Introduction
The last decade has witnessed a tremendous interest in vitamin D, based on the awareness of a worldwide high prevalence of vitamin D deficiency. Particularly high-risk groups, such as infants, children, pregnant women and lactating mothers, elderly people, or individuals who cover their bodies for cultural reasons, are affected [
1‐
8]. Vitamin D, long known for being essential in building and maintaining the integrity of the skeleton, has only in the last decade been recognized for its involvement in multiple other functions. Vitamin D modulates, regulates, and stabilizes the immune and defense system [
9‐
11]. It may therefore not be surprising that vitamin D deficiency has been linked to a multitude of negative health outcomes such as cancer, auto-immune diseases, infections, allergies, asthma and even depression [
12‐
15]. These new insights have led public health authorities and nutritional societies to reconsider their recommendations for daily vitamin D intake [
16,
17]. In January 2012, the nutritional societies of Germany, Austria and Switzerland (D–A–CH) increased their vitamin D intake recommendations for all age groups [
18]. In 2013, the European Society for Pediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN) drew attention to the problem of vitamin D deficiency among European children and adolescents, and called for action [
19]. There is an urgent need for strategies to improve the vitamin D status of children and adolescents, which has recently been reconfirmed by a consortium of European pediatricians [
20]. Although many national and international authorities recognize the need for improvement, they seem to fail in translating knowledge into current practice. The D–A–CH nutrition societies only recommend vitamin D supplementation if there is no endogenous production via solar exposure. This means, in practice, that children, adolescents, parents and primary caregivers are left alone in evaluating the effectiveness of their solar exposure and/or their vitamin D status through their 25(OH)D blood levels.
The question as to whether a recommended higher vitamin D intake would reduce the prevalence of vitamin D deficiency in our most vulnerable population group, in children and adolescents, needs to be answered. The main aim of our study was (1) to evaluate the vitamin D status of various age groups from the first years until adulthood and (2) to compare the 25(OH)D status in period 1 (years 2009–2012) with that in period 2 (years 2013–2014), reflecting the vitamin D status of children and adolescents before and after the fourfold increase in D–A–CH recommendations (from 200 to 800 IU per day).
Discussion
In 2012, Germany, Austria, and Switzerland increased their vitamin D intake recommendations twofold for toddlers, and even fourfold for children and adolescents, in comparison to previous recommendations [from 5 µg (200 IU) vitamin D to 20 µg (800 IU) per day] [
18] (D–A–CH 2012). These changes were based on the increasing awareness of the high prevalence of vitamin D deficiency influencing growth and development in children and adolescents [
1,
2,
4,
7,
8,
11,
13,
19,
35‐
39].
The issue of which concentration of 25(OH)D in blood best reflects an appropriate vitamin D status is still a matter of controversy [
5,
17,
22,
24,
40,
41]. The German Society of Pediatrics and Adolescent Medicine (DGKJ) [
23] defined “vitamin D deficiency” at 25(OH)D concentrations in serum below 20 ng/ml. Concentrations < 10 ng/ml were classified by ESPGHAN as “severe vitamin D deficiency” [
19]. For high-risk groups, an adequate vitamin D supply is recommended to guarantee 25(OH)D concentrations of 30 ng/ml and more [
19]. The latter is in agreement with the US Endocrine Society [
42] which defined the “sufficiency status” at serum 25(OH)D concentrations of at least 30 ng/ml based on data showing a minimal PTH release and maximum calcium absorption [
42,
43].
We used a combination of recommendations, i.e., a “deficiency” cut-off 25(OH)D ≤ 20 ng/ml given by the DKGJ [
23] and ESPGHAN [
19] (which mainly follow the IOM [
22]) as well as the opinion of the Endocrine Society [
33] and authors of the HELENA study [
24] with regard to an “optimal” 25(OH)D status (≥ 30 ng/ml) to evaluate whether the increased recommendations for vitamin D in Germany led to an improved vitamin D status in the following years. The results represent the first data on 25(OH)D serum levels of infants, children and adolescents of the KIDS 4.0 study. Blood was collected in a pediatric group practice in Mülheim an der Ruhr between 2009 and 2014. The median serum 25(OH)D level during the study period ranged between 13.0 and 20.8 ng/ml with large individual variations. According to the current statements of ESPGHAN and other societies, this data indicates a vitamin D deficiency status [25(OH)D < 20 ng/ml] of most children and adolescents throughout all seasons. Even during the summer months, median 25(OH)D concentrations were low [20.6 ng/ml in period 1 (2009–2012) and 21.5 ng/ml in period 2 (2013–2014)]. This may be partly motivated by an indoor lifestyle and sun protection measures. Due to decreasing solar exposure, vitamin D serum levels fall during winter and reach their nadir in early spring. Even 25(OH)D levels indicating a severe vitamin D deficiency according to the ESPGHAN criteria [25(OH)D lower than 10 ng/ml] were found in 6–32% of the study participants. This study confirms our previous results from a small pilot study in 2007/2008, with 202 participating children and adolescents from the same urban area [
21].
When classifying our data according to age groups, median 25(OH)D serum levels reached little more than 20 ng/ml only in infants aged 0–2 years in the years 2013–2014. This is most likely the result of the vitamin D supplementation which is recommended during the first 12–18 postnatal months in Germany. The fact that more than 50% of infants between 0 and 2 years in period 1 (2009–2012) did not reach vitamin D sufficiency status (median 14.6 ng/ml) despite regulatory advice for vitamin D prophylaxis (400–500 IU/D) may be explained by the small number of samples and possible selection bias.
Our observations in children and adolescents living in Germany support the conclusion that vitamin D serum levels in these age groups are even lower than in adults, as reported in the KiGGS study [
44,
45] and recently in the DEGS1 study [
46]. In the Nutrition and Lifestyle in European Adolescents (HELENA) study, which included only adolescents aged between 12.5 and 17.5 years from ten countries, about 42% of all participants had 25(OH)D concentrations below 50 nmol/l (or 20 ng/ml); the lowest 25(OH)D concentrations were measured in adolescents from Dortmund (Germany) with a mean level of 49 nmol/L [
25]. In our cross-sectional study, we could show that the median vitamin D serum level in children and adolescents was mostly insufficient which is in agreement with the Helena study. Low 25(OH)D levels, in particular at puberty, have also been found in many European countries [
47‐
51].
Although the health risk associated with an insufficient or deficient vitamin D status has been increasingly recognized, often confusing or misleading recommendations have been given to the public. In a recent publication, the authors recommended: “… efforts should be made to maintain vitamin D status throughout the year by spending time outside regularly (without taking risks of sunburns and skin cancer) and paying attention to a healthy diet rich in vitamin D, especially during winter and spring” [
46]. This is a representative example for many publications, and official statements in various countries which, although recognizing the health risks resulting from vitamin D deficiency, recommend activities which are ineffective in their translation into practice for various reasons: (1) due to lifestyle changes, children and adolescents are no longer involved in enough outdoor activities, as many publications confirm; (2) in Germany, as well as in various other European countries, even if enough time is spent outdoors, it would be impossible to produce sufficient vitamin D in the skin during half of the year (roughly from October to March) as sufficient solar UVB radiation is missing [
2,
52]; (3) it has been known for a long time (and is recalled by the same authorities in their statements) that dietary vitamin D intake provides only 5–10% of the recommendations, meaning that vitamin D dietary intake is negligible and vitamin D status cannot be improved by a healthy diet alone; (4) low storage of vitamin D in the liver and fat tissue are considered reasons for low 25(OH)D levels in winter and spring. If we take into account that body fat may store vitamin D, the question arises as to why obese individuals show a mean 35% and overweight individuals a mean 24% higher vitamin D deficiency status compared to average weight individuals, and why they must be considered as a high risk group for vitamin D deficiency [
53].
Our study has some limitations which may have an influence on the vitamin D status. For example, (1) the vitamin D intake by diet or supplements is unknown; (2) low outdoor activity and frequent screen time (TV or computer) are relevant parameter that could explain low vitamin D supply. Since leisure activities are not considered in this study it cannot be concluded if low vitamin D supply, even in the summer months, can be explained either by the amount of outdoor activities or by the low solar radiation in Germany; (3) the color of the skin (skin type) was not considered but 75% of the subjects were of Caucasian origin; (4) body weight has not been recorded. This should be investigated in more detail in further studies as it is known that not only overweight but also underweight has to be considered as risk factor triggering low vitamin D supply and (5) social status and education of the subjects are not known.
The strength of our study is the collection of samples under everyday conditions in a pediatric group practice. A previous study on vitamin D in Mülheim (Germany) has shown that the data correspond very closely to the KiGGs results [
54]. The current study is an additional and more detailed analysis of samples collected over many years showing the same results. Hence, we are convinced that the results can be generalized.
The data obtained correspond to the median vitamin D serum levels of the KiGGS study (10,015 boys and girls, 267 cities and communities, May 2004–May 2006, median vitamin serum level 16.96 ng/ml) [
35]. The KIGGS study and our study are comparable as both covered the age between birth up to 17 years; as the KIGGS data have been collected from 2003 to 2006, long time before the recommendations have been increased by the DACH societies, we can conclude that all activities to improve the vitamin D status so far have been ineffective.
As the methods for determining vitamin D and metabolites is of particular importance we used the diagnostic RIA assay from DiaSorin which comes close to the mostly recommended gold standard LC-MS/MS (liquid chromatography–tandem mass spectrometry), but which is only available in a few places. In a comparison study, the RIA assay showed a performance comparable to the LC-MS/MS method with a concordance correlation coefficient of 0.97 [
55]. Any differences due to the DiaSorin assay should therefore be negligible for the interpretation of our data set.
Considering the importance of an adequate vitamin D status for children and adolescents, we need to answer the question as to why efforts to improve the vitamin D status in children, adolescents and in the adult population have failed in spite of current guidelines. There is an urgent need to implement clear and practical strategies in order to translate scientific knowledge into practice. Our results show that just changing guidelines is not enough and has no bearing on vitamin D status.
The question as to what may be the best strategy to improve the population-wide deficient vitamin D status must be answered. We strongly recommend that public health authorities and nutrition societies should not only focus on recommending a higher vitamin D intake, but concentrate more on strategies to translate current knowledge and guidelines successfully into practice. It is the responsibility of scientific societies (1) to guarantee that the population can follow their recommendations and (2) to ensure that the health risk is kept at a minimum by finding ways to improve an insufficient vitamin D status. In Germany, as in many other European countries, dietary vitamin D intake is negligible and UVB-induced epidermal production too low or non-existent during about 6 months of the year. Therefore, the question needs to be answered as to whether supplementation or food fortification or a combination of both strategies are options to improve the status. Certainly, this is not an easy task, but increasing recommendations without such strategies seem to be ineffective, as shown by our results. Successful strategies to improve vitamin D status in Northern European children have been discussed [
56]. The data show that, for example, food fortification is feasible to maintain adequate circulating vitamin D levels, especially during winter months.
Despite fortification of milk products and vegetable oils, EVIRA, the Finnish Food Safety Authority, started to recommend that all children, adolescents and adults should be supplemented with 10 µg of vitamin D per day throughout the entire year. It may be possible to also reach the target of vitamin sufficiency [minimum serum 25(OH)D level of 20 ng/ml] via sufficient intake of milk and fortified vegetable oil [
57]. The British National Health Service (NHS) and Public Health England (PHE) also advise that all children over 1 year of age and adults should consider taking a daily supplement containing 10 µg of vitamin D, particularly during fall and winter [
58].
We possess no information about the impact of these new recommendations in Finland and in Great Britain on vitamin D status. Our current data show that the results of the D–A–CH vitamin D guideline update in 2012 has had no effect on the vitamin D status of children and adolescents living in Mülheim an der Ruhr. We may cautiously assume that this holds true for all German children and adolescents. Other nutritional studies have also shown that it is difficult to follow recommendations in changing lifestyles to improve health-related behavior [
59,
60]. Our results suggest, that respective societies should ponder on the reasons why these recommondations fail in improving the health status of their addressees. A lack of simplicity and clarity (being indispensable for the implementation into everyday life) is characteristic for the recommendations currently available, be it from ESPGHAN, DGKJ or D–A–CH. Often, there are mainly three reasons why guidelines are not followed by the general population: first, a lack of sufficient information with respect to significance and meaning of the published guidelines, second, the lack of clarity and simplicity of the guidelines, and third, both resulting in a lack of motivation to follow the guidelines [
61].