Abstract
Vitamin D deficiency in known to be high in obese and overweight adolescents. Few studies in other countries have shown lower parathyroid hormone (PTH) levels in obese adolescents despite high vitamin D deficiency. The aim of the study is to assess vitamin D and PTH levels and their relationship in overweight and obese adolescents in Telangana. This cross-sectional study was carried out in 108 overweight and obese boys and girls aged 12–18 years. A pretested Questionnaire was administered to collect information on demographics, sun exposure, medical and nutritional history. Anthropometry and blood sample was collected for estimating 25 hydroxy vitamin D, and PTH. Body mass index Z scores (WHO growth standards) were used for assessing overweight and obesity in adolescents. 54.6% of the subjects were boys. Mean (SD) levels of vitamin D and PTH were 18.25 (9.26) ng/mL and 45.39 (28.23) ng/L respectively. The prevalence of vitamin D deficiency and insufficiency in the current study was 54.6% and 25.9% respectively. However, PTH levels were high only in 24.2% of subjects (> 65 ng/L). There was an inverse but non-significant correlation between vitamin D and PTH. The association was same after adjusting for age, gender and weight. Our study highlights the high prevalence of vitamin D deficiency among overweight and obese adolescents in Telangana. Despite high vitamin D deficiency, very few had high PTH levels and the vitamin D–PTH axis may be altered in overweight and obese adolescents.
Keywords: Adolescents, Obese, Overweight, Parathyroid hormone, Vitamin D deficiency
Introduction
Hypovitaminosis D is considered to be a worldwide problem in both adults and children [1]. Vitamin D deficiency prevails in epidemic proportions all over the Indian subcontinent, with a prevalence of 70–100% in the general population [2]. With increasing urbanization, prevalence of obesity in adolescents is also increasing across the globe. The worldwide prevalence of overweight and obesity rose by 47.1% in children and adolescents in between 1980 and 2013 [3]. A recent study conducted among 24,000 school children in south India showed that the proportion of overweight children increased from 4.94% of total students in 2003 to 6.57% in 2005 demonstrating the time trend of this rapidly growing epidemic [4].
Excess adiposity is known to be associated with vitamin D deficiency [5] and it is estimated that about 34–92% of obese children have suboptimal vitamin D status [6, 7]. Epidemiological data from western countries suggest that the prevalence of vitamin D deficiency in obese children increases with increasing degree of adiposity, with overweight children at 29%, obese at 34% and severely obese at 49% [6].
Serum 25 hydroxyvitamin D [25(OH)D] and parathyroid hormone (PTH) levels are also known to correlate inversely [8]. The synthesis and secretion of parathyroid hormone (PTH) is higher in those with vitamin D deficiency [9]. Both PTH and 25(OH)D play important roles in calcium homeostasis. In the kidney, PTH triggers the hydroxylation of 25(OH)D to its active form, (1 alpha, 25(OH)D), which enhances the intestinal absorption of calcium [9]. Chronic elevations of serum PTH increase osteoclast activity and the urinary excretion of phosphorous, thus having a negative impact on bone density [9].
While serum 25(OH)D levels are lower in obese individuals, likely due to sequestration of vitamin D in the adipose tissue, it is unclear, if the lower 25(OH)D levels in obese children are associated with a PTH increase in the same manner as it is in normal weight children. The aim of the study is to assess relationship between PTH and Vitamin D in overweight and obese adolescent boys and girls.
Materials and Methods
This study is a cross sectional study carried out in Junior college and high school in Medchal district and in the city of Hyderabad. Subjects include 108 boys and girls aged between 12 and 18 years. Systemic random sampling was adopted for each class of high school/college. Inclusion Criteria included Boys and girls aged between 12 and 18 years, after taking assent from them and also written informed consent from their parents and guardians. Exclusion Criteria included boys and girls who have taken vitamin D supplements in last 3 months. Individual who covered themselves completely were excluded from the study. Before the start of the study, Institutional ethical committee clearance was taken. A pretested questionnaire was administered to collect demographics, physical activity, medical and nutritional history. Anthropometry including Height to the nearest 0.1 cm, weight (to nearest 100 grams, Hip circumference (to the nearest 0.1 cm) and waist circumference (to the nearest 0.1 cm) was measured using standard equipment.
Blood Sample Collection
A 5 ml fasting blood sample was collected for estimation of vitamin D and PTH. 25(OH) Vitamin D was measured using a high-performance liquid chromatography (HPLC) method and detected at 265 nm using an ultraviolet detector (CV: 7). Intact PTH was measured by chemiluminescence assay on Siemans advia centaur autoanalyzer. National committee for laboratory standards (NCCLS) Guidelines was followed for sample collection, handling and processing. The cut off points for Vitamin D deficiency was defined based on levels less than 20 ng/dl and insufficiency was defined as levels less than 30 ng/dl. The cut off points for PTH for High (secondary hyperparathyroidism, > 65 ng/L), normal (10–65 ng/L) and low (< 10 ng/L) were considered.
Data Analysis
The data was entered into CSPro software (version 6.1). R Programming software (Version 3.1) was used for data analysis. Body Mass Index for age (BMIZ) and Height for age (HAZ) were calculated using R macro using WHO growth standards. Overweight was defined as BMIZ more than + 1 SD and Obesity as more than + 2 SD for given age and sex. For continuous variables Mean and SD were calculated along with t test to assess differences between boys and girls. For categorical variables, frequencies and crosstabs were calculated along with Chi square test. For prevalence of vitamin D deficiency, binomial test was done to assess confidence intervals. Pearson correlation test was carried out to assess relationship between vitamin D and PTH and similarly for other biochemical and anthropometric measurements. Linear regression was conducted with Vitamin D as dependent and PTH as independent variable and age, gender and weight as confounding variables. P < 0.05 will be considered statistically significant.
Results
General and Personal Details (Table 1)
Table 1.
Characteristics of the study subjects
| (N = 108) | |
|---|---|
| Age in years (mean (sd)) | 15.38 (1.29) |
| Gender = Male (%) | 59 (54.6) |
| Residence = Urban (%) | 34 (31.5) |
| Religion (%) | |
| Christian | 15 (13.9) |
| Hindu | 85 (78.7) |
| Muslim | 8 (7.4) |
| Caste (%) | 15 (13.9) |
| OBC | 55 (51.4) |
| OC | 14 (13.1) |
| SC | 26 (24.3) |
| ST | 12 (11.2) |
| Number of meals per day (mean (sd)) | 2.80 (0.64) |
| Number of snacks per day (mean (sd)) | 1.08 (0.50) |
| Number of tea or coffee per day (mean (sd)) | 1.41 (0.75) |
| Food type = Vegetarian (%) | 20 (18.5) |
| Fish consumption (%) | |
| Monthly | 11 (10.2) |
| Never | 58 (53.7) |
| Occasionally | 37 (34.3) |
| Weekly | 2 (1.9) |
| Milk consumption in ml per day (mean (sd)) | 74.63 (78.14) |
| Sun exposure duration (mean (sd)) | 37.85 (24.45) |
| How many hours do you sleep sch (mean (sd)) | 7.51 (0.90) |
| Color of the skin (%) | |
| Dark | 16 (14.8) |
| Fair | 10 (9.3) |
| Intermediate | 82 (75.9) |
| Sun screen lotions = Yes (%) | 10 (9.3) |
| Weight (mean (sd)) | 55.11 (11.17) |
| Height (mean (sd)) | 152.10 (9.12) |
| Waist circumference (mean (sd)) | 72.86 (9.50) |
| Hip circumference (mean (sd)) | 87.70 (11.41) |
| HAZ (mean (sd)) | − 1.49 (1.30) |
| BMIZ (mean (sd)) | 1.19 (1.27) |
| WHO stunting (%) | |
| Moderate | 73 (67.6) |
| Normal and Above | 24 (22.2) |
| Severe | 11 (10.2) |
| BMIZ grades | |
| Normal and less | 27 (25.0) |
| Overweight | 59 (54.6) |
| Obesity | 22 (20.4) |
| Vitamin D (mean (sd)) | 18.25 (9.26) |
| Vitamin D status (%) | |
| Deficiency | 59 (54.6) |
| Insufficiency | 28 (25.9) |
| Normal | 21 (19.4) |
| PTH (mean (sd)) | 45.39 (28.23) |
| PTH (%) | |
| High | 23 (24.2) |
| Normal | 63 (66.3) |
| Low | 9 (9.5) |
Among 108 adolescents, 54.6% of them were boys. Mean age of the study subjects was 15.38 years (1.29). 31.5% of the study subjects belong to urban area. Majority of the study subjects belonged to Hindu religion (78.7%), followed by Christians (13.9%) and Muslims (7.4%). Mean consumption of meals per day among study subjects was 2.8 meals per day (Range 1–4 meals per day). Mean consumption of snacks per day was 1 snack per day (Range 0–3 snacks per day). Similarly, the mean consumption of tea or coffee per day was 1.4 times per day (Range 0–2 times per day). The consumption of meals, snacks and tea or coffee was in general lower in girls than boys. About one-fifth of the study subjects were vegetarian (i.e. who did not eat either meat or eggs). 53.7% the study subjects did not consume fish in the past one year and only 2% of them consumed fish weekly. The average consumption of milk was about 74.63 ml per day. Mean (SD) duration of sleep was 7.51 h (0.90). Sleep duration was significantly higher in boys than girls (P < 0.001). The Mean (SD) duration of sun exposure among study subjects was 37.85 min (24.45). The duration of sun exposure was significantly higher in boys than girls (P < 0.001). Only 14.8% had dark color skin, and the rest had either intermediate or fair skin.
Anthropometry and Biochemical Parameters (Table 1)
Mean (SD) weight and height of the study subjects was 55.11 (11.17) kg and 152.10 (9.12) cm respectively. Mean (SD) Waist and hip circumference of the study subjects was 72.86 (9.50) cm and 87.70 (11.41) cm respectively. Mean (SD) Body mass index for Age Z (BMIZ) score was 1.19 (1.27). 54.6% of study subjects were overweight, 20.4% obese while the rest were normal.
Mean (SD) Vitamin D of the study subjects was 18.25 (9.26) ng/dl. The overall Vitamin D deficiency and insufficiency in the study subjects was 54.6% and 25.9% respectively. Mean (SD) PTH of the study subjects was 45.39 (28.23) ng/dl. High PTH was seen in 24.2% of the study subjects.
Relationship Between Vitamin D and PTH in Relation to Anthropometry (Tables 2 and 3)
Table 2.
Characteristics of study subjects with Vitamin D deficiency
| Yes | No | P value | |
|---|---|---|---|
| n | 59 | 49 | |
| Gender = Male (%) | 25 (42.4) | 34 (69.4) | 0.005 |
| Weight (mean (sd)) | 59.43 (10.86) | 49.90 (9.22) | < 0.001 |
| Height (mean (sd)) | 152.43 (8.99) | 151.71 (9.36) | 0.689 |
| Waist circumference (mean (sd)) | 75.70 (10.33) | 69.43 (7.09) | < 0.001 |
| Hip circumference (mean (sd)) | 90.69 (13.04) | 84.10 (7.76) | 0.002 |
| HAZ (mean (sd)) | − 1.44 (1.26) | − 1.55 (1.35) | 0.653 |
| BMIZ (mean (sd)) | 1.72 (0.99) | 0.55 (1.29) | < 0.001 |
| WHO stunting (%) | 0.660 | ||
| Normal and above | 42 (71.2) | 31 (63.3) | |
| Moderate | 12 (20.3) | 12 (24.5) | |
| Severe | 5 (8.5) | 6 (12.2) | |
| BMIZ grades (%) | < 0.001 | ||
| Normal and less | 1 (1.7) | 26 (53.1) | |
| Overweight | 41 (69.5) | 18 (36.7) | |
| Obesity | 17 (28.8) | 5 (10.2) | |
| PTH (mean (sd)) | 38.13 (22.63) | 52.80 (31.52) | 0.011 |
| PTH (%) | 0.035 | ||
| High (> 65 ng/L) | 7 (14.6) | 16 (34.0) | |
| Normal (10–65 ng/L) | 34 (70.8) | 29 (61.7) | |
| Low (< 10 ng/L) | 7 (14.6) | 2 (4.3) |
Table 3.
Characteristics of study subjects in relation to BMIZ grades
| Normal and less | Overweight | Obese | P value | |
|---|---|---|---|---|
| n | 27 | 59 | 22 | |
| Gender = Male (%) | 14 (51.9) | 36 (61.0) | 9 (40.9) | 0.256 |
| Weight (mean (sd)) | 43.84 (5.23) | 56.32 (8.02) | 65.66 (11.84) | < 0.001 |
| Height (mean (sd)) | 152.85 (8.98) | 152.03 (8.78) | 151.39 (10.50) | 0.854 |
| Waist circumference (mean (sd)) | 66.70 (5.28) | 73.66 (8.77) | 78.25 (11.48) | < 0.001 |
| Hip circumference (mean (sd)) | 83.15 (6.93) | 87.31 (10.53) | 94.36 (14.94) | 0.002 |
| HAZ (mean (sd)) | − 1.62 (1.28) | − 1.40 (1.27) | − 1.59 (1.45) | 0.731 |
| BMIZ (mean (sd)) | − 0.55 (0.92) | 1.47 (0.30) | 2.55 (0.95) | < 0.001 |
| WHO stunting (%) | 0.782 | |||
| Normal and above | 18 (66.7) | 38 (64.4) | 17 (77.3) | |
| Moderate | 7 (25.9) | 14 (23.7) | 3 (13.6) | |
| Severe | 2 (7.4) | 7 (11.9) | 2 (9.1) | |
| Vitamin D (mean (sd)) | 28.76 (4.68) | 15.41 (7.20) | 12.97 (8.54) | < 0.001 |
| Vitamin D status (%) | < 0.001 | |||
| Deficiency | 1 (3.7) | 41 (69.5) | 17 (77.3) | |
| Insufficiency | 7 (25.9) | 17 (28.8) | 4 (18.2) | |
| Normal | 19 (70.4) | 1 (1.7) | 1 (4.5) | |
| PTH (mean (sd)) | 66.91 (30.96) | 38.61 (20.11) | 32.26 (26.37) | < 0.001 |
| PTH (%) | < 0.001 | |||
| High (> 65 ng/L) | 14 (51.9) | 5 (10.2) | 4 (21.1) | |
| Normal (10–65 ng/L) | 13 (48.1) | 39 (79.6) | 11 (57.9) | |
| Low (< 10 ng/L) | 0 (0.0) | 5 (10.2) | 4 (21.1) |
Table 2 shows anthropometric and biochemical parameters in relation to Vitamin D deficiency. There were no significant differences in height, and HAZ in relation to Vitamin D deficiency. Mean weight, BMIZ, waist and hip circumference was significantly higher in subjects with Vitamin D deficiency. 69.5% were overweight and 28.8% obese in subjects with vitamin D deficiency compared to 36.7% overweight and 10.2% obese in subjects without Vitamin D deficiency. While PTH mean was significantly higher [52.80(31.52) vs. 38.13(22.63)] ng/dl in subjects without vitamin D deficiency compare to subjects with Vitamin D deficiency (P = 0.011). 34% of the subjects with normal vitamin D levels had high PTH values while 14.6% had higher PTH with Vitamin D deficiency. In relation to BMIZ grades weight, waist and hip circumference and BMIZ mean was significantly higher in obese subjects than normal and overweight (Table 3). The mean Vitamin D was significantly lower in obese subjects 12.97(8.54) ng/dl than overweight [15.41(7.20) ng/dl] and normal weight and less subjects [28.76(4.68)] ng/dl. 77.3% of obese subjects and 69.5% of overweight subjects were Vitamin D Deficient compared to 3.7% in normal weight and less subjects. The mean PTH values 32.26(26.37) ng/dl were significantly lowest in obese subjects compared to the other two groups. 51.9% of normal weight and less subjects had high PTH compared to 10.2% in overweight subjects.
Table 4 shows the relationship as assessed by Pearson correlation test with anthropometric and biochemical parameters. Vitamin D was significantly related to age, weight, height, waist and hip circumference but not HAZ and BMIZ. While there was an inverse relationship between Vitamin D and PTH (r = − 0.073), but the correlation was not statistically significant. This was similar after adjusting for age, gender and weight. Beta coefficient in the linear regression with Vitamin D and PTH did not show any significant association with and without adjustment for confounding variables except gender (Table 5).
Table 4.
Pearson correlation matrix for Anthropometric and biochemical parameters in Overweight and Obese children
| Age in years | Weight | Height | HAZ | BMIZ | Vitamin D | Waist circumference | Hip circumference | PTH | |
|---|---|---|---|---|---|---|---|---|---|
| Age in years | 1 | 0.616* | 0.413* | − 0.024 | 0.168 | − 0.421* | 0.61* | 0.67* | − 0.049 |
| Weight | 0.616* | 1 | 0.738* | 0.51* | 0.357* | − 0.324* | 0.751* | 0.764* | − 0.026 |
| Height | 0.413* | 0.738* | 1 | 0.839* | − 0.003 | − 0.234* | 0.545* | 0.58* | − 0.003 |
| HAZ | − 0.024 | 0.51* | 0.839* | 1 | − 0.127 | − 0.082 | 0.315* | 0.329* | 0.047 |
| BMIZ | 0.168 | 0.357* | − 0.003 | − 0.127 | 1 | − 0.026 | 0.236* | 0.283* | 0.128 |
| Vitamin D | − 0.421* | − 0.324* | − 0.234* | − 0.082 | − 0.026 | 1 | − 0.348* | − 0.38* | − 0.073 |
| Waist circumference | 0.61* | 0.751* | 0.545* | 0.315* | 0.236* | − 0.348* | 1 | 0.824* | 0.064 |
| Hip circumference | 0.67* | 0.764* | 0.58* | 0.329* | 0.283* | − 0.38* | 0.824* | 1 | 0.029 |
| PTH | − 0.049 | − 0.026 | − 0.003 | 0.047 | 0.128 | − 0.073 | 0.064 | 0.029 | 1 |
***P < 0.001; **P < 0.01; *P < 0.05
Table 5.
Linear regression model with Vitamin D as dependent variable and PTH as independent variable and age (Model 2), age and gender (Model 3) and age, gender and weight (Model 4) as confounding variables in overweight and obese children
| Beta coefficient | Lower CL | Upper CL | P value | |
|---|---|---|---|---|
| Model 1 | ||||
| PTH | − 0.03 | − 0.11 | 0.06 | 0.55 |
| Model 2 | ||||
| PTH | − 0.03 | − 0.11 | 0.04 | 0.40 |
| Age | − 2.43 | − 3.69 | − 1.17 | < 0.001 |
| Model 3 | ||||
| PTH | − 0.02 | − 0.09 | 0.05 | 0.56 |
| Age | − 0.83 | − 2.23 | 0.56 | 0.24 |
| Gender | 7.57 | 3.75 | 11.39 | < 0.001 |
| Model 4 | ||||
| PTH | − 0.02 | − 0.09 | 0.05 | 0.57 |
| Age | − 0.90 | − 2.45 | 0.65 | 0.25 |
| Gender | 7.71 | 3.64 | 11.78 | < 0.001 |
| Weight | 0.02 | − 0.18 | 0.22 | 0.83 |
Discussion
The prevalence of vitamin D deficiency and insufficiency in overweight and obese children in the current study was 69.5% and 77.3% respectively. The prevalence was similar to recent study in Amaravati, where they found a high prevalence (95.2%) of hypovitaminosis D in 59 adolescent boys and girls aged 13–15 years conducted during the winter season in the month of January [10]. Puri et al. [11] found that 91% of healthy school girls aged 6–18 years in Delhi had hypovitaminosis D. In other study conducted in north India, they demonstrated clinical evidence of vitamin D deficiency in 10.8% of apparently healthy adolescents [12] which is based on a cut-off point of serum 25(OH)D concentrations of 9 ng/mL (lower limit of manufacturer’s normal range). The mean (SD) levels of Vitamin D was 11.8 (7.2) ng/mL in that study, which is lower than the current study of 18.25 (9.26) ng/ml. In the Amaravati study, the mean (SD) serum concentration of 25(OH) D was 12.25 (3.88) ng/ml. There is lack of studies on vitamin D in overweight and obese adolescents in Indian population for comparison. The higher prevalence of Vitamin D deficiency in over weight and obese children than the earlier reported studies of the western countries [6] was expected.
In a study in 133 obese children at baseline, mean (SD) PTH and Vitamin D was 29 (9) pg/ml and 11 (4) ng/ml respectively similar to that of this study [13]. PTH correlated positively to BMIZ (SDS–BMI) (r = 0.25, 0.008) and negatively to 25-OH Vit D (r = − 0.23, P = 0.004). In our study PTH correlated positively to BMIZ (r = 0.128) and negatively to 25-OH Vitamin D (r = − 0.07) but was not statistically significant probably due to lower effect size (Cohen’s d) and sample size. In an another study in overweight and obese children, the level of serum 25(OH)D below which PTH begins to rise was significantly lower (p < 0.001) in overweight/obese children compared to normal weight children [12.4 (95% CI 9.8–15.0) vs. 17.0 ng/ml (95% CI 11.4–22.6)]. The study also concluded that in overweight and obese children, the PTH axis is activated at much lower 25(OH)D levels than in normal weight children [14]. These findings were a consequence of similar ionized calcium levels in these groups despite lower serum 25(OH)D levels in obese children.
In our study, children with Vitamin D deficiency, had less high PTH levels (14.6 vs. 34%) and normal PTH levels were more common (70.8%) than those without Vitamin D deficiency (61.7%). However we also observed a lower PTH levels in Vitamin D deficiency (14.6 vs. 4.3%) than in those without it. This suggests a U shape relationship between PTH and Vitamin D in overweight and obese children. However, there may also be a possibility of other confounding factors that may have influenced this relationship, as a study in adults has shown that, age, lesser energy intake, kidney function, higher ionized calcium, insulin-like growth factor (IGF1), testosterone and smoking influenced PTH levels significantly [15]. In a study in mature obese and lean rats, fed on diet high in dairy calcium, there were significant differences in changes to markers of bone turnover with vitamin D supplementation between obese and lean rats [16]. The anticipated compensatory increase in PTH in response to vitamin D deficiency and insufficiency was observed only among the non-obese suggesting that the innate PTH response to vitamin D deficiency or insufficiency may be blunted in the obese state [16].
The relationship between the serum levels of 25OHD and maximal suppression of PTH has been assessed in only a few studies in adults. Results from one study, show that serum 25(OH)D needs to be higher than 31 ng/mL to suppress PTH in normal weight adult population [17]. For obese population, the maximal PTH suppression was observed when 25OHD was at 11.1 ng/mL, while the overall population has maximal PTH suppression when 25OHD reaches 21.7 ng/mL [17]. In obese African American women, maximal PTH suppression was seen at 16.8 ng/mL serum 25OHD [18]. Similar results were observed in older adults with an average BMI of 26.7 kg/m2, and the maximal suppression of PTH was seen at 16–20 ng/mL [19]. However, this observation is not consistent and some studies did not demonstrate a threshold at all [20]. The above studies suggest differences in physiological response may play a role in the variation of serum 25OHD concentration that is needed for maximal suppression of PTH, which helps to explain why obese individuals require a higher dose of vitamin D to sufficiently lower their PTH levels [21].
The limitations of the study include the sampling procedure to select schools with in and around the city. A convenience sampling procedure was used in selecting the schools and colleges. However, with in each school a systemic random sampling procedure was followed to select students within each class. The strength of the study includes inclusion both boys and girls of all adolescent age groups. Further Vitamin D was measured using HPLC method rather than RIA method and is considered to be the gold standard for measuring vitamin D deficiency.
Conclusion
Thus our study highlights the high prevalence of vitamin D deficiency among overweight and obese adolescents in Telangana. Despite high vitamin D deficiency, very few had high PTH levels and the vitamin D–PTH axis may be altered in overweight and obese adolescents. In normal adolescents the vitamin D–PTH axis is not altered.
Acknowledgements
We thank management of SHARE INDIA, MediCiti Institute of Medical Sciences for their constant support and encouragement.
References
- 1.van Schoor NM, Lips P. Worldwide vitamin D status. Best Pract Res Clin Endocrinol Metab. 2011;25:671–680. doi: 10.1016/j.beem.2011.06.007. [DOI] [PubMed] [Google Scholar]
- 2.Gupta R, Gupta A. Vitamin D deficiency in India: prevalence, causalities and interventions. Nutrients. 2014;6:729–775. doi: 10.3390/nu6020729. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet Lond Engl. 2014;384:766–781. doi: 10.1016/S0140-6736(14)60460-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Raj M, Sundaram KR, Paul M, Deepa AS, Kumar RK. Obesity in Indian children: time trends and relationship with hypertension. Natl Med J India. 2007;20:288–293. [PubMed] [Google Scholar]
- 5.Drincic AT, Armas LAG, Van Diest EE, Heaney RP. Volumetric dilution, rather than sequestration best explains the low vitamin D status of obesity. Obesity (Silver Spring) 2012;20:1444–1448. doi: 10.1038/oby.2011.404. [DOI] [PubMed] [Google Scholar]
- 6.Turer CB, Lin H, Flores G. Prevalence of vitamin D deficiency among overweight and obese US children. Pediatrics. 2013;131:e152–e161. doi: 10.1542/peds.2012-1711. [DOI] [PubMed] [Google Scholar]
- 7.Olson ML, Maalouf NM, Oden JD, White PC, Hutchison MR. Vitamin D deficiency in obese children and its relationship to glucose homeostasis. J Clin Endocrinol Metab. 2012;97:279–285. doi: 10.1210/jc.2011-1507. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Martins JS, Palhares M de O, Teixeira OCM, Gontijo Ramos M. Vitamin D status and its association with parathyroid hormone concentration in Brazilians. J Nutr Metab [Internet]. 2017 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5318626/. Accessed 11 June 2018 [DOI] [PMC free article] [PubMed]
- 9.Holick MF. The vitamin D epidemic and its health consequences. J Nutr. 2005;135:2739S–2748S. doi: 10.1093/jn/135.11.2739S. [DOI] [PubMed] [Google Scholar]
- 10.Dhore R. Vitamin D status of apparently healthy early adolescents in Amravati City of Maharashtra, India. Int J Collab Res Intern Med. 2013;5:608–612. [Google Scholar]
- 11.Puri S, Marwaha RK, Agarwal N, Tandon N, Agarwal R, Grewal K, et al. Vitamin D status of apparently healthy schoolgirls from two different socioeconomic strata in Delhi: relation to nutrition and lifestyle. Br J Nutr. 2008;99:876–882. doi: 10.1017/S0007114507831758. [DOI] [PubMed] [Google Scholar]
- 12.Marwaha RK, Tandon N, Reddy DRHK, Aggarwal R, Singh R, Sawhney RC, et al. Vitamin D and bone mineral density status of healthy schoolchildren in northern India. Am J Clin Nutr. 2005;82:477–482. doi: 10.1093/ajcn/82.2.477. [DOI] [PubMed] [Google Scholar]
- 13.Reinehr T, de Sousa G, Alexy U, Kersting M, Andler W. Vitamin D status and parathyroid hormone in obese children before and after weight loss. Eur J Endocrinol. 2007;157:225–232. doi: 10.1530/EJE-07-0188. [DOI] [PubMed] [Google Scholar]
- 14.Amini Z, Bryant S, Smith C, Singh R, Kumar S. Is the serum vitamin D-parathyroid hormone relationship influenced by obesity in children? Horm Res Paediatr. 2013;80:252–256. doi: 10.1159/000354645. [DOI] [PubMed] [Google Scholar]
- 15.Gunnarsson O, Indridason OS, Franzson L, Sigurdsson G. Factors associated with elevated or blunted PTH response in vitamin D insufficient adults. J Intern Med. 2009;265:488–495. doi: 10.1111/j.1365-2796.2008.02044.x. [DOI] [PubMed] [Google Scholar]
- 16.Cifuentes M, Morano AB, Chowdhury HA, Shapses SA. Energy restriction reduces fractional calcium absorption in mature obese and lean rats. J Nutr. 2002;132:2660–2666. doi: 10.1093/jn/132.9.2660. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Gallagher JC, Yalamanchili V, Smith LM. The effect of vitamin D supplementation on serum 25(OH)D in thin and obese women. J Steroid Biochem Mol Biol. 2013;136:195–200. doi: 10.1016/j.jsbmb.2012.12.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Aloia JF, Talwar SA, Pollack S, Feuerman M, Yeh JK. Optimal vitamin D status and serum parathyroid hormone concentrations in African American women. Am J Clin Nutr. 2006;84:602–609. doi: 10.1093/ajcn/84.3.602. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Durazo-Arvizu RA, Dawson-Hughes B, Sempos CT, Yetley EA, Looker AC, Cao G, et al. Three-phase model harmonizes estimates of the maximal suppression of parathyroid hormone by 25-hydroxyvitamin D in persons 65 years of age and older. J Nutr. 2010;140:595–599. doi: 10.3945/jn.109.116681. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Sai AJ, Walters RW, Fang X, Gallagher JC. Relationship between vitamin D, parathyroid hormone, and bone health. J Clin Endocrinol Metab. 2011;96:E436–E446. doi: 10.1210/jc.2010-1886. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Lotito A, Teramoto M, Cheung M, Becker K, Sukumar D. Serum parathyroid hormone responses to vitamin d supplementation in overweight/obese adults: a systematic review and meta-analysis of randomized clinical trials. Nutrients. 2017;9(3):241. doi: 10.3390/nu9030241. [DOI] [PMC free article] [PubMed] [Google Scholar]