Anemia and Associated Factors among Public Elementary School Children in Asella Town, Southeast Ethiopia: A Facility-Based Cross-Sectional Study

Background Anemia has a negative impact on school children, including poor physical growth and reduced mental performance. Children show poor attentiveness, behavior, and memory and reduced school performance. There is limited evidence of the magnitude of anemia and associated factors in school-age children in Ethiopia, including the study area. Objective To assess the magnitude of anemia and associated factors among public elementary school children in Asella Town, Southeast Ethiopia, in 2022. Methods A school-based cross-sectional study was conducted in Asella Town from April 5 to May 5, 2022. A total of 442 school children aged 7–14 years were included in the study using the multistage sampling method. Data were collected using a pretested and semistructured questionnaire through a face-to-face interview technique. The hemoglobin concentration was determined by using the HemoCue 301+ analyzer. Anthropometric data and stool examinations were collected from participants. Data were entered into EpiData version 4.6, transported, and analyzed by Statistical Package for Social Sciences version 26. Bivariable and multivariable logistic regression analyses were carried out. Adjusted odds ratios along with their 95% confidence interval were used, and a p value of ≤0.05 was used for declaring statistical significance. Results A total of 435 students with a mean age and standard deviation of 10.77 ± 2.21 years participated in the study. The magnitude of anemia was 78 (17.9%), with a 95% CI (14.3, 21.47). Of the participants, 63 (14.5%) were mild anemic and 15 (3.4%) were moderately anemic. Children whose mothers have no formal education (AOR = 3.94, 95% CI: 1.89, 8.21), underweight children (AOR = 3.83, 95% CI: 1.98, 7.40), and parasites in their stool (AOR = 3.72, 95% CI: 1.50, 9.20) were significantly associated with anemia in school-age children. Conclusion Anemia among school-age children was found to be a mild public health problem. Uneducated mothers, intestinal parasite infections, and underweight children were found to be determinants of anemia among school-age children. Health professionals should provide health education for mothers about child-feeding practices and the consumption of dietary sources of iron.


Introduction
Anemia is a condition in which the number and size of red blood cells, or the hemoglobin concentration, fall below an established cut-of point, consequently impairing the capacity of the blood to transport oxygen around the body [1,2].Anemia is an indicator of both poor nutrition and poor health [1].When hemoglobin (Hob) levels fall below the population-specifc Hob threshold, it is considered a public health issue [3] and can be classifed as no, mild, moderate, and severe public health problems when the prevalence is ≤4.9%, 5.0-19.9%,20.0-39.9%,and ≥40%, respectively [2,4].
Te World Health Organization (WHO) defnitions of anemia vary by age, and the sixth WHO defnes anemia in children aged 5-11 years as hemoglobin <11.5 g/dl and in children aged 12-14 years as hemoglobin <12 g/dl [5].Among school-age children, it could be due to inadequate consumption of nutrient-rich foods, dietary taboos, lack of access to health care, and inefcient utilization of available micronutrients due to cause of infections and parasitic infestations, among other reasons [4,6,7].Anemia is a worldwide public health problem afecting both developing and developed countries, with major negative impacts on human health and social and economic development [8].
Globally, around 1.62 billion people are afected by anemia, which accounts for more than 24.8% of the world population, and from 30 to 50% of anemia is caused by iron defciency.Iron defciency anemia (IDA) resulted in 273,000 deaths in the world, and 97% of deaths occurred in developing countries.According to a WHO report, the global anemia prevalence of school-age children (SAC) was 25.4%, followed by preschool children under 5 years old (47.4%) [9].Anemia results from one or more of the following processes: defective red cell production, increased red cell destruction, or blood loss [9].Iron is necessary for the synthesis of hemoglobin [9].Iron defciency is thought to be the most common cause of anemia globally, but other nutritional defciencies such as folate, vitamin B12, and vitamin A, acute and chronic infammation, parasitic infections, and inherited or acquired disorders that afect Hob synthesis, red blood cell production, or red blood cell survival can all cause anemia [10,11].At least half the burden of anemia is associated with iron defciency [11].
Africa and Southeast Asia are the regions that present the highest prevalence of this disease [12].A study conducted in eight countries in Africa and Asia showed that 12-58% of SAC are sufering from anemia and 12%, 41%, 54%, 57%, and 58% in Malawi and Kenya, Ghana, Mozambique, Tanzania, and Mali, respectively, and 30% in Vietnam and Indonesia [13][14][15].More than 40% of SAC in developing countries sufer from anemia, and it is considered a severe public health problem.Sub-Saharan African countries shared a greater burden of the problem [16].
Children are particularly vulnerable to iron defciency anemia (IDA) because of their increased iron requirements during periods of rapid growth, especially in the frst 5 years of life [17].Public health interventions to ameliorate micronutrient malnutrition in preschool and school-age children include the promotion of dietary diversifcation to include foods rich in highly absorbable vitamins and minerals, anthelminthic treatment, mass fortifcation of staple foods and condiments, home (point-of-use) fortifcation of foods, and provision of micronutrient supplements [18].
Iron defciency, a common form of nutritional defciency during childhood, results from sustained negative iron balance, which is caused by inadequate dietary intake, absorption or utilization of iron, increased iron requirements during the growth period, or blood loss due to parasitic infections such as malaria, soil-transmitted helminth infestations, and schistosomiasis.In later stages of iron depletion, the hemoglobin concentration decreases, resulting in anemia [18].Te main risk factors for IDA include a low dietary intake of iron or poor absorption of iron from diets rich in phytates or phenolic compounds [4].Anemia has a negative impact on school children (SC), including poor physical growth, and children show poor attentiveness, behavior, and memory and reduced school performance [19].Children who sufer from anemia have reduced mental (cognitive) performance, poor attention span and learning ability in children, delayed psychomotor development, impaired work performance, and increased morbidity because of reduced resistance (low tolerance) to infection; in addition, they experience impaired coordination of language and motor skills, equivalent to a 5-10 point defcit in intelligence quotient [9,12,[20][21][22].Anemia has detrimental efects on the cognitive performance and physical development of school children, which can lead to low productivity, limited work capacity, delayed physical growth, and poor academic achievement [17,23,24].
Studies conducted in Ethiopia documented that factors that afect anemia in school-age children were mother occupation status, father occupation status, maternal education, father education, family size, parasites in the stool, stunted, and underweight [12,15,16,[24][25][26][27][28][29].Te Ethiopian government has been working to address the nutritional concerns of SAC, mainly by integrating nutritionally sensitive interventions such as conducting regular monitoring of the nutritional status of school-age children/students together with biannual deworming and water hygiene and sanitation (WASH) programs in schools [30], mass fortifcation of staple foods and condiments, home (point-of-use) fortifcation of foods, initiating a homegrown school feeding program for school-aged children, and provision of micronutrient supplements and weekly iron and folic acid supplementation (WIFAS) [19,31].
Tere is limited evidence on the magnitude of anemia and associated factors in school-age children in Ethiopia, including the study area.Terefore, this study aimed to assess the magnitude of anemia and identify associated factors among SC attending public elementary schools in Asella Town, Southeast Ethiopia.

Methods and Materials
2.1.Study Design, Period, and Setting.A school-based crosssectional study design was conducted in public elementary schools in Asella Town from April 5 to May 5, 2022.Asella is the capital city of the Arsi Zone, which is located at a distance of 165 km from Addis Ababa, Southeast Ethiopia.Te estimated population of Asella Town in 2022 is 113,445, of whom 57,290 are male and 56,155 are female.According to the education ofce of the town, Asella Town has a total of 27 primary schools (9 governmental and 18 private) during the study.In the academic year 2022, there were a total of 11654 students from grades 1-8.From this, about 46.6% of students were female.Regarding the health facilities of the town, there is one referral hospital, two governmental health centers, eight health posts, fourteen medium clinics, and thirty pharmacies and drug stores.

Source Population.
Te source population for this study was all SC (aged 7-14 years) in public elementary schools in Asella Town.

Study Population.
Te study population was all school children (aged 7-14 years) in the randomly selected elementary schools in Asella Town.
By comparing the frst and second objectives, the maximum sample size was 201 from the frst objective, and by considering the design efect of 2 and 10% of the nonresponse rate, the fnal sample size was 442.Te sample size was calculated for the second objective (selected associated factors) using Epi Info, assuming a two-sided confdence level � 95%, power � 80%, and ratio � 1 (Table 1).

Sampling Procedure.
A multistage sampling procedure was used to choose the study participants.In the beginning, governmental elementary schools in the town were registered.Ten, three governmental schools were randomly selected from 9 elementary schools found in Asella Town using the lottery method.Ten, the study participants in the target age group enrolled in the selected schools were identifed and the total number of students was obtained from each school director's ofce.Based on the number of students in each school and class/grade, the sample size was proportionally distributed across the selected schools.Next, the number of participants required to be enrolled was allocated proportionally based on the number of students in each class and grade level.Finally, the allocated sample size was selected from each school by a simple random sampling procedure using computer-generated random numbers (Figure 1).

Data Collection Tools and Procedures.
Questionnaires were adapted and modifed from studies [12,16,26].Te questionnaire contains variables on sociodemographic characteristics, educational status, and factors associated with anemia.Tree BSc nurses and two medical laboratory technologists were recruited for data collection, and one senior laboratory technologist checked for discrepancies between the two data collectors.One health ofcer was recruited as supervisor, and the investigators were supervised for leading the whole data collection process.Data were collected through a face-to-face interview in the language of the respondent by using a semistructured Afaan Oromo version questionnaire and laboratory investigation.
2.5.1.Anthropometric Measurements.Anthropometric data were collected by recording the age, weight, and height of the participants according to the WHO guidelines [33].A portable digital weight scale with a capacity of 120 kg was used, and each child was weighed with slight clothing and barefoot and recorded to the nearest 0.1 kg.Height was measured in the Frankfurt position (head, shoulder, buttocks, knee, and heels touching the vertical board) by using a portable wooden height board (audiometers) with a sliding head bar, and then, height was measured to the nearest 0.1 cm.Every measurement was calibrated by placing standard calibration weights on the scale to ascertain accuracy.Measurements of weight and height were taken twice, and the mean was recorded [33].
To determine the nutritional status of school children, the anthropometric measurements were converted into height-for-age Z score (HAZ) and body mass index (BMI)for-age Z score (BAZ) using WHO AnthroPlus (version 1.0.4).Children whose BAZ was below −2 standard deviation (SD) and whose BAZ was >−2 SD of the WHO standard were classifed as wasted and normal, respectively.However, stunting was used as an indicator of chronic malnutrition and was defned as HAZ < −2 SD of the WHO standard [4,34].

Hemoglobin Measurement.
Te hemoglobin level was adjusted for the altitude of the town before defning anemia [5] by using the formula: Hob � −0.32 × (altitude in meters × 0.0033) + 0.22 × (altitude in meters × 0.0033) [16,17].Ten, the Hob concentration of each participant was measured by pricking the tip of the fnger with a sterile disposable lancet.Te frst and second drops of blood were wiped away, and the third drop of blood was allowed to enter the optical window of the microcuvette through capillary action and using a portable hemoglobinometer instrument (HemoCue 301+ analyzer, Sweden), which was recommended by the WHO for the use of feld surveys [4,10,22,35].Two trained senior laboratory technologists and one senior laboratory technologist were involved when the discrepancy occurred between the two data collectors.
Te cuvette holder was cleaned every day with alcohol or mild detergent (checking the operating manual) and the optical unit was cleaned, once a month with a HemoCue cleaner (cleaning swab), which comes together with the analyzer.Also, it is cleaned after 50 measurements or when an error message is shown.Hemoglobin readings were corrected for altitude by subtracting the expected normal increase in altitude proposed by the WHO based on the altitude of the town nearest to each school [33].Anemia 2.5.3.Stool Examination.From each study participant, fresh stool samples were collected following the standard operating procedures (SOPs) in clean and labelled leak-proof stool cups.Te stool specimens were transported in screwcapped cups in 10% formalin to the laboratory.Intestinal parasites were detected microscopically by direct saline wet mount.A saline wet mount was made by mixing a small quantity (about 2 mg) of feces in a drop of saline placed on a clean glass slide.Ten, the smear stool was examined under a microscope.A saline wet mount was used for the detection of trophozoites and cysts in protozoa and eggs and larvae in helminths.
2.6.2.Independent Variables.Sociodemographic characteristics of school children and parents or guardians are as follows: respondent age, sex, ethnicity, grade level of children, religion, marital status of parent, occupational status of parent, educational level of parent, and family size.
Nutrition-related factors are as follows: stunting, wasted, underweight, taking tea and/or cofee within 30 minutes after a meal, and dietary diversifcation.

Measurements and Operational Defnitions
Anemia: hemoglobin level <11.5 g/dl for age ranges from 5 to 11 years (5,9,12) Mild Anemia: hemoglobin level of 11.0-11.4g/dl for age ranges from 5 to 11 years (5,9,12) Moderate Anemia: hemoglobin level of 8.0-10.9g/dl for age ranges from 5 to 11 years (5,9,12) Severe Anemia: hemoglobin level of <8.0 g/dl for age ranges from 5 to 11 years (5,9,12) Anemia: hemoglobin level below 12 g/dl for age ranges from 12 to 14 years (5,9,12) Mild Anemia: hemoglobin level of 11.0-11.9g/dl for age ranges from 12 to 14 years (5,9,12) Moderate Anemia: hemoglobin level of 8.0-10.9 for age ranges from 12 to 14 years (5,9,12) Severe Anemia: hemoglobin level of <8.0 g/dl for age ranges from 12 to 14 years (5, 9, 12)  4 Anemia Dietary Diversity Score: it was calculated from ten food groups, and children getting greater or equal to 7 food groups were classifed as getting high dietary diversity; otherwise, they were considered as getting medium and low dietary diversity scores of 4-6 and less than or equal to 3, respectively [12] Intestinal Parasite Infection: the participant was recorded as positive for intestinal parasites if the stool sample examined by microscopy became positive for ova, cysts, or trophozoites of any parasites [36,37] 2.8.Data Quality Assurance.A questionnaire was prepared in English and then translated into Afaan Oromo for appropriateness and easiness by linguistic language experts.Te Afaan Oromo questionnaire was again translated back to the English language to verify the content validity of the original version.Te training was given to data collectors and supervisors for two days on the method of anthropometric measurements, blood and stool sample collection and examination, ethical issues, and the purpose of the study.Hemoglobin measurement and stool microscopic examination were carried out following standard operating procedures (SOPs), and a HemoCue Hob 301 analyzer was used to determine the hemoglobin level.A direct stool examination using a saline smear was used to investigate the intestinal protozoa, eggs, and larvae of helminths.Daily monitoring was carried out during the data collection period.A pretest was conducted on 5% of students at primary schools in Iteya Town, which is located 25 kilometers away from the study area, and necessary modifcations were made.
2.9.Data Processing and Analysis.Te collected data were checked for completeness, coded, and entered into EpiData version 4.6 and then exported to SPSS for Windows version 26 for statistical analysis.Descriptive statistical analysis was used to compute the frequency and percentage of independent and dependent variables.Bivariable analyses were carried out by using a binary logistic regression model to select candidate variables for multivariable logistic regression analysis.Variables with a p value <0.25 in the bivariable analysis were transferred to the multivariable analysis to control the efect of confounders.Te strength of association was measured using adjusted odds ratios with a p value less than or equal to 0.05 together with 95% confdence intervals in the multivariable analysis and was considered signifcantly associated.Multicollinearity was also checked among selected variables by using a cut-of point of variance infation factor <10.However, the result of VIF for all variables was found to be less than 10 (VIF � 5.62), which indicates there was no multicollinearity among variables.Te Hosmer-Lemeshow model was used to check model ftness, and its p value was found to be 0.64.Finally, the results were presented in the form of tables, fgures, and texts based on the obtained data.

Sociodemographic Characteristics of the SAC.
A total of 435 school-age children have participated in this study, making a response rate of 98.4%.Of the total, 227 (52.2%) were male.Participants ranged in age from 7 to 14 years, with a mean age of 10.77 and an SD of 2.21.Two hundred ffty-one (57.7%)SC were aged 7-11 years.Tree hundred forty-two (78.6%) participants were Oromo in ethnicity.Two hundred thirty-one (53.1%) participants were in grades 1-4.Te estimated mean family size of the participants was 5.20 and 1.662 SD, and 279 (64.1%) participants had 5 or more family members (Table 2).

Magnitude of Anemia among School-Age Children.
Te magnitude of anemia among SAC was 78 (17.9%) with a 95% CI (14.33, 21.47).Te hemoglobin level of the SAC ranged from 10.1 g/dl to 15.4 g/dl with a mean (±SD) value of 12.78 ± 1.107 g/dl.Forty-eight (19.1%)SAC who had anemia were in the age group of 7-11 years, of whom 30 (16.3%) were in the age group of 12-14 years (Figure 2).

Dietary Diversity Practice of School-Age Children.
Regarding the dietary diversity score (DDS), the mean dietary diversity score of respondents was 5 (±1.373).Tree hundred twenty-fve (74.7%) had a medium dietary diversity score and consumed four up to six diferent food groups, followed by 53 (12.2%)SAC, who had a high dietary diversity score of seven and above food groups, and the rest of the respondent had a low DDS of three and below food groups.Te minimum dietary diversity score of school-age children was 2 (consumed only two food groups), and the maximum dietary diversity score was 9 out of 10 food group items (Figure 3).

Factors Associated with Anemia among School-Age
Children.In the bivariable analysis, father occupation, mother occupation, family size, mother educational status, father educational status, underweight, dietary diversifcation, and intestinal parasite were signifcantly associated with anemia among school-age children at p value less than 0.25.Te result of the multivariable logistic regression model revealed that mother education, underweight, and intestinal parasites were found to be signifcantly associated with anemia among school-age children at a p value of ≤0.05 together with 95% confdence intervals.
Children who were positive for intestinal parasitic infections were 3.72 times more likely to be anemic than those who were negative for intestinal parasitic infections Anemia (AOR � 3.72, 95% CI: 1.50, 9.20).Students whose mothers had no formal education were 3.94 times more likely to be anemic than students whose mothers had secondary and above levels of education (AOR � 3.94, 95% CI: 1.89, 8.21).Underweight children were 3.83 times more likely to be anemic than normal weight children (AOR � 3.83; 95% CI: 1.98, 7.40) (Table 4).

Discussion
Te overall magnitude of anemia among school-aged children identifed in this study is 17.9%, with a 95% CI (14.33, 21.47).Tis study identifed factors that established an association with anemia among school-aged children such as intestinal parasitic infections, maternal education, and being underweight.
Te magnitude of the present study was in line with the study conducted in Gondar Town (15.5%) [12] and North-Western Morocco (16.2%) [38].However, this result was lower than a study conducted in Indonesia (45.57%),Egypt (38.7%),Somaliland (23.1%),Arab Minch (37.3%),Pawe Town, Northwest Ethiopia (33.9%) [15,16,28,39], and Gurage Zone (21.71%) [40].Te diference might be related to the diference in sample size used, study population, setting of the study area, time period gap among studies, geographical variation, and socioeconomic status.Currently, in Ethiopia, there are several interventions made by the Ministry of Health through health extension workers that might contribute their share to decreasing the burden of anemia among school children.
Te magnitude of anemia in this study is higher than that in a study conducted in Northwest Ethiopia (7.6%) [41], Durbete Town, Northwest Ethiopia (10.7%) [29], and China (8.4%) [27].Te discrepancy may be attributed to the diferences in socioeconomic, sociodemographic, and cultural behaviors, studied population, and study period and setting.
In this study, maternal education was found to be signifcantly associated with anemia in SC.Children whose mothers had no formal education were 3.94 times more likely to be anemic than children whose mothers had secondary and above levels of education.Tis fnding is supported by the study conducted in Egypt, Somaliland, Gondar Town, and Pawe Town [12,26,28,39].Tis might be related to a low level of awareness among uneducated mothers to understand the nutritional requirements of children, easily follow the recommended child-feeding practices, and use diversifed diets including iron and other micronutrients.
Underweight children were 3.83 times more likely to be anemic than normal weight children.Our fnding was in agreement with studies conducted in Pawe Town, Benishangul-Gumuz Region [19].Tis might be related to the fact that underweight is due to acute or chronic inadequate nutrition intake.In addition, not washing hands before eating may cause an acute bacterial or parasitic infection that would lead to diarrhea or malabsorption problems and acute undernutrition.Also, this might be due to the long-term efects of low iron intake and other micronutrient defciencies.
School-age children infected with intestinal parasites are 3.72 times more likely to be anemic than noninfected children.Tis fnding was supported by studies conducted in Somaliland, Filtu Town, Arba Minch, Gondar Town [13,16,19,21], and Mihur Na Aklil District of Gurage Zone [40].Tis may be because the majority of intestinal parasites, particularly hookworm and ascariasis, contribute to blood loss and/or red cell destruction and thus contribute to anemia.In addition, this might be due to nutritional competition, red blood cell destruction and feeding, and loss of appetite caused by worms.Additionally, these parasites directly invade and damage the intestinal mucosa wall, which impairs the absorption of nutrients.

Conclusion
In this study, the magnitude of anemia was a mild public health problem among the SAC.Intestinal parasitic infections, maternal education, and being underweight were found to be the major factors that contributed to the development of anemia in the study area.Tus, health professionals should provide health education for mothers about child-feeding practices and consumption of dietary sources of iron to reduce the burden of anemia, and the Asella Town Health Ofce should strengthen nutrition education, good hygiene, and sanitation in the community and school.
Te families of the study participants should focus on periodic deworming of their children, which is an essential intervention in children because intestinal parasites, particularly hookworm infection, lead to blood loss in the intestines, which, in turn, contributes to anemia.Asella Town Education Bureau should work on strengthening the schools to improve personal hygiene and environmental sanitation and control the transmission of these parasites, and school teachers should advise both children and their parents regarding the advantages of a balanced diet.manuscript, and edited the manuscript.KK, MM, and DBS proposed the methodology, contributed to project administration, provided resources, contributed to data curation, performed analysis, performed investigation, performed supervision, contributed to validation, wrote the review of the manuscript, and edited the manuscript.

Figure 1 :
Figure 1: Schematic presentation of the sampling procedure for the assessment of anemia and associated factors among public elementary school children in Asella Town, 2022.

Figure 2 :
Figure 2: Magnitude of anemia among school-age children in public primary school students in Asella Town, Southeast Ethiopia, 2022.

Figure 3 :
Figure 3: Dietary diversity score among school-age children in public primary school students in Asella Town, Southeast Ethiopia, 2022.
[12]ents treated for intestinal schistosomiasis and/or soil-transmitted helminths in the past month and children with deformity were excluded.2.3.Sample Size Determination.Te sample size for the frst objective was determined using Epi Info 7 by consideration of the following assumptions: prevalence of 15.5%[12], 95% confdence level, 5% margin of error (d), design efect of 2, and nonresponse rate of 10%.

Table 1 :
Double population proportions based on factors associated with anemia in school children in Asella Town, Oromia Regional State, Southeast Ethiopia, 2022.

Table 2 :
Sociodemographic characteristics of SAC among public primary school students in Asella Town, Southeast Ethiopia, 2022.

Table 3 :
Anthropometric and clinical characteristics of school-age children in public primary school students in Asella Town, Southeast Ethiopia, 2022.

Table 4 :
Bivariable and multivariable analysis of selected variables associated with anemia among SAC in public primary school students in Asella Town, Southeast Ethiopia, 2022.Limitations of the Study.Tis study used a crosssectional study design that does not show cause-and-efect relationships.Recall bias might have been introduced.Tere are a few limited reference materials used to compare similar studies in the same study area.