Micronutrients and Nutrition Status of School-Aged Children in Indonesia

Micronutrient deficiencies (MNDs) in school-aged children are still a major health problem in Indonesia. This study was designed to examine the status of micronutrients and their relationship to the nutritional status of children aged 5–12 years since an up-to-date database on the micronutrient status of children aged 5–12 years is needed. Data from the 2018 Indonesian Basic Health Research (Riskesdas) were used in this study, with 2456 subjects for analysis. Micronutrient analysis was carried out, including iron status (ferritin, C reactive protein (CRP)), levels of zinc, vitamin D, calcium, and vitamin A (retinol) in school-aged children (5–12 years). The ELISA measurement was applied to measure CRP, ferritin, and vitamin D. Zinc levels were analysed with atomic absorbance spectroscopy (AAS). Moreover, high-performance liquid chromatography (HPLC) was applied to calculate vitamin A. In addition, stunting and thinness data were also obtained from the Riskesdas study. The results showed that the prevalence of stunting and thinness in school-aged children was 11.4% and 9.2%, respectively, showing that the stunting prevalence in the city was lower than in the village (4.5% vs. 6.9%, P = 0.000, respectively). In addition, the prevalence of MNDs in Indonesian children was 13.4%, 19.7%, 4.2%, 3%, and 12.7% for ferritin, zinc, calcium, vitamin A, and vitamin D, respectively. The mean serum level of vitamin A and zinc was significantly lower in stunted children compared to normal school children (P = 0.010 and P = 0.014). The serum concentration of vitamin D was significantly lower in overweight children compared to thin and normal children (P = 0.000). Serum values of ferritin, zinc, and vitamin A were significantly higher in overweight children compared to thin and normal children (P = 0.000). A poor correlation was observed between the z-score of height-for-age (HAZ) and the levels of zinc (r = 0.089, P = 0.000), vitamin A (r = 0.105, P = 0.000), and vitamin D (−0.073, P = 0.000). In addition, very weak correlations between z-scores of body mass index-for-age (BAZ) and the serum concentrations of ferritin (0.091, P = 0.000), zinc (r = 0.115, P = 0.000), vitamin A (r = 0.137, P = 0.000), and vitamin D (r = −0.112, P = 0.000) were also seen. In conclusion, school-aged children in Indonesia experienced stunting, thinness, and micronutrient deficiency. Furthermore, stunting and thinness were also related to micronutrient deficiencies.


Introduction
A tiny amount of micronutrients, vitamins, and minerals are consumed, but it is essential to physical and mental growth, specifcally for producing enzymes, hormones, and other biomarkers [1,2].As of yet, micronutrient defciencies (MNDs) are still a signifcant global health problem, and WHO predicts that more than 2 billion people sufer from these defciencies [1].School-aged children are one of the atrisk groups to experience MNDs in developing and transition economies countries [3] since micronutrients supplementation is not supplied over again by the government, such as vitamin A. MNDs cause direct and indirect efects on people and society such as deprived health states, inferior scholastic accomplishment, reduced workability, and potency of achievement [4].In addition, if MNDs happen in childhood, it afects growth and health consequences, including stunting, decreased cognitive and working capacity, repeated infections, growth failure, and increased risk of death [4,5].Despite MNDs, children are susceptible to a lack of macronutrients such as stunting, being underweight, and thinness.Tus, relating micro-and macronutrient defciencies is needed, particularly in Indonesia.
MNDs are reported to be global problems in school-aged children.Te studies observed that lack of iron, iodine, folic acid, vitamin A, and zinc is the most commonly reported causes [2,4,6].Anemia is a condition where blood hemoglobin is less than the standard and iron defciency contributes around 50% [7,8].Anemia in school-aged children still becomes a national health problem, showing that the prevalence was more than 20%, contributing 26.4% [9].In addition, the South East Asian Nutrition Survey (SEANUTS) in 2012 highlighted that the prevalence of iron, vitamin A, and vitamin D defciency in 5-12 years children was 8.8%, 1.43%, and 44.3%, respectively [10].Moreover, zinc also happens to be a health problem in Indonesia, but until now, studies regarding its prevalence have not been done nationally.A study in the Bogor district observed that in group-aged children of 11-15 years, zinc defciency was 38.8% [11].In addition, a study in Semarang City found that its prevalence was 92% in children between 9 and 12 years old [12].Other studies in Indonesia reporting the prevalence of calcium defciency were not found, suggesting that national data must be measured.Furthermore, an update on other MNDs' prevalence is also required since the previous study reported its prevalence in 2012.
Studies outside Indonesia also found similar problems, suggesting that school-aged children risk experiencing MNDs [4,[13][14][15][16].A study in Tanzania found that most rural children had a greater risk of having at least one of the MNDs [13].In the United States of America (USA), nearly one-third of the children and adult population (>9 years) is at risk of at least one vitamin defciency or anemia [17].Moreover, in Ethiopian school-aged children, a study observed that 8 of 10 children had minimally one defciency of micronutrients, and children with two or greater than two MNDs were 40.5% [18].Tus, performing MNDs studies becomes essential to examine how big the problem is for Indonesia.
On the other hand, macronutrient problems, including stunting and thinness, are still a national obstacle.At this time, the Indonesian government had put much efort into decreasing this problem, practicing nutrition-sensitive and specifc interventions [19].Stunting prevalence was observed at 30.8% in 2018 [9].Stunting is a chronic undernutrition status that took place long ago [20].Tus, it is needed to prevent it before it occurs, meaning that the nutrition approach must be performed when children are in a thinness situation.Literature noted that protein and diversity of micronutrient consumption such as iron, zinc, calcium, vitamin A, and vitamin D contributed to optimal linear growth [21,22].Moreover, a study stated that the primary source of micronutrients is obtained from animal sources [23].However, the food consumption survey results in Indonesia showed that 56% of Indonesian people's food consumption was obtained from cereals.Animal-based products such as meat and poultry, egg, and fsh were 2%, 2%, and 5.8%, respectively [24].A study based on an evaluation of individual food consumption reported that the diets of children (4-10 years) and adolescents (11-18 years) in Indonesia were lower than the required value, showing defcient intakes of iron (26 and 38%, respectively), zinc (60 and 64%, respectively), and vitamin A (57 and 16%, respectively) [25].School-aged children in Nigeria also experience inadequate intake of micronutrients such as vitamins A, C, B, and Ca [26].
It is imminent, therefore, to assess micronutrient and micronutrient status in the school-age group, considering that data on micronutrient status in this age group are minimal on a national scale.[27].Height was measured using a multifunctional height meter with an accuracy of 0.1 cm, and weight was measured using an electronic AND weighing scale (AND, Japan) with an accuracy of 50 grams [28].Height for age Z-scores (HAZ score) and BMI for age Z-scores (BAZ score) were calculated using the WHO Anthro Plus software.Stunting was defned as having a HAZ score of <−2 SD, whereas normal was organized if the HAZ was between −2 and +1 SD.Tinness, normal weight, and overweight status were classifed as having a BAZ score of <−2 SD, −2-+1 SD, and >+1 SD, respectively [29].

Specimen of Serum Collection.
Te serum samples, archived biological material of the Riskesdas study, were stored in an ultra-low-temperature freezer at 80 °C.First, a procedure from the laboratory information management system (LIMS) and Biorepository of Basic Technology Center for Biomedical and Health National Institute of Health and Research and Development was followed to obtain the serum samples.Second, the serums were checked for their number and grouped according to age and serum conditions, whether they were lipemic or not.Last, 2456 serums were used and examined to measure the micronutrient value.

Determination and Classifcation of Micronutrients
Content in Serum.Serum samples from LIMS were prepared at room temperature before analysis, and each sample was checked for its identifcation number, sex, age group, and condition (whether excellent or lipemic).High-performance liquid chromatography (HPLC) was used to analyse vitamin A. Next, zinc serum was measured using atomic absorbance spectroscopy (AAS).Enzyme-linked immunosorbent assay (ELISA) was then performed to measure vitamin D, Creactive protein (CRP), and ferritin.Last, an autoanalyzer was used to calculate calcium value.
Te ferritin value was adjusted for infammation if the CRP value was higher than 5, applying a multiplier factor of 0.65 [30].Te ferritin defciency was categorized if the ferritin value was less than 15 ng/L [8].Zinc defciency, second, was classifed when the value of zinc serum was less than 0.7 mg/L [31].Tird, a smaller amount of vitamin A (retinol), further down at 20 µg/dL, is considered a vitamin A defciency [32].Fourth, putting together the inadequate serum vitamin D level, a concentration of vitamin D (25hydroxyvitamin D) lower than 30 ng/mL was labeled as vitamin D defciency [33].Finally, calcium defciency was categorized when calcium was less than 8.8 mg/dL [34].

Statistical Analysis. SPSS version 18
was used to analyse the data.First, a one-sample Kolmogorov-Smirnov test was applied to evaluate the data's normality.A descriptive analysis was executed to explain the mean and frequency of each parameter.In addition, a T-test was used to observe the diference in micronutrient value in HAZ and BAZ for gender and subjects' residency, as well as the nutrition status of either stunting or normal children.Te prevalence of stunting, thinness, and micronutrient status was compared in diferent subcategories using chi-square analysis.In addition, the ANOVA test was also used to analyse the difference in micronutrient value in thin, normal, and overweight children.Last, to assess the correlation between two continuous variables, Pearson's test was performed, correlating the z scores of HAZ and BAZ with serum values of ferritin, zinc, vitamin A, vitamin D, and calcium.P values less than 0.05 were assigned as statistically signifcant results.

Results and Discussion
Tis study used 2456 samples from archived biological material of children aged 5-12 years who were collected in the 2018 Riskesdas study.Table 1 shows that the majority of respondents lived in urban areas (56.3%), were male (52.7%), and were aged between 5 and 9 years (67.8%).
Table 4 shows the concentrations of serum ferritin, zinc and calcium, vitamin A, and vitamin D based on nutritional status (HAZ and BAZ).Te mean serum values of zinc and vitamin A were considerably inferior in stunted rather than normal children (0.82 ± 0.17 and 0.85 ± 0.19 mg/L, P � 0.014 and 1.08 ± 0.24 and 1.13 ± 0.25 µmol/L, P � 0.010, respectively).However, serum concentrations of ferritin, calcium, and vitamin D were no diferent between stunted and normal nutritional status.A higher value of ferritin was observed in overweight (52.63 ± 37.13 ng/mL) than in thinness (42.33 ± 40.83 ng/mL) and normal (43.29 ± 33.03 ng/mL) (P � 0.000).Serum zinc, furthermore, was signifcantly higher in overweight (0.90 ± 0.19 mg/L) compared to thinness (0.82 ± 0.20 mg/L) and normal (0.83 ± 0.18 mg/L) (P � 0.000).Tis study also found that the concentration of vitamin A was signifcantly higher in overweight children compared to thin and normal children ( MNDs prevalence was depicted in Table 5.In this study, 13.4% of respondents had ferritin defciency; dividing by gender showed that the prevalence for boys and girls was 7.2%    Pearson's correlation analysis resulted in signifcant outputs between z-scores of HAZ and the levels of zinc (r � 0.089, P � 0.000), vitamin A (r � 0.105, P � 0.000), and vitamin D (r � −0.073, P � 0.000) (Table 6).A very weak positive correlation was observed between BAZ and the values of ferritin (0.091, P � 0.000), zinc (r � 0.115, P � 0.000), and vitamin A (r � 0.137, P � 0.000) (Table 6).In addition, vitamin D (r � −0.112, P � 0.000) was negatively correlated with BAZ, showing a poor magnitude (Table 6).

Discussion
Tis study revealed an overview of the present data on the nutritional status of Indonesian children aged 5-12 years.Te available data showed that stunting and thinness prevalence (11.4% and 9.2%, respectively) are persistent problems in Indonesian school-aged children [35].Tis result is similar to the stunting prevalence of children aged 6-12 years in Ethiopia (11.6%) and much lower than in Africa (22%), South-East Asia (29%), Latin America (16%), the Eastern Mediterranean (24%), and the Western Pacifc (28%) [3,36].Regarding thinness, this study showed a higher prevalence than in Latin America (6%) and much lower than in Ethiopia (10.8%),Africa (36%), South-East Asia (34%), Eastern Mediterranean (13%), and Western Pacifc (14%) [3,36].Tis achievement in stunting and thinness prevalence might be explained by the National Movement for Stunting Prevention and Multi-Sector Partnership Cooperation in Indonesia, which includes specifc and sensitive, nutrition interventions for children in their frst 1,000 days of life in various development activities beyond the health sector targeting the general population [19].In addition, the Indonesian government's commitment and ambition to address stunting have also contributed to this achievement [37].However, the prevalence of both stunting and thinness in Indonesian children aged 5-12 years was still in the medium category [35].Nutrition interventions aimed at improving nutritional status, such as promoting dietary diversity and balanced diets and community-based and school-based approaches to micronutrient supplementation (especially iron), have shown diverse results and are not yet fully efective due to Indonesia's vast territory.Similar eforts to improve nutrition in school-aged children have also been undertaken in Ethiopia [36], resulting in a similar prevalence of stunting in Indonesia and Ethiopia of 11.4% and 11.6%, respectively.Tis study also could not detect the mean diference between HAZ and BAZ between boys and girls.However, a study in low-and middle-income countries (LMICs) conducted on children and adolescents suggested that low nutritional status (stunting and thinness) was higher in boys compared to girls [38].
Te mean diference between HAZ and BAZ scores among schoolchildren was signifcantly superior in the city rather than in rural.A study in LMICs confrmed this fnding that living in urban areas, having higher socioeconomic status, safer food security, and healthier eating habits such as breakfast tradition and healthy snacks consumption reduced the chance of stunting and thinness in school-aged children and adolescents [38].Undernutrition among this age group is often neglected even though a study in rural Indian boys aged ≥5 years showed that prepubertal height defcits among stunted children were carried into adult height, increasing the risk of potentially irreversible loss of growth and cognitive functions [39].Terefore, this problem should be addressed earlier, and intervention must provide sufcient time to evaluate the growth of this age group.Screening for low HAZ and BAZ scores in children through school or pediatric primary health care should be considered a national program priority.
In addition to nutritional status, this current study also showed the prevalence of MNDs on a national scale.Te results observed that in school-aged children, the prevalence of ferritin, zinc, calcium, vitamin A, and vitamin D was  13.4%, 19.7%, 4.2%, 3%, and 12.7%, respectively.Te national prevalence of zinc and calcium defciency in schoolaged children was reported for the frst time in this study.In addition, this fnding also updated the prevalence data from 2012 for iron, vitamin A, and vitamin D defciency in 5 to 12year-old children, which was 8.8%, 1.43%, and 44.3%, respectively [10].Tis study showed that the highest micronutrient defciency proportion was found in ferritin and zinc.A study on Ethiopian children aged 10-14 confrmed this study [16].A national food consumption survey of Indonesian school-aged children (5-12 years) might explain this result, reporting less than half of children consumed iron-and zinc-source foods, for example, meat (24.6%), fsh (25.1%), eggs (43.6%), and soybeans (35.9%) [24].In addition, this study found that micronutrient defciency was more prevalent in girls than boys.A study on the US population supported this fnding that points to the risk of vitamin defciency or anemia being more frequent in girls than in boys [17].Ferritin serum levels were lower in thin and normal school-aged children than in those who were overweight (P � 0.000).A study among Saudi children and adolescents confrmed that thin children were likelier to have lower serum ferritin than normal BMI children [40].Iron defciency indicated by low serum ferritin impairs education achievement, productivity, and ability, and chronic anemia damages growth and the function of the cardiovascular system [41,42].
Zinc serum level was lower in thin and stunted schoolaged children compared with their counterparts in this study.Tis result is in accordance with the study of Indian children and adolescents, which concluded a higher number of low serum zinc levels in underweight and stunted children [43].Evidence has shown that zinc signifcantly afects children's linear growth and weight gain [44][45][46].However, a meta-analysis of randomized controlled trial studies in children aged 1-8 years found that zinc supplementation did not signifcantly afect weight gain or the scores of weightfor-age, length/height-for-age, and weight-for-height [47].
Tis study found that stunted and thin school-aged children had lower vitamin A serum levels than the standard group.Vitamin A's role in controlling average growth and development through its direct efect on growth hormone and its carrier protein may explain this result [48,49].Moreover, a study in Uganda of under-fve children supported this study's results that concluded vitamin A defciency was independently connected to higher odds of stunting growth (adjusted odds ratio, 1.43 (95% CI: 1.08-1.89),P � 0.01) [49].
Vitamin D has signifcant contributions to a child's growth.Evidence from child and adolescent studies showed that declining linear growth was related to vitamin D defciency [50][51][52].Vitamin D contributes to bone mineralization, increases the sensitivity of the growth plate cells to growth hormone, and promotes the growth plate cells to appropriately diferentiate and mature [50,53].Tis study found that overweight school-aged children sufered lower vitamin D serum values than thin and normal children (P � 0.000).Te reviewed study stated that overweight and obese people tend to have vitamin D defciency, ranging from 5% to 90% [54,55].A potential explanation of this phenomenon is that overweight and obese people experience infammation of adipocyte tissues [54] and vitamin D dilution due to a higher distributed volume of serum [55].In addition to calcemic functions, it is also found that vitamin D plays a prominent role in energy metabolism, in particular glucose and fat metabolism in adipocyte cells that afects insulin sensitivity [54].Tus, overweight and obese children with vitamin D defciency are needed to increase vitamin D consumption before adulthood, helping to reduce the risk of metabolic syndromes such as type 2 diabetes mellitus, dyslipidemia, hypertension, and others.
Further analysis showed that zinc and vitamin A exhibited a very weak positive correlation with the HAZ and BAZ scores.On the other hand, vitamin D negatively correlated with both HAZ and BAZ in a very weak capacity.In addition, ferritin was only poorly correlated with BAZ.All of this evidence reported that undernutrition in school-aged children was related to low serum levels of several vitamins and minerals.Reports elucidating the correlation between HAZ, BAZ, and micronutrient value were limited.A study in Cameroon children found that HAZ was signifcantly correlated to zinc, calcium, and iron with a poor magnitude, providing coefcient values of 0.093, 0.029, and 0.111, respectively [56].In addition, in preschool children of Sri Lanka, it was reported that vitamin D was negatively correlated with WAZ (weight for age) and WHZ (weight for height) [57].Tese consistent fndings may be due to similar energy intake among this group.Indonesian children consumed energy of 1.636 kcal whereas Cameroon and Sri Lanka children consumed energies of 1.640 kcal and 1.708 kcal, respectively [58,59].Tus, to tackle the MNDs, it is important to provide nutritious foods to children.One of the best approaches is through the education system, where schooling may serve as an efective entry point for implementing nutrition intervention programs that can efciently reach children.Tese programs could include nutritious meals at school with a particular focus on food sources rich in iron and zinc, as well as vitamin and micronutrient supplementation, deworming prophylaxis, and nutrition education emphasizing balanced nutrition.Tese programs also should be monitored and regularly evaluated.In addition, it is essential to encourage children to have breakfast before starting their day and provide sufcient time to eat lunch at school.Having ≥20 minutes of lunch is related to considerable consumption of grains, meats, milk, and vegetables [60].All of the approaches might be efective in boosting the intake of micronutrients and addressing defciencies.
Te strength of this study was the nationally representative data from the Indonesian Ministry of Health survey with a large sample size.Moreover, data from biochemical analyses of ferritin, zinc, calcium, vitamin A, and vitamin D provide good indicators of MNDs among school-aged children.However, the use of cross-sectional data was a limitation of this study which does not allow for causal inferences.

Conclusions
Te current study observed that the prevalence of MNDs for ferritin, zinc, calcium, vitamin A, and vitamin D in Indonesian school-aged children was 13.4%, 19.7%, 4.2%, 3%, and 12.7%, respectively.In addition, stunting and thinness prevalence were 11.4% and 9.2%, respectively.Moreover, chronic nutritional status was correlated with zinc and vitamin A. Furthermore, acute nutritional status (BAZ) was correlated with a lack of micronutrients, specifcally ferritin, zinc, and vitamin A. Tese fndings indicate that micronutrient defciencies in school-aged children must be addressed immediately by evaluating and planning health programs to address these problems, such as supplementation and fortifcation of micronutrients, deworming, vector control, nutrition and health education, sanitation improvement, clean water supply, and other appropriate approaches.

Table 2 :
Te mean score of HAZ and BAZ and nutritional status prevalence of Indonesian children aged 5-12 years regarding gender.

Table 3 :
Te mean score of HAZ and BAZ and nutritional status prevalence based on the residency of children 5-12 years in Indonesia.

Table 4 :
Level of micronutrients (mean ± SD) according to nutritional status in children aged 5-12 years.

Table 6 :
Correlation between micronutrient value and nutritional status (HAZ and BAZ) of 5-to 12 -year-old children.