We found that the overall prevalence of anemia in our study population of adolescents aged 10-14 years in rural western China was 11.7%, with 9.7% and 14.4% in males and females, respectively. Multivariate analysis identified lower maternal education, lower household wealth, female sex, pre-puberty development, lower consumption of flesh foods, eggs and dairy products, and lower meal frequency were risk factors for anemia. In addition, we found that higher stage of puberty development was associated with reduced risk of anemia for male adolescents but not for females.
The prevalence of anemia in our study population (11.7%) would be classified as a mild public health problem according to the WHO , which was also lower than the prevalence of 25.5% from a cross-sectional survey on middle school students conducted in our study area in 2006 . Similar decrements were also observed as compared with the prior prevalence from other western rural areas in China [30, 31]. These findings indicate that the prevalence of adolescent anemia in China has improved to some extent. Besides, the decreasing tendency was also observed among adolescents aged 12-17 in the 2002 and 2012 Chinese National Nutritional and Health Survey, which may be due to the great improvements in socioeconomic status, dietary diversity and/or availability of fortified foods such as soy sauce with NaFeEDTA . Nevertheless, the prevalence of adolescent anemia in our study population was still higher than that in more developed areas of China such as 2.9% among adolescents aged 12-14 in Yiwu, a city in eastern China , which warrants further studies on risk factors and developing intervention strategies for adolescent anemia in western China.
We found positive associations between being female and adolescent anemia which was in line with previous studies conducted in Turkey and Indonesia [9, 33]. This finding could be explained by the occurrence of menarche and associated regular blood loss . Further, one study from India reported that adolescent girls tended to consume fewer protein- and vitamin-rich foods compared with boys .
In addition, our results show that adolescent sex significantly modifies the associations between stages of puberty development and anemia. We found that males with higher stages of puberty development had reduced odds of anemia while there was no association among females, which was similar to the results of one study from Indonesia . Some studies reported that the hemoglobin concentration in adolescent boys could increase along with the puberty development, which was regulated by the testosterone and other androgen effects [35, 36]. However, we could not provide evidence for the causality between puberty development and anemia due to the cross-sectional design. Based on a cohort study in Pakistan, Campisi and colleagues reported that anemia and stunting in childhood can delay the adolescent puberty onset . We hypothesized that among female adolescents, those who had puberty onset may have better nutrition status and lower risk of anemia, on the other hand the onset of puberty among those with better nutritional status was associated with regular blood loss and risk of anemia, which potentially resulted in the null associations between puberty development and anemia among females.
Some studies reported that the risk of having anemia increased with age among adolescents that may be explained by puberty development , however these studies did not adjust for stages of puberty development in the models. We noted significant associations between continuous adolescent ages and anemia even after adjusting for stages of puberty development. The models produced a condition index of 8.16 which indicated that the multicollinearity between age and stages of puberty was not a concern (data not shown) . We noted, in the same study population, that adolescent age was positively associated with prevalence of stunting. Taken together, these findings suggest that data on adolescent health outcomes e.g. anemia, should be reported by sex and age and that when possible development stages of puberty should be factored in the interpretation of the findings.
Although dietary intake is an important contributor to adolescent nutrition, and early adolescence is a critical period in the dietary transition from mid-childhood through adolescence to adulthood [39, 40], related data on anemia are limited. In the adjusted models, we found that higher consumption of egg, flesh foods and dairy products were associated with decreased odds of having anemia. A meta-analysis of randomized controlled trials from China also reported that dietary interventions such as consuming eggs before or after the meal once a day could significantly improve the iron deficiency in children with iron deficiency anemia . Further, another study conducted in a refugee camp of Ethiopia found that adolescent girls who consumed more heme-iron containing food sources were less likely to have anemia . These foods such as eggs, dairy products, and flesh foods, are important source of protein, vitamin B12, bioavailable iron and other micronutrients, all of which are determinants of anemia . In a recent study, it was estimated that less than half of adolescent girls consumed daily dairy products, flesh foods, or eggs (41%, 46%, and 19%, respectively) in LMICs, highlighting the essence of improving dietary intake to prevent anemia and other poor health outcomes among adolescents . Subclinical micronutrient deficiency (including iron and vitamin B12) can occur before the onset of anemia , warranting improved dietary intake as a preventive strategy. WHO recommended weekly iron and folic acid supplementation for menstruating adolescent girls in settings with 20% or higher levels of anemia prevalence , however whether this public health program had similar benefits on other settings or adolescent boys is inconclusive. In agreement with another study in southern Ethiopia , we also found that consuming three or more of meals per day was associated with reduced risk of developing anemia. We assumed that adolescents who ate more times per day would have higher likelihood of consuming iron-rich foods and meeting their nutritional requirements. It is notable that in our study area majority of families had only two times of meal per day and ate the first meal by noon, i.e., skipping the breakfast, which also might lead to poor health status for adolescents who are susceptible to nutrition deficiency. One study from China reported that skipping breakfast was associated with higher risk of stunting, wasting and malnutrition among children aged 6-17 years .
In addition to biomedical influences, we also found that adolescents from higher-income households or whose mothers had higher educations were less likely to be anemic, which is in accord with other studies [6, 11]. Similar results were observed when using the continuous Hb as the outcome. Individuals from higher socioeconomic status consume more iron- and vitamin C-rich food . Tur and colleagues also reported that maternal education was positively associated with the quality of dietary mineral and vitamin intakes among adolescents . In the stratified analysis by sex, although the significant association of maternal education with adolescent anemia was only found in females but not in males, we could not identify similar finding in the literature for explaining this result. We hypothesized that adolescent girls were more likely than boys to follow mothers’ advice on healthy behaviors , which warrants further study. However, these findings suggest that programmes that only emphasized biomedical factors might not sufficient to prevent adolescent anemia, and that integrated interventions addressing biomedical determinants and targeting at high-risk subpopulations are essential to improve adolescent health.
This study has some limitations that should be noted. First, we obtained the sample from follow-up of offspring born by women who participated in an antenatal micronutrient supplementation trial, and this population may not be a truly representative sample of our target population. However, our prior data had shown that the background characteristics between participants followed and those lost to follow-up at adolescence were balanced . Besides, the cluster-randomized trial included all pregnant women in villages, representing the community to some extent. Second, we focused on high protein-, vitamin-, and mineral-based foods, but some studies reported that regular consumptions of fruits and green leafy vegetables were also associated with reduced odds of having anemia in adolescent girls , and this is an area to pursue in further research. Besides, other factors associated with anaemia were not accounted in the present study such as parasite infection, thalassemia, and maternal nutritional status. Finally, owing to the cross-sectional study design used, prospective study with careful control of potential confounders are needed to verify the relationships between identified factors and anemia among adolescents. The presented results provide, however, basic evidence that could help develop intervention strategies and target at high-risk subpopulations in this vulnerable population group, as adolescence is a critical window in life for achieving human potential.