A Review of the Risk Factors for Iron Deficiency Anaemia among Adolescents in Developing Countries

Introduction Identifying the root causes of iron deficiency anaemia is a prerequisite for effective management and prevention in adolescents. This systematic review assessed risk factors of iron deficiency anaemia among adolescents living in developing countries. Method Electronic databases such as PubMed, Cochrane Library, Science Direct, Google Scholar, and SCOPUS were comprehensively searched for studies published between 1990 and 2020 that involved risk factors of iron deficiency anaemia among adolescents living in developing countries. The quality of the included studies was assessed using the American Dietetic Association Quality Criteria Checklist. Results A total of 2,252 publications were reviewed, and only fifteen cross-sectional studies were eligible for inclusion, eight of which focused on female adolescents and seven on both genders. Direct risk factors contributing to anaemia among adolescents included food intake practices (n = 10 studies), female adolescents (n = 8 studies), menstruation (n = 5 studies), and parasitic infection (n = 6 studies). Indirect risk factors found to be associated with anaemia among adolescents included low educational status (n = 4 studies) and low socioeconomic status (n = 3 studies). All fifteen studies were of good quality. Conclusion Food intake practices, female adolescents, menstruation, parasitic infection, and low educational status were the leading risk factors of iron deficiency anaemia among adolescents. Further research should concentrate on assessing the effectiveness and efficacy of existing interventions aimed at preventing iron deficiency among vulnerable groups in developing countries.


Introduction
Adolescents undergo physiological and psychological growth to set the foundation of adulthood. Te biological well-being of adolescents requires improved nourishment. It has been revealed that prolonged insufcient intake of foods rich in micronutrients such as iron, zinc, and vitamin A relevant to support the biological metamorphosis in adolescents can adversely afect their growth and well-being [1]. Te majority of adolescents habitually skip breakfast, fruits, vegetables, and milk daily, reducing their dietary intake [2,3]. Adolescents with such dietary practices manifest micronutrient inadequacies such as iron, calcium, zinc, folic acid, and vitamins A, D, and C [4,5]. Tese defciencies expose adolescents to perpetual nutritional and health vulnerabilities.
Defciencies of iron, folate, and vitamin B 12 contribute to nutritional anaemia in adolescents [6,7]. Among the different types of nutritional anaemias, iron defciency anaemia is the most prevalent [8][9][10]. Iron defciency anaemia (IDA) is measured with indicators such as haemoglobin, serum ferritin, transferrin receptors, transferrin saturation/total iron binding capacity, and zinc protoporphyrin [11,12]. Anaemia is mostly defned as low haemoglobin levels in the blood or haemoglobin levels less than 120 g/l in adolescents [13].
Statistics show that about 30-35% of the world's population sufers from iron defciency anaemia, which afects about 47.5% of people living in Africa [7,14]. Populations most at risk of iron defciency anaemia are children aged less than fve years, adolescents, women of reproductive age, pregnant women, and lactating mothers [14].
To ameliorate the prevalence and consequences of iron defciency anaemia in adolescents, a review study recommended the identifcation of localized risk factors of iron defciency anaemia to aid in efective management and prevention [15]. Predictors of iron defciency anaemia among adolescents have been reported by diferent studies in several countries [16][17][18]. In developing countries, risk factors of IDA include but are not limited to malaria, worm infestation, low dietary iron intake, micronutrient defciencies, the human immunodefciency virus, and inherited disorders [19]. Te wide variety of contributory factors of IDA reported by many studies negatively impacts adolescent's health. Due to this, several interventions have failed to reduce the high prevalence of IDA among adolescents in the long term.
Iron defciency anaemia negatively impacts the educational and economic well-being of adolescents. It has been associated with stunting, wasting, being underweight, poor cognitive function, low physical activity, and attention defcit hyperactive disorders in adolescents [20][21][22][23][24][25][26]. Iron defciency anaemia is now known to be the leading cause of disability adjusted live years in adolescents [27].
To successfully address iron defciency anaemia, it is critical to holistically identify the key risk factors afecting adolescents that contribute to this defciency. Te systematic review assessed the risk factors of iron defciency anaemia among adolescents living in developing countries.

Study Design and Search
Strategy. Tis systematic review was conducted following the guidelines provided by Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) [28]. Te current review defned an adolescent as an individual with an age ranging from 10 to 19 years [29]. Te list of developing countries considered was based on country classifcations by the United Nations Children's Fund [30]. A comprehensive search of articles published from January 1990 to December 2020 was sourced from Google Scholar, PubMed, Scopus, Science direct, and Cochrane Library. Te search terms used either singly or in combination included risk factors of anaemia, iron defciency anaemia, determinants of anaemia, predictors of anaemia, anaemia in adolescents, low haemoglobin, anaemia, and adolescents.

Study Selection and Eligibility Criteria.
Te review focused on studies with the primary objective of identifying risk factors of iron defciency anaemia (IDA) among adolescents living in developing countries. Studies conducted among adolescents without any underlying health conditions were included. Research conducted among adolescents with pregnancy, lactating, sickle cell, or genetic haemoglobin or with any underlying condition, age group mixed, and other forms of anaemia were excluded. Studies with inaccessible full articles, non-English written articles, and articles published before 1990 were also excluded.

Outcomes Assessed.
Te outcomes assessed in this review were risk factors of iron defciency anaemia among adolescents. Te primary outcomes were the risk factors directly associated with adolescents contributing to iron defciency anaemia. Te secondary outcomes were risk factors indirectly associated with adolescents, leading to iron defciency anaemia.

Data Extraction and Synthesis.
Te primary information from each study was extracted by one researcher. Te primary information for the review included the following: author (s), country, year, gender, age, sample size, and risk factors of iron defciency anaemia. Te data are summarized in Table 1.

Quality Assessment.
Te methodological quality assessment of each study was checked using the American Dietetic Association Quality Criteria Checklist [46]. Te overall quality of each study was rated positive, negative, or neutral. Te fndings of the quality assessments are shown in Table 2.

Study Selection.
A total of 2,252 articles were retrieved from the fve databases. Six hundred and eighteen (618) duplicates were removed and one thousand, four hundred and ninety-two (1,492) records were excluded after screening by title and abstract. One hundred and forty-two (142) articles were fully assessed for eligibility, and one hundred and twenty-seven (127) articles were also excluded based on the inclusion and exclusion criteria. Finally, ffteen (15) studies were included in the review ( Figure 1).

Study Characteristics.
All studies included in this review were cross-sectional and published between the years 1990 and 2020. Five studies were conducted in Ethiopia [31,32,34,36,38]; four studies were also conducted in India [37,39,40,43]; two studies were conducted in Kenya [41,44]; and one study was conducted in Ghana [33], Egypt [45], Nepal [35], and Iran [42]. Only two of the studies had nationwide representation [35,45]. Eight of the studies recruited exclusively female adolescents and seven of the studies recruited adolescents of mixed gender. Te studies had sample sizes ranging from 137 to 2,032. Participants were aged 10-19 years (Table 1). Table 2 shows the quality assessment of the studies using the quality control checklist. All studies were cross-sectional, and attributes of the quality criteria checklist were modifed for maximum use in assessment. Attributes such as "comparable study groups" 2 Anemia   N/A, not applicable (due to cross-sectional design of study); NR, not reported. +, positive overall score: this overall score is given if criteria 2, 3, 6, and 7 of the QCC and one additional criterion have received a positive score. Ø, neutral overall score: this score is given if more criteria are met than for a negative overall score, but an overall positive score is not reached. −, negative overall score: this score is given if six or more QCC criteria are not met.

Anemia 5
and "use of blinding" were not applicable for the assessment of the studies. All ffteen studies had a positive quality rating.

Associated Factors of Adolescent Iron Defciency Anaemia.
Te various studies assessed diferent factors contributing to iron defciency anaemia among adolescents in developing countries. For this review, the factors have been grouped under direct factors: food intake practices, malaria infection, worm infestation, female adolescents, blood loss, and indirect factors: educational status, socioeconomic status, rural areas, family size, religion, and walking barefoot ( Figure 2).

Food Intake Practices.
Ten studies assessed the relationship between iron defciency anaemia and food intake practices among adolescents. Tree of these studies indicated that vegetarian dietary practices increased the odds of anaemia among adolescents [39,40,43]. Kuar et al. [42] reported that vegetarian adolescents had higher odds of being anaemic than those who consumed a mixed diet (OR = 8.5, 95% CI = 5.7-12.8). In another cross-sectional study, vegetarian adolescents had a 4.4% greater chance of being anaemic than their counterparts who did not practice vegetarianism [40]. Two studies reported on dietary diversity. Te studies documented that low dietary diversity signifcantly increased adolescents' risk (AOR = 3.57, 95% CI: 1.88-6.75) [31] and (AOR = 2.33, 95% CI: 1.2-4.86) [32] of being anaemic. Furthermore, low dietary iron intake signifcantly increased anaemia among adolescents [41,43]. Two studies reported on meal skipping and meal frequency [33,36]. Adolescents who skipped meals and had a low meal frequency had high chances of being anaemic. One study among adolescents in Ghana showed that snacking was not signifcantly associated with anaemia (β = 0.484, p > 0.05) [33].

Parasitic Infections.
Six studies reported on parasitic infections. Malaria and worm infestations, particularly schistosomiasis and ova ascaris, were the common parasitic infections found among adolescent girls in the studies 6 Anemia included in this review. Five studies indicated that worm infestation signifcantly increased the odds of anaemia incidence in adolescents [40][41][42][43][44]. One cross-sectional study reported that malaria signifcantly increased the odds of anaemia in adolescents (OR � 3.68, 95% CI: 1.69-7.98) [41].

Educational Status.
Among the four studies that reported on educational status as a risk factor of anaemia, three studies indicated that maternal education was a key determinant [32,39,45]. El Sahn et al. [45]; reported that the risk of anaemia increased signifcantly with decreased level of education (OR = 3.5, 95% CI: 10.90-6.32). Adolescents with education up to the junior high school level or lower were found to have increased odds of being anaemic [32,33].

Socioeconomic Status.
Tree studies assessed the relationship between socioeconomic status and anaemia. Te outcome indicated that low socioeconomic status increased the odds of anaemia in adolescents [31,39,45]. All studies found adolescents with low socioeconomic backgrounds to have increased odds of being anaemic, OR = 2.16, 95% CI:

Rural Areas.
Two studies reported on rural areas and anaemia [36,38]. Te studies showed that adolescents living in rural areas had an increased risk of anaemia. Regasa and Haidar found that the odds were statistically signifcant.

Family Size.
Two studies assessed the relationship between family size and anaemia [36,42]. Te studies indicated that large family size increased the odds of anaemia. Ramzi et al. [42] showed signifcant association, while Shaka and Wondimagegne [36] indicated otherwise.

Religion.
Only one study investigated the association between religion and anaemia. However, the results of the study showed no signifcant efects of religion on anaemia among adolescents [39].
3.14. Walking Barefooted. Only one study reported that adolescents who walk barefooted have higher odds of having anaemia [35]. According to the authors, adolescents who walked barefoot had a 1.78 chance of being anaemic (AOR � 1.78, 95% CI: 1.08, 2.94).

Discussion
Te prevalence of anaemia among adolescents is of public health concern despite the application of varied interventions. Management and prevention of iron defciency anaemia are complex, indicating that diferent factors contribute to IDA in diferent geographical settings. Te present study assessed the risk of iron defciency anaemia among adolescents in developing countries. Te risk factors of iron defciency anaemia among adolescents are conglomerate. However, food intake practices, low educational status, parasitic infections, older adolescent girls, menstruation, and low socioeconomic status were the leading risk factors that predispose adolescents to iron defciency anaemia ( Figure 2).

Food Intake Practices.
Adolescents prefer to explore their dietary environment and, thus, consume foods that are pleasing to the eyes with little or no consideration of the nutrients needed for their growth and well-being. Most adolescents binge on junk foods due to the neglect of a nutritious diet [47]. Tese poor food choices afect their nutrient needs, leading to micronutrient defciencies, particularly anaemia. Te negative efects of IDA on learning, scholastic performance, and achievement among adolescents contribute to dropout rates [21,23,25]. Adolescents with low educational status are unable to gain employable skills, thereby afecting their economic status [48]. Unskilled labour pays less as guardians are unable to give their children a good education and also meet their nutritional needs. Tese adolescents also become mothers of children with iron defciency anaemia to perpetuate the cycle of consequences of anaemia. In this review, most of the studies found that vegetarian dietary practices increased the risk of anaemia among adolescents [39,40,43]. Inadequate dietary iron intake [41,43] and low dietary diversity [31,32] were second in contributing to IDA among adolescents. Most iron-rich food sources are expensive in developing countries [49].
Other food intake practices, such as meal skipping, lower meal frequency, lower dietary diversity, household food insecurity, and snacking, also increased the risk of IDA among adolescents. Poor nutrition has been a major risk factor for IDA among adolescents [40,50].

Adolescent Girls.
Our review showed that female adolescents had a higher risk of iron defciency anaemia, particularly older girls. It was thus not surprising that eight of the ffteen studies focused on female adolescents [31,34,37,38,[41][42][43][44]. Older girls may prefer to eat out of home, skip meals, and diet to maintain certain body curvature, making them more vulnerable to IDA. Most guardians have less control over an older adolescent girl's food intake. Te fear of gaining weight and low nutrition knowledge infuence the eating habits of adolescents and contribute to IDA [51,52]. Menstruation and childbearing have increased the odds of anaemia in older adolescents. A nationwide study in Namibia, Malawi, Zimbabwe, and Mozambique showed that anaemic mothers have higher odds of delivering children with low haemoglobin levels [53].

Guardian Education.
Low educational status of guardians, particularly mothers, has been linked to a high risk of anaemia in adolescents in diverse settings and studies [32,39,57]. Mothers with limited formal education may not be able to read and understand food labels. Knowledge levels of nutrition by mothers are critical as most are key kitchen persons in most homes infuencing food preparation, dietary choices, and intake of the family. Maternal education status has been shown to infuence children's normal haemoglobin levels [58]. Te education level of fathers and adolescents rarely led to iron defciency anaemia within our target group.

Socioeconomic Status.
Higher maternal education and employment status reduce the odds of iron defciency anaemia in children [59]. Guardians with low educational status have low skilled employment with poor remuneration [60]. Low socioeconomic status due to unemployment affects the purchasing power of the household. Adolescents largely depend on guardians or parents for their fnancial and dietary needs. Households with low socioeconomic status face the risk of food insecurity, low dietary diversity, and inadequate food intake, which pose health risks [61,62].

Strength and Limitations.
Te study gives an overview of the risk factors of iron defciency anaemia among adolescents in developing countries. Te sample sizes of most of the studies were not nationally representative, and female adolescents were the target for most of the studies; therefore, the outcome cannot be generalized.

Conclusion and Further Directions
Te review showed that food intake practices, parasitic infections, menstruation, increasing age of female adolescents, and low educational status of guardians were the leading risk factors of iron defciency anaemia among adolescents in most developing countries. Funding agencies should support nationally representative nutrition research to continue to identify localized risk factors that precipitate IDA among adolescents. Further studies should focus on assessing the efectiveness and efcacy of already existing interventions such as iron-folic acid supplementation, nutrition education, use of insecticide mosquito nets, and intermittent deworming of adolescents, and developing appropriate policies and programmes to strenghten such interventions. Developing countries should continue to adopt policies and programmes to sustain girl child education, maternal education, and economic empowerment of guardians, particularly women, to reduce the prevalence and 8 Anemia menace of IDA in adolescents. Governments and nongovernmental organizations should prioritize adolescent nutrition as it is another gateway to having a positive impact on the lifecycle.

Data Availability
Te data supporting this systematic review are from previously reported studies and datasets, which have been cited. Te processed data can be obtained from the corresponding author upon reasonable request.

Ethical Approval
Findings of the study were in the public domain; therefore, the authors needed no ethical approval for the systematic review.