonchol M. 25-Hydroxyvitamin D deficiency is independently associated with cardiovascular disease in the Third National Health and Nutrition Examination Survey. Atherosclerosis 2009;205:255–60. [4] Looker AC, Pfeiffer CM, Lacher DA, Scgleicher RL, Picciano MF, Yetley EA. 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Vitamin D status and seasonal changes in plasma concentrations of 25-hydroxyvitamin D in office workers in Ankara, Turkey.

Lack of sun exposure is one of the primary causes of epidemic vitamin D deficiency worldwide. The aim of this study was to investigate vitamin D statu...
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