Introduction

Micronutrient deficiency resulting in disorders such as anemia commonly affects adolescents in developing countries. Around one-quarter of adolescents in developing countries are anemic [1], but prevalence estimates for adolescent anemia in the South-East Asia region range from 27% to 55% [2]. Adolescents’ vulnerability to anemia is commonly attributed to the biological demands for micronutrients (such as iron and folic acid) associated with rapid physical growth, as well as from loss of these micronutrients due to parasitic infestations like malaria and hookworm [3]. At the end of adolescence, male rapidly regain adequate nutrient stores, whereas female remain vulnerable to anemia as a result of menstrual blood loss. They may therefore continue to be anemic or become more anemic because of increased micronutrient requirements from menstruation as well as from pregnancy and lactation [4].

Anemia not only adversely affects adolescents’ physical growth, but it also hinders them achieving their full potential by diminishing educational achievement and labor productivity [2]. Previous research has shown adverse effects of anemia on adolescents’ cognitive function and mental health, as well as lower school attendance, learning, academic achievements and decreased work performance [5–8]. In pregnant girls, anemia increases the risk for birth complications and delivery of low birth-weight infants. Hence, anemia is not only a concern for today’s adolescents, but also for society’s future development [9].

In the context of LMICs including Nepal, there is scarce evidence on micronutrient deficiencies among adolescents and in particular, around anemia in adolescents [10]. The Nepal Demographic and Health Survey (NDHS) is a primary source of national data on anemia, but it explicitly provides information on only mothers and children under-five years old. According to the NDHS 2011, 46% of children aged 6–59 months, and 35% of women aged 15–49 years were anemic [11]. Although there has been a substantial reduction of anemia among women in Nepal between 2001 and 2006, but improvements have stagnated since 2006. Several small-scale studies have attempted to examine the prevalence of anemia in adolescents with alarming results. For example, a survey of 308 adolescents aged 10 to 19 years from the Morang district in Nepal showed an overall prevalence of adolescent anemia of 66% [12]. Hospital-based studies conducted among 10 to 19 year old adolescents showed an overall prevalence of 52% - 56% [13, 14]. However, these small studies were each limited to a local region. We designed the current study to determine the prevalence of adolescent anemia and its correlates within a larger nationally representative sample (n = 3780) of 10 to 19 year olds in Nepal.

Methods

Results

Anemia prevalence

Table 1 shows the status of anemia among adolescents by socio-demographic, behavioral and cluster characteristics. Overall, 31% (95%CI: 28.2, 33.5) of adolescents were anemic at the time of the study. The prevalence was particularly high among 15 to 19 year olds (37%, 95%CI: 33.5, 40.6) and female adolescents (38%, 95%CI: 34.0, 41.8) compared to young (10–14 years) and male adolescents, respectively. Anemia prevalence was also high among Hindus (31%, 95%CI: 28.4, 34.0) and the disadvantaged ethnic groups (34%, 95%CI: 30.7, 37.0) compared to non-Hindus and the elite ethnic groups. Adolescents living in the lowlands (Terai) had the highest prevalence of anemia (38%, 95%CI: 33.8, 41.4) compared to hills (24%, 95%CI: 20.4, 28.4) and the mountains (23%, 95%CI: 16.9, 30.0) regions. Forty-eight percent (95%CI: 36.2, 60.0) of adolescents who walked barefoot were anemic, compared to 30% of adolescents who wore shoes (95%CI: 27.4, 32.5). Anemia was common among those with less diversity in their diets. For example, 34% (95%CI: 30.8, 36.3) of adolescents who consumed food from less than four food groups were anemic compared to 25% of those consuming meals consisting of more than four food groups per day (95%CI: 20.0, 28.8).

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Table 1. Prevalence of anemia among adolescents in Nepal obtained from National Adolescent Nutrition Survey 2014.

https://doi.org/10.1371/journal.pone.0208878.t001

Correlates of anemia

Table 2 depicts correlates of adolescent anemia obtained by using multivariable logistic regression. Multivariable analysis revealed that the likelihood of anemia was higher among older adolescents (aOR 1.75, 95%CI: 1.44, 2.13) and females (aOR 2.02, 95%CI: 1.57, 2.60) when compared to younger adolescents and males, respectively. Regarding ecological region, a significant association was observed for those living in the Terai (aOR 1.80, 95%CI: 1.18, 2.77) compared with those living in the mountains. Adolescents who walked barefoot (aOR 1.78, 95%CI: 1.08, 2.94) were more likely to be anemic than those who wore shoes while outdoors. In contrast, anemia was less likely among those who consumed four or more food groups (aOR 0.71, 95%CI: 0.57, 0.88) compared to those who ate less than four food groups per day. No clear associations were found between adolescent anemia and marital status, religion, family size, presence of household latrine, weight status, or place of residence (urban versus rural).

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Table 2. Multivariable analysis of adolescent anemia.

https://doi.org/10.1371/journal.pone.0208878.t002

Discussion

This is the first national survey to investigate adolescent anemia in Nepal. It reveals that the overall prevalence of anemia among adolescents aged between 10 and 19 years was 31%. This is lower when compared to prevalence rates (between 52 and 66%) reported in previous studies from Nepal [12–14], which were limited to small-scale hospital based surveys. The risk of anemia was greater in females, older adolescents and adolescents from the lowlands and lower in adolescents consuming food from multiple food groups. The findings provide a national estimate of adolescent anemia, which will serve as a benchmark to evaluate current nutrition programs as well as serve to estimate the National Burden of Disease for Nepal. This finding also provides insights into the determinants of anemia in adolescents within the context of countries like Nepal that have lacked reliable primary data at the national level.

In developing countries, major drivers of malnutrition, including nutrition-related anemia, include family poverty as well as one’s social position within a household. Lack of education, early marriage and childbearing during adolescence may adversely affect girls’ nutritional status. Especially in South Asia, gender inequality and the resulting lack of control by women and girls over their lives, can be an important underlying determinant of malnutrition in general and access to iron-rich foods [25]. Rapid physical growth in adolescence, menarche and resulting blood loss may also have reduced girls’ iron levels and consequently lead to anemia, particularly in older adolescent girls. For instance, adolescent girls in the United States who have more than three years of menstrual history have been shown to have three times the risk of anemia compared to adolescents with less than three years of menstruation [26].

Nepali adolescent girls, particularly Hindus, experience severe stigmatization around menstruation, which prevents full participation in household chores. This may further limit their access to food and sanitation [27, 28]. Higher rates of anemia have been found among Hindu adolescents in several North Indian studies [29–32]. We found higher odds of anemia in adolescents of Hindu background, although this was not significant. The association between ethnicity and anemia was also not significant suggesting that religion and ethnicity may not be determining factors. Rather, the availability of dietary iron and access to iron-rich foods may be more limited in certain religious or ethnic groups due to food beliefs and eating habits [33]. Further research to assess the effect of food beliefs and nutritional practices on adolescent anemia appears indicated.

In line with previous studies [34–36], eating patterns are major contributors to anemia. We found a higher prevalence of anemia in adolescents who consumed fewer food varieties. The limited consumption of a variety of food sources may reflect household food insecurity from poverty. This may have contributed to the comparatively higher prevalence of anemia in the lowlands (Terai) where, despite fertile and industrial lands, poverty and income disparities are higher than in the other regions [37]. Further, a lack of sanitation facilities in the Terai [11] leads to fecal transmission of helminths, thus inhibiting the internal absorption of nutrients [38, 39]. In this study it was also found that adolescents who did not wear shoes outside were more likely to be anemic. While not wearing shoes can be viewed as a proxy measure of poverty (and thus reflect lack of access to nutritious food), not wearing shoes outside is also a proxy for poor hygiene and increases the chances of hookworm infection [38].

The findings raise a need for context-specific and integrated nutrition programs that address the underlying structural, socio-cultural, environmental and economic determinants of adolescent anemia. An important emphasis should therefore be on integrating nutrition programs with Water Sanitation and Hygiene (WASH) programs in the lowlands, but also with programs that focus on treating hookworm and other helminths. Another strategy could be to introduce a weekly dose regimen of iron supplementation for adolescent girls in schools in order to increase girls’ iron intake [40]. A recent review by Lassi et al [41] showed that iron supplements could significantly improve hemoglobin concentration in adolescents. Efforts should also be steered towards nutritional programs that promote dietary diversity in order to improve the content and bioavailability of micronutrients in household diets [42, 43].

We had a response rate of 99.5%, which is exceptionally high for studies collecting biochemical samples through invasive procedures such as finger prick. The less invasive (and thus less painful) screening method was used to measure capillary hemoglobin, which might have facilitated participation. Lack of routine screening services for anemia in rural areas of Nepal might also have encouraged participation by adolescents.

Despite the strengths that accompany a nationally representative survey with a high response rate, some limitations exist. Our study does not provide regional or district-level estimates of adolescent anemia. We relied on research participants’ perspectives to obtain information on certain determinants, such as dietary habits and sanitary practices. This may have led to some social desirability bias, misclassification and measurement errors. For instance, although a wealth of studies [31, 35, 44–46] have established the effect of economic factors in anemia, no meaningful differences were found between anemia prevalence and the level of household income in the present study. This finding should be interpreted with caution as social desirability bias around family income may have led to some misspecification of the association between the variables. While our study indicated a number of factors significant to iron deficiency anemia, there may be other contributing factors such as thalassemia trait. For instance, the frequency of α-thalassemia trait is high in certain ethnic groups living in malaria-endemic districts of the Terai [47, 48]. This suggests that more detailed hematological testing is warranted on a smaller sample to explore the association with adolescent anemia.

Conclusion

Overall, anemia is a persisting major public health problem among adolescents in Nepal, particularly in the Terai and among older and female adolescents, where a higher prevalence of anemia was observed. The findings of this study suggest that such high-risk populations should be the focus of context-specific, integrated nutrition intervention programs including nutrition education, mass supplementation with iron and folic acid tablets, treatment of hookworm, and sanitation programs for adolescent girls.

Acknowledgments

The authors would like to acknowledge the Nepal Health Research Council for ethical review, as well as for technical and financial support for this study. The authors would like to thank Prof Ramesh Kant Adhakari, Dr. Guna Raj Lohani, Mr. Bihungum Bista, Mr. Bijay Kumar Jha and Mr. Purushottam Dhakal for their advice and support in this study. Special thanks go to the enumerators as well as the research participants.