Discussion

In the present study, we demonstrated that low vitamin D status is highly prevalent among healthy Korean adolescents and that adolescents’ vitamin D status is highly related to parental vitamin D status.

The optimal level of 25(OH)D in adults has been suggested to be ≥75 nmol/l, a level associated with maximal suppression of parathyroid hormone and reduced fracture risk⁽ Reference Heaney ^{14 ,} Reference Holick, Binkley and Bischoff-Ferrari ^{15 )}. Vitamin D deficiency in adults is commonly defined as serum 25(OH)D <50 nmol/l, where parathyroid hormone levels begin to reduce in vitamin D-deficient adults who receive vitamin D₂ supplementation⁽ Reference Heaney ^{14 ,} Reference Holick, Binkley and Bischoff-Ferrari ^{15 )}. In children, there is a lack of consensus on the ideal 25(OH)D level to prevent health complications; however, limited data have suggested that serum 25(OH)D ≥50 nmol/l⁽ Reference Pettifor ^{16 )} or ≥75 nmol/l⁽ Reference Wagner and Greer ^{17 )} is needed to decrease serum parathyroid hormone level to a low plateau in children. The 2011 report of the Institute of Medicine concluded that a serum 25(OH)D level of 50 nmol/l meets the needs of 97·5 % of the population and levels ≥75 nmol/l are not consistently associated with increased benefit⁽ Reference Ross, Manson and Abrams ^{18 )}. The 75th and 90th percentile values of serum 25(OH)D were 53·7 and 72·4 nmol/l in our study participants. We defined vitamin D insufficiency as serum 25(OH)D <50 nmol/l rather than <75 nmol/l, which could define the majority (96·2 %) of Korean adolescents as insufficient. The 25(OH)D cut-off value for defining deficiency in children and adolescents varies between studies, with the majority consensus setting the level at 25–30 nmol/l, based on 25(OH)D levels found in children with reduced bone mineral density or rickets⁽ Reference Kumar, Muntner and Kaskel ^{6 ,} Reference Pettifor ^{16 ,} Reference Wagner and Greer ^{17 ,} Reference El-Hajj Fuleihan, Nabulsi and Choucair ^{19 )}. Also, the Institute of Medicine report suggests that persons are at risk of vitamin D deficiency at serum 25(OH)D levels <30 nmol/l^{( 20 )}. We defined vitamin D deficiency as serum 25(OH)D <27·5 nmol/l, which corresponds to the Institute of Medicine recommendations and the 10th percentile value of our participants’ 25(OH)D levels.

We found that the mean serum 25(OH)D level of Korean adolescents (44·2 nmol/l) was lower than the reported values of 63·9 nmol/l among US adolescents⁽ Reference Looker, Dawson-Hughes and Calvo ^{21 )} and 50 nmol/l among New Zealand children⁽ Reference Rockell, Green and Skeaff ^{7 )}. The prevalence of vitamin D deficiency among senior high school students (19·6–25·4 %) in Korea (34–38°N) was higher than the reported 18 % among UK (50–58°N) adolescents⁽ Reference Prentice ^{22 )} and 10–13 % among Canadian (45–48°N) adolescents⁽ Reference Mark, Gray-Donald and Delvin ^{23 )}. It has been well documented that vitamin D deficiency in adolescence is highly prevalent in Indian⁽ Reference Marwaha, Tandon and Reddy ^{8 )} (36 %), Iranian⁽ Reference Neyestani, Hajifaraji and Omidvar ^{24 )} (86 %), Mexican⁽ Reference Kumar, Muntner and Kaskel ^{6 )} (7–20 %) and non-Hispanic black⁽ Reference Kumar, Muntner and Kaskel ^{6 )} (43–59 %) populations, because skin pigmentation of these ethnic groups reduces the skin's production of vitamin D₃. Besides dark-skinned ethnic groups, East Asian populations including Korean, Chinese and Japanese also seem to be predisposed to low vitamin D status. As with Korean adolescents, high prevalence of vitamin D deficiency was reported in Chinese adolescent girls living in Beijing (45 %)⁽ Reference Du, Greenfield and Fraser ^{25 )} and Japanese young women (42 %)⁽ Reference Nakamura, Nashimoto and Matsuyama ^{26 )}. The prevalence of adolescents with serum 25(OH)D ≥75 nmol/l was only 3·8 % in our Korean adolescents, which was about one-eighth that reported (30 %) among US children⁽ Reference Kumar, Muntner and Kaskel ^{6 )}. Several factors can explain low vitamin D status in East Asian adolescents. Inadequate sunlight exposure was prevalent among Chinese adolescents and their skin exposure to UV light mainly determined vitamin D status⁽ Reference Du, Greenfield and Fraser ^{25 )}. The vitamin D and Ca intakes from food sources were often much lower than the RNI for Chinese adolescents, and their low Ca intake was significantly associated with vitamin D deficiency⁽ Reference Du, Greenfield and Fraser ^{25 )}. The situation is similar in Korean adolescents, which will be discussed in detail later.

Consistent with other studies⁽ Reference Rockell, Green and Skeaff ^{7 ,} Reference Prentice ^{22 )}, mean serum 25(OH)D value was the highest in summer and the lowest in spring and winter in the present study. Winter/spring season was the most potent predictor of 25(OH)D deficiency in Korean adolescents.

Our study demonstrated that girls had a higher prevalence of vitamin D deficiency than boys, and this pattern was consistent through all age groups. Some studies have supported a higher prevalence of 25(OH)D deficiency in girls than in boys⁽ Reference Kumar, Muntner and Kaskel ^{6 ,} Reference El-Hajj Fuleihan, Nabulsi and Choucair ^{19 )}, while other studies have not found any gender differences⁽ Reference Marwaha, Tandon and Reddy ^{8 ,} Reference Weng, Shults and Leonard ^{27 )}. We found that girls had less physical activity and lower Ca intake as %RNI compared with boys. Also, the consumption of vitamin D from food sources (such as milk, eggs and oily fish) was lower in girls than in boys (data not shown), which was consistent with US studies⁽ Reference Moore, Murphy and Keast ^{28 )}. We speculate that all of these factors could be possible explanations for a higher prevalence of vitamin D deficiency in girls than in boys.

There seems to be a high probability of familial correlation in vitamin D status. Poor maternal vitamin D status has been implicated in vitamin D deficiency of breast-feeding infants⁽ Reference Pettifor ^{16 ,} Reference Park, Namgung and Kim ^{29 )}, and a few studies with small sample size have shown higher familial history of vitamin D deficiency in rachitic children than in non-rachitic children⁽ Reference Thacher, Fischer and Pettifor ^{30 ,} Reference Bener and Hoffmann ^{31 )}. However, the association between adolescent vitamin D deficiency and parental vitamin D status has not been previously reported in a population study. We found a strong association of parent–adolescent vitamin D status. Also, parental vitamin D deficiency was an independent predictor for adolescent vitamin D deficiency independently from season, age, region and obesity. Possible explanations for the parent–adolescent association could be the cultural and dietary habits shared by family members, or genetic factors involved in vitamin D-endocrine metabolism such as dermal production⁽ Reference Holick, Uskokovic and Henley ^{32 )} or degradation of vitamin D⁽ Reference Awumey, Mitra and Hollis ^{33 )}. Our findings support the suggestion that a strong familial tendency of vitamin D deficiency in Korea warrants vitamin D screening for family members of deficient individuals.

Few studies have shown that older children were more likely to be 25(OH)D deficient⁽ Reference Kumar, Muntner and Kaskel ^{6 ,} Reference Prentice ^{22 )}. The prevalence of vitamin D deficiency in adolescents increased with age, reaching the highest in senior high school students (19·5 % in boys, 25·1 % in girls), and age was one of the most potent predictors of vitamin D deficiency in the present study. The main factor that explains the association between age and vitamin D status seems to be sunlight exposure. The students in higher grades tend to spend much of the daytime indoors for study, and the proportion of physical education in the curriculum is reduced. Moreover, most physical training programmes for high school students are carried out in a gymnasium, which limits UVB exposure. Media promotion announcing the high prevalence of vitamin D deficiency in Korean high school students and long-term public health plans are needed to improve sunlight exposure in Korean adolescents by schools and government.

Physical inactivity, previously reported as an important factor for vitamin D deficiency⁽ Reference Holick, Binkley and Bischoff-Ferrari ^{15 ,} Reference Foo, Zhang and Zhu ^{34 )}, was not an independent factor for vitamin D deficiency in the present study. However, the questionnaire conducted by KNHANES did not query where individuals do physical activity, if it is indoor or outdoor activity; therefore it has some limitation in reflecting sunlight exposure. Also, half of the participants had low physical activity of less than 1 h/week. Therefore it might not have an effect as a predictor for vitamin D deficiency in our study.

Obesity has been cited as a risk factor for vitamin D deficiency because the body fat sequesters the fat-soluble vitamin D, resulting in decreased bioavailability from cutaneous and dietary sources⁽ Reference Wortsman, Matsuoka and Chen ^{35 )}, and obese people may have a more sedentary, indoor lifestyle⁽ Reference Rajakumar, Fernstrom and Holick ^{36 )}. Previous studies in adults⁽ Reference Kamycheva, Joakimsen and Jorde ^{37 ,} Reference Arunabh, Pollack and Yeh ^{38 )} and children⁽ Reference Rockell, Green and Skeaff ^{7 ,} Reference Gordon, DePeter and Feldman ^{39 )} have shown an inverse correlation between BMI and serum 25(OH)D levels. However, we could not find a correlation between obesity status and 25(OH)D concentration. The prevalence of obesity was low, at 4·7 % of participants in our study, which limits the ability to demonstrate the effect of obesity in vitamin D deficiency.

Dietary Ca intake may play a role in vitamin D metabolism. Insufficient intake of Ca can induce mild hyperparathyroidism and consequent elevation of 1,25-dihydroxyvitamin D production, which enhances the catabolism of 25(OH)D and lowers circulating vitamin D⁽ Reference Pettifor ^{16 )}. A study from China found that adolescent girls who had Ca intake below 280 mg/d showed a 50 % higher risk of vitamin D deficiency⁽ Reference Du, Greenfield and Fraser ^{25 )}. We found that the mean value for Ca intake as %RNI was as low as 53·8 % (Table 1) and insufficient Ca intake was a significant factor for vitamin D deficiency in boys (Table 3). As milk is a main source of both Ca and vitamin D, low Ca intake might be a reflection of limited intake of vitamin D in Korean adolescents.

The Dietary Reference Intakes of vitamin D from the Institute of Medicine (2010) and the American Academy of Pediatrics state that the Estimated Average Requirement (EAR) of vitamin D is 10 μg/d for all ages and the Adequate Intake (AI) is 15 μg/d for children and adolescents⁽ Reference Wagner and Greer ^{17 ,} Reference Ross, Manson and Abrams ^{18 )}. However, in the Dietary Reference Intakes of vitamin D for Koreans published in 2010, the AI of vitamin D is 5 μg/d for children and adolescents⁽ Reference Seo, Kim and Cho ^{10 )}. Several experts suggest that, without adequate sunlight exposure, children and adolescents require 25 μg/d to achieve adequate levels⁽ Reference Holick, Binkley and Bischoff-Ferrari ^{15 )}. As we previously reported, only 14·2 % of Korean children and adolescents use multivitamin supplements⁽ Reference Huh and Park ^{40 )} and most of the over-the-counter multivitamin or vitamin D supplements in Korea provide 2–5 μg of vitamin D₂ or D₃ daily⁽ Reference Yang, Seo and Kim ^{41 )}, which is too low to meet the suggested vitamin D intakes. Further research is needed to establish the AI of vitamin D to maintain sufficient vitamin D levels for the Korean population.

There were some limitations in our study. First, the study was cross-sectional and therefore causality cannot be inferred. Second, we did not use validated tools to measure sunlight exposure. Last, dietary vitamin D intake was not analysed in the KNHANES, so we could not assess the effect of vitamin D intake. Nevertheless, to our knowledge, the present study is the first one that has demonstrated the association between parental vitamin D deficiency and the risk of adolescent vitamin D deficiency using the most recent nationwide data.