Low calcium and vitamin D intakes have been associated with health risks in childhood and adulthood. This study aims to investigate dietary sources of calcium and vitamin D intake, and its associated sociodemographic, economic and lifestyle factors among preschoolers.
Three-day estimated diet records from 696 Flemish preschoolers 2.5–6.5 years old (51% boys) were used (66% of 1052 collected diaries). Contribution of 58 food groups to calcium and vitamin D intake were computed. Multiple linear regression was used to examine associations of intakes with sociodemographic, economic and lifestyle factors.
Mean calcium intake (844 mg per day) was above, and mean vitamin D intake (2.0 μg per day) largely below the Belgian recommendations. Milk, sweetened milk drinks and cheese were the main sources of calcium intakes (26, 25 and 11%, respectively). Butter and margarine were the main vitamin D sources (26%), followed by growth milk (=fortified milk) (20%) and fish (15%). Calcium and vitamin D intake were negatively associated with participants’ age, and calcium positively with parental education and family size. The child's gender, supplement use and physical activity level, and the employment status and smoking behaviour of the parents were not associated with calcium or vitamin D intake.
Flemish preschoolers had too low vitamin D intakes while most had adequate calcium intakes. Milk (including sweetened, fortified/growth milk) was the main food source of calcium intake and the second important source of vitamin D intake after butter and margarine. Calcium intake was positively associated with parental education, while vitamin D intake was not.
Although clinical consequences of adverse bone health are predominantly seen in older age, accumulating evidence indicates that many predisposing factors arise in childhood (Davies et al., 2005). Bone mineral content at older age is determined by the peak bone mass attained in young adulthood and subsequent adult bone loss (Kalkwarf et al., 2003; Davies et al., 2005). Therefore, interventions designed to maximize bone health should start at an early age. While peak bone mass is mainly genetically controlled, calcium and vitamin D intake during childhood and adolescence are considered to have an important role in bone health (Johnston et al., 1992; Matkovic, 1992; Davies et al., 2005; Rizzoli et al., 2010).
Previous findings on calcium and vitamin D intakes of Flemish preschoolers suggest that <70% of the children comply with the recommendations (Hoge Gezondheidsraad, 2003) for calcium intake and <15% with the recommendations for vitamin D intake (Huybrechts and De Henauw, 2007). These borderline calcium and inadequate vitamin D intakes, in comparison with the Belgian Superior Health Council recommendations (Hoge Gezondheidsraad, 2003), are cause of concern for the health of Belgian preschool children, and provide evidence of dietary inadequacies in an understudied subgroup of the population. Therefore, it is important to examine the food sources contributing most to daily calcium and vitamin D intakes of Flemish preschoolers, and sub-populations most vulnerable of inadequate intakes in order to enable targeted interventions.
The aim of this study is to investigate dietary sources of calcium and vitamin D intakes and its associated sociodemographic, economic and lifestyle factors among Flemish preschoolers.
Materials and methods
The study used data from the Flanders preschool dietary survey (data collected from October 2002 until February 2003), in which usual dietary intake was estimated from 3-day estimated dietary records and a 47 item Food Frequency Questionnaire, completed by a proxy (parent/caregiver). The sampling design, methods response rate (50%) and representativity of the study sample were described previously (Huybrechts et al., 2008b). In brief, schools were used as primary sampling units and classes as secondary sampling units. A total of 2095 children from 43 schools were invited to participate. The percentage of under-reporters was low (<2% of the children when using the individual Goldberg cut-offs adopted for children) and has been described in depth elsewhere (Huybrechts and De Henauw, 2007).
Sociodemographic, economic and lifestyle information about the child and its family was collected via a parental questionnaire: employment status (employed or unemployed); educational attainment (lower secondary, secondary or higher education); and smoking status (currently smoking: yes/no) of the parents; family size (less or more than two children); children’s physical activity level (light, medium or high) and supplement use (yes/no) of the child. Level of physical activity was assessed via a short parental questionnaire asking about their subjective perception of the physical activity level of their child (very active (for example, running, swimming, cycling), active (for example, walking, actively playing) or less active (for example, mainly sitting or screen activities), and the number of hours their child spends in organized sport activities (for example, football, ballet, and so on).
The Ethical Committee of the Ghent University Hospital granted ethical approval for the study. Informed written consent was obtained from all parents.
Assessment of dietary calcium and vitamin D intake
For the purposes of the current analysis, only food diaries with three completed record days were included resulting in a final sample of 696 (66% of the 1052 collected) diaries.
Using a systematic procedure, the following food composition tables (listed in order of priority) were used to perform nutrient calculations: the Belgian food composition tables NUBEL (NUBEL, 2004), Dutch food composition database NEVO (NEVO, 2001), food composition tables of the Belgian Institute Paul Lambin (IPL, 2004) and the McCance and Widdowson's UK food composition tables (FSA, 2002). Within the context of this study, systematic procedure refers to the use of the Belgian food composition tables as the basic tables and thereafter when insufficient information was available in this Belgian database, the other databases were used.
In total, 936 foods and composite dishes were reported in the food diaries of the 696 children that were included in the study sample. All recipes described in depth as ingredients in the diaries were encoded as ingredients in the database. In order to enable classification of foods into food groups of the Flemish Food-Based Dietary Guidelines (FBDG) (Vigez, 2004), eight extra composite dishes had to be disaggregated. After the disaggregating procedures, food items were divided into 58 food groups of similar nutrient content based on the classification of the Flemish FBDG and the expert opinion of the investigators (see Table 2).
The contribution of dietary supplements to total calcium and vitamin D intake was not considered in this study. However, in depth analysis reporting the frequency of consumption of dietary supplements among Flemish preschoolers is published elsewhere (Huybrechts et al., 2010).
The Statistical Package for the Social Sciences for Windows version 14 (SPSS Inc., Chicago, IL, USA) was used to perform statistical analyses.
Mean and median usual intakes of the population and the proportion below or above defined cut-offs (Hoge Gezondheidsraad, 2009), were calculated using statistical modelling (NUSSER method, developed at Iowa State University, IA, USA) in order to correct for day-to-day variability in the 3-day estimated dietary records (Nusser et al., 1996; Guenther et al., 1997). The program used to calculate usual intakes was the Software for Intake Distribution Estimation (C-side) (Iowa State University) (Iowa State University, 2006). Recommendations of the Belgian Superior Health Council (revised version 2009) were used to evaluate total calcium and vitamin D intakes (Hoge Gezondheidsraad, 2009).
The population proportion formula was used to determine the percentage contribution of each food group to the intake of calcium and vitamin D (Krebs-Smith et al., 1989), which includes summing the amount of the component provided by the food for all individuals divided by the total intake of that component from all foods for the entire study population (Krebs-Smith et al., 1989; Royo-Bordonada et al., 2003; Fox et al., 2006).
Multiple linear regression analysis was used to investigate the associations of mean calcium and vitamin D intake (dependent variables) with the sociodemographic, economic and lifestyle variables available from the parental questionnaires (independent variables). Associations were simultaneously controlled for all variables included in the models: total energy intake, sex, age, physical activity level, supplement use, household size, occupational status and educational level of the parents and smoking of the parents. Interactions of the independent variables with age and gender were also included. Only significant variables associated with calcium and vitamin D intake were included in the final model. All two-tailed statistical analyses were tested with a significance level set at P<0.05.
Characteristics of the study population
The total study sample of 696 children included 51% boys and 49% girls. In all, 30% of the children were between 2.5 and 3 years old and 70% between 4 and 6.5 years old (Table 1). The proportion of children studied in each province (30% in Antwerp, 24% in East-Flanders, 22% in West-Flanders, 15% in Flemish Brabant and 9% in Limburg), compared well with the proportions derived from the target population, namely preschool children in Flanders (28, 23, 18, 18 and 13% respectively). Mean calcium intake (95% confidence interval) was 844 (821–868) mg per day and mean vitamin D intake was 2.0 (1.8–2.2) μg per day. Mean calcium intake was above and mean vitamin D intake largely below the age-specific recommendations for children.
In total, 86% of the children 2–3 years old met the calcium recommendation of 500 mg per day and 64% of the children 4–6 years old met the recommendation of 700 mg per day. Only 5% of the children met the vitamin D recommendation of 10 μg per day (4% in the children 2–3 years old and 1% in the children 4–6 years old).
Dietary sources of calcium and vitamin D intake
Table 2 lists food and beverage categories and their relative contributions to daily calcium and vitamin D intake in preschool children. Milk, sweetened milk drinks and cheese were the main sources of calcium intakes (26, 25 and 11%, respectively), followed by milk desserts, sweet snacks (for example, child biscuits), cooked vegetables and fruit juice.
Butter and margarine (26%), fortified milk drinks (growth milk) (20%) and fish (15%) were the main sources of vitamin D, followed by meat products, sweet snacks, milk, eggs and hard cheese. Very similar results were obtained, for what concerns the main food sources contributing to total calcium and vitamin D intakes, when stratifying for age or gender.
Associations of calcium and vitamin D intake with sociodemographic and economic factors
Calcium and vitamin D intake were both negatively associated with age of the child, and calcium was positively associated with both maternal and paternal educational level and family size (Table 3). Gender, supplement use and physical activity level of the child, and employment status and smoking behaviour of the parents were not associated with calcium or vitamin D intake.
Mean calcium intake was above and mean vitamin D intake largely below the recommendation for children (95% of the children had vitamin D intakes below the recommendation) (Hoge Gezondheidsraad, 2009). Milk, sweetened milk drinks (for example, chocolate milk) and cheese were the main sources of calcium intakes (26, 25 and 11%, respectively). Butter and margarine were the main sources of vitamin D (26%) probably due to the mandatory fortification of margarine in Belgium, followed by fortified milk drinks (20%) and fish (15%). Meat and poultry also contributed importantly to vitamin D intakes (11% for meat and poultry together). Both nutrients were negatively associated with participants’ age, and calcium was positively associated with parental educational level and family size, but not with the child's gender, supplements use, the occupational status and smoking behaviour of the parents. The lower calcium and vitamin D intakes in the oldest age group are likely due to the reduced milk intakes in the oldest age group compared with the youngest children (Huybrechts et al., 2008a).
It should be taken into consideration that our low estimated vitamin D intakes do not necessarily imply a problem of vitamin D deficiency given that vitamin D is also derived from the action of sunlight on the skin. Unfortunately, sun exposure was not assessed in this study, and also contributions from supplements have not been taken into account. However, studies conducted in similar geographical altitude have reported that the contribution of vitamin D derived from sunlight is insufficient to reach the vitamin D requirement (Tylavsky et al., 2006; Stellinga-Boelen et al., 2007). Previous research showed that the vitamin D intake provided via dietary supplements was about 1.3 μg per day for children <4 years old and 0.9 μg per day for children at least 4 years old (Huybrechts et al., 2010). In that study, it was shown that the group of children taking dietary supplements had still mean vitamin D intakes below 5 μg per day. Therefore, young children in Belgium might risk having an inadequate vitamin D intake during winter months (Davies et al., 1999; Emmett et al., 2002).
Comparison with the literature
Differences in dietary intake assessment methods, study design and food grouping made it difficult to compare our calcium and vitamin D intakes, and food contributions to results derived from other studies. These limitations should be considered when interpreting the comparisons with other studies reported below.
Low vitamin D intakes found in our preschool children were similar to that observed in other European studies (Emmett et al., 2002; Lambert et al., 2004; Serra-Majem et al., 2006). For instance, the results concerning vitamin D intake and compliance to the recommendations were comparable to those of Spanish children 2–5 years old (boys: 1.4 μg per day; girls: 1.2 μg per day) and children from the United Kingdom aged 1–3 years old (1.8 μg per day) (Emmett et al., 2002; Serra-Majem et al., 2006). In contrast, calcium intakes in the Spanish children (boys: 135 mg/1000 kcal; girls: 116 mg/1000 kcal) were much lower than those observed in our Belgian sample of children (Serra-Majem et al., 2006). Similarly, calcium intakes of the United Kingdom (boys: 796; girls: 732 mg per day) were lower than those reported for Belgian children (Emmett et al., 2002; Serra-Majem et al., 2006).
Similarly to our study, milk was the main calcium source in another survey among Spanish children, (26% in Spain compared with 50% in Belgium) (Royo-Bordonada et al., 2003). Fish was the main vitamin D source in Spanish children (43%), while margarine/butter in Flemish preschoolers (9% in Spanish children) (Royo-Bordonada et al., 2003). Comparison with main vitamin D contributors among 4-year-old Swedish children showed that in the Swedish preschoolers, the contribution of margarine, butter and oils (20%) and of fish (11%) to total vitamin D intakes was lower in comparison with our Flemish preschoolers (Garemo et al., 2007).
Both calcium and vitamin D intakes derived from food intake alone was higher for children in the United States (calcium: boys: (<4 years) 999 mg per day, (>4 years) 1058 mg per day; girls: (<4 years) 965 mg per day, (>4 years) 951 mg per day; vitamin D: boys: (<4 years) 7.2 μg per day, (>4 years) 6.4 μg per day; girls: (<4 years) 6.9 μg per day, (>4 years) 5.5 μg per day) than to those of our sample (Bailey et al., 2010). The main calcium food sources in US children 2–5 years old were milk and cheese and the percentage of contribution for those two food groups (59 and 11%, respectively) was very similar to the percentages reported for Belgian children (Table 2) (Subar et al., 1998).
When considering the above comparison with European countries, it appears that the intakes of calcium and vitamin D are lower in European children than in children from the United States. This could be attributed to differences in fortification policies or food composition. In addition, within Europe, differences in fortification policies might be causing differences in vitamin D and calcium intakes and in the main food sources contributing to these intakes (for example, because of margarine fortification, the main vitamin D sources in Belgian children were margarine/butter compared with fish in Spain).
Although no information was found of the influence of parental education on the intake of children's calcium and vitamin D intakes, Galobardes et al. (2001) showed that calcium and vitamin D intakes were positively associated with the educational level of the study subjects. A recent study in Polish children and adolescents (7–16 years old) also showed more frequent fish, fruit and vegetable intakes among children and adolescents of higher socioeconomic status families (Suliga, 2010). Given the gap in data investigating the influence of sociodemographic and economic factors influencing calcium and vitamin D intakes among preschool-aged children, future studies investigating preschoolers dietary intakes should look at possible sociodemographic and economic factors influencing these intakes to evaluate the results obtained in our study.
Strengths and limitations
Although, willingness to participate leads to some selection bias, these data represent a more general population of preschool children in Flanders compared with other food consumption surveys mostly restricted to local areas. Nonetheless, as shown previously (Huybrechts et al., 2008b), the study sample was subject to some selection bias, with lower socioeconomic classes being slightly underrepresented. Although this slight selection bias might have influenced our results concerning the association between calcium and vitamin D intakes and socioeconomic factors, it is not possible to prevent such selection bias in large-scale surveys.
Similarly, to other dietary assessment methodologies, diet records are prone to a degree of misreporting, which possibly had an influence in the classification of compliance and non-compliance with the recommendations. However, the percentage of under-reporters in the final sample for analysis was <2%. In addition, a 3-day diet record does not necessarily reflect individual's usual intake. For this reason, statistical modelling (NUSSER method) that accounts for within-individual variability (Iowa State University, 2006) was used in order to calculate usual calcium and vitamin D intake. Unfortunately, it was impossible to correct for seasonal variations, because the fieldwork was conducted only during autumn and wintertime. No data were found about potential seasonal influences on nutrient intake in this population group in Belgium. However, from the results of the National Food Consumption Survey (2004), it could be concluded that seasonal variations have a small effect on nutrient and food intakes (De Vriese et al., 2006), likely due to the widespread availability of most foods all year round. In addition, it should be noted that food composition data used for calculating nutrient intake might also introduce some bias in dietary surveys reporting nutrient intake. Therefore, the investigators would like to emphasize the growing requirement for good quality food composition data.
Finally, it should also be mentioned that the socioeconomic status and lifestyle variables used in the analyses were obtained via a parental questionnaire that included some basic questions about the family situation and some lifestyle habits of the child. These subjective socioeconomic status and lifestyle measure could also introduce some bias (for example, because of social desirable answers).
Our study findings and published literature indicate unfavourably low vitamin D intakes among childhood populations. Enhancing the daily amount of spreadable margarine/butter on preschool children's bread and increasing fatty fish intake could contribute importantly to higher vitamin D intakes. While spreadable margarine for preschool children's bread was under-consumed in comparison with the FBDG (Huybrechts et al., 2008a), it was still the main source of vitamin D intakes. Although spreadable fat is an item that might be more prone to underreporting in diaries, the results from the Food Frequency Questionnaire also revealed that more than one-third of the children never consume spreadable fat on their bread (Huybrechts et al., 2008a). However, in the battle against obesity one should keep in mind that the total energy intake should not be influenced by the enhancement of these fatty food groups what could necessitate a concomitant decrease in other (energy dense) foods containing invisible fat or sugar (for example, soft drink and candy bars). In the Flemish FBDG, children are recommended to use about 5 g margarine per slice of bread (3–5 slices of bread per day are recommended in preschool-aged children and margarine is recommended above butter because of its more advantage fatty acid contents).
Also, the consumption of fortified (growth) milk in children could be recommended to increase children's vitamin D intake. However, most of these growth milks contain added sugar, which makes them energy dense and less appropriate in the fight against obesity.
If public health policies for the increase in vitamin D intake are to be effective, policy development and implementation needs to target the main sources of dietary vitamin D in various populations (including higher as well as lower educated populations). In addition to the mandatory fortification of margarines, manufacturers could also contribute by reformulating existing products to incorporate more calcium and/or vitamin D.
Flemish preschoolers surveyed between 2002 and 2003, had mean vitamin D intakes largely below the recommendation, whereas mean calcium intake was above the minimum recommended intake level. This situation could be improved by promoting the consumption of food categories with high vitamin D contents such as margarine, fish and fortified dairy products. Both calcium and vitamin D intakes were negatively associated with age, and calcium intake was positively associated with the educational level of the mother and the father and family size. This finding suggests that prevention strategies should especially focus on children from lower educated parents.
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We thank all the parents and teachers who participated into this project and generously volunteered their time and knowledge. The Flanders preschool dietary survey was funded by the Belgian Nutrition Information Center (NICE).
The authors declare no conflict of interest.
Contributors: IH performed and interpreted statistical analyses and drafted the article. YL contributed to the statistical analyses and the interpretation of the results. All other authors helped in the evaluation of the results and the writing of the paper. Moreover, IH and SDH were responsible for the study protocol and the fieldwork. All authors have read and have approved the paper as submitted.
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Huybrechts, I., Lin, Y., De Keyzer, W. et al. Dietary sources and sociodemographic and economic factors affecting vitamin D and calcium intakes in Flemish preschoolers. Eur J Clin Nutr 65, 1039–1047 (2011). https://doi.org/10.1038/ejcn.2011.71
- dietary sources
- vitamin D
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