1. Introduction
More than 2 billion people suffer from micronutrient deficiencies worldwide, including many school-aged children and adolescents in developing countries [
1]. A recent systematic review reported that China has a high prevalence of micronutrient deficiencies, and that 55.7%, 45.2%, and 84.7% of children have insufficient iron, vitamin D, and selenium, respectively [
2]. For instance, iron deficiency can have a detrimental effect on physical performance in children and adolescents [
3]. Vitamin D deficiency in early life may negatively affect neuronal differentiation, axonal connectivity, dopamine ontogeny, and brain structure and function [
4]. Retinoic acid, the active metabolite of vitamin A, is tied to processes of neural plasticity, and may influence memory [
5,
6]. Micronutrient deficiencies have been linked to damaging physical performance [
3], impaired cognitive functioning [
7], suboptimal learning [
8], and poor academic performance [
9]. These endpoints, in turn, may lead to an increased risk of adulthood obesity [
10,
11], living in poverty [
12], depression [
13], and other psychiatric disorders [
14]. Hence, there is a need to identify and evaluate safe, tolerable, and cost-effective nutritional interventions in school children and adolescents.
Food fortification has been an effective public health strategy to decrease micronutrient deficiencies [
15,
16], but the effect of micronutrient-fortified food on academic performance remains unclear [
17,
18]. A 2012 literature review [
17] identified four studies, none of which showed a positive effect of micronutrient supplementations on school examination grades. On the other hand, a systematic review of randomized controlled trials (RCTs) in 2016 [
18] reported a lack of consistency in school performance among students receiving micronutrient interventions. In the latter review, 8 of 19 trials incorporated assessment of academic performance, and one reported significant improvements in mathematics, while no improvement was observed in other academic subjects. Several factors might influence the effect of fortified food on academic performance, such as motivation and learning strategies, which also play important roles in the process of learning and have significant influences on academic performance [
19]. In a cross-sectional study, milk intake showed significant positive correlations with testing technique and learning strategy in Korean male high school students [
20]. However, there have been few studies investigating the effect of fortified food on both motivated strategies for learning and academic performance.
China has a considerable number of school-aged children and adolescents who would benefit from an integrated nutrition improvement policy approach. In 2011, the General Office of the State Council launched the Nutrition Improvement Program for Rural Compulsory Education Students (NIPRCES), which allots children undergoing compulsory education a daily container of milk and a chicken egg [
21]. Although NIPRCES has been implemented for several years, it has not yet been utilized fully in many urban areas, and has yet to be studied for potential effects on school performance. Given this dearth of knowledge, we hypothesized that milk fortified with micronutrients would go further than regular milk in improving micronutrient status, and would positively influence academic performance, motivation, and use of effective studying strategies.
4. Discussion
We conducted a cluster-randomized, controlled feeding intervention study to determine the effect of micronutrient-fortified milk versus unfortified milk on academic performance among Chinese middle school students aged 12 to 14 years. The micronutrient-fortified milk intervention raised blood vitamin B2 and iron levels, and appeared to increase academic performance, physical performance, learning motivation, and the successful use of study strategies.
Children in our study who consumed micronutrient-fortified milk had significantly higher academic performance than those who consumed unfortified milk, not entirely consistent with findings in previous studies [
9,
17,
28,
29]. A recent literature review found that there was a correlation between micronutrients and the academic performance in school children [
9]. However, another systematic review concluded no positive effect of multiple micronutrient supplementations on school examination grades [
17]. For specific micronutrients, one cross-sectional study showed that iron insufficiency was related to disadvantages in learning, and insufficient serum iron concentration was correlated with significantly lower mathematic scores in female students (r = 0.628) [
27]. Another interventional study suggested that improving iron status through fortified rice can enhance school performance (
p = 0.022) [
29]. In addition, a systematic review concluded that serum vitamin B
12 levels were associated with cognitive function [
30], which may further influence academic performance in school children [
31]. Moreover, Babur demonstrated the negative effect of selenium deficiency on learning and memory in adult rats [
32].
The beneficial effect on academic performance in the present study can be attributed to improved vitamin B
2 and iron status. Students who consumed fortified milk showed less iron deficiency, although iron was not added to the milk. The reason for this finding is unclear, although vitamin B
2 may influence iron status, possibly at the level of iron absorption [
33]. Micronutrient levels have been linked in Indian school children to improved cognitive and physical performance [
34]. Iron may alter the intracellular signaling pathways and electrophysiology of the developing hippocampus, the brain region responsible for recognition, learning, and memory [
35]. In addition, we found that students in the intervention group had significantly higher physical performance than what was observed in controls. This may be attributed to improved iron status and oxygen carrying capacity in hemoglobin [
36].
Another possible mechanism contributing to the improved academic performance might be the mediating role of learning strategies [
37]. The present study found that students in the intervention group were more self-efficacious and had less test anxiety, and were also more likely to use cognitive strategies in the process of learning. Students’ perception of self-efficacy and the evaluation of their own competence were significantly and positively related to academic achievement [
38,
39]. In a study of Finnish upper secondary school students [
40], a statistically significant correlation was found between test anxiety levels and academic performance. Abdollahpour [
41] also revealed that using cognitive strategies were positively correlated particularly with math achievement among male high school freshmen. Similarly, Zahrou [
42] found that the consumption of fortified milk has a favorable effect on cognitive ability. Our data suggest that use of cognitive strategies may mediate the association between nutrient status and academic performance. Taken together with the results of these previous studies, our findings suggest a potentially long-term benefit to school-aged children from a relatively inexpensive intervention.
There are two strengths in the present study. Firstly, we not only examined the effect of fortified milk on students’ nutritional status, but also on their academic performance, motivation, and use of learning strategies. Secondly, the cluster-randomized controlled trial design allows control of both measured and unmeasured confounding factors. Furthermore, the cluster-randomized design minimizes the possibility of contamination between the intervention and control group [
43], because there is less opportunity to exchange the milk product for the participating students.
Several limitations of our study must be considered. Information on dietary factors other than nutritional supplements during the intervention period was not collected. Therefore, we cannot be certain that our results were not influenced by unmeasured dietary factors. Similarly, we did not account for factors such as “self-concept” [
44], physical fitness [
45], and cell phone use [
46], which have been found to affect academic achievement. Lastly, the six-month follow-up period precluded the examination of longer-term effects of micronutrient-fortified milk on academic outcomes.