Anemia is a disease in which reduced hematocrit or hemoglobin levels lead to hemoglobin (Hgb), diminished oxygen-carrying capacity that does not optimally meet the metabolic demands of the body, as a result of deficiency of one or more essential nutrients, heavy blood loss, parasitic infections and congenital hemolytic diseases . Anemia is a global public health problem affecting the majority of the population of the world in both developed and developing countries with major consequences on human health as well as social and economic development. It is the world’s second leading cause of disability of the whole global disease burden  . It is considered as a public health problem when the hemoglobin (Hb) value is below the population-specific Hb threshold.
It can be classified as no, mild, moderate, and severe public health problem when the prevalence is ≤4.9%, 5.0% - 19.9%, 20.0% - 39.9%, and ≥40%, respectively . It affects 1.62 billion (24.8%) of the population, among them it is affecting 305 million (25.4%) school-age children (SAC) . Despite implementation of control programs including iron supplementation, deworming and insecticide-treated bed net distribution, and anemia remains a major global concern in child health, especially in SSA . While it may be difficult to separate the effects of anemia (low hemoglobin (Hb)) from those of its underlying biological mechanisms (e.g., nutritional deficiency, chronic infections, heamoglobin pathoies), anemia has been independently associated with overall increased mortality in young children’s . Several international studies have examined the role of demographic, social, environmental, and geographic determinants of anemia as significant risk factors for childhood anemia  . Blood loss such as that associated with schistosomiasis, hookworm infestation, hemorrhage in childbirth, and trauma, can also result in both iron deficiency and anemia. Lastly, as with vitamin A deficiency, inhibition of the normal metabolism of iron can result in anemia . Despite the high prevalence and adverse health consequences reported internationally, there have been limited national representative findings on the prevalence and factors contributing to the development of anemia in SC, particularly in the study area. Anemia has been shown to contribute to mortality; a recent meta-analysis of nearly 12,000 children from six African countries aged 28 days to 12 years indicates that for each 1 g/dL increase in Hb, the risk of death falls by 24% . Therefore, the present study was carried out as the first study and aimed to determine the prevalence of Iron Deficiency Anemia and its associated risk factors among a sample of primary school students in Burao city, Somaliland. To identify the relationship between anemia and BMI of school-age children in primary schools in Burao city, Somaliland, 2020 and identify intestinal parasitic infections related.
2. Materials & Methods
A school-based cross-sectional study design was done in four primary schools in Burao city, Somaliland. About 285 school-age children in the age group between 6 - 14 years were selected with a respondent rate of 93.4%.
The sample size (305) was calculated using a single population proportion formula by considering a 23.6% prevalence of anemia among SC from study done in Filtu Town, Somali region, Southeast Ethiopia, 5% margin of error, 95% confidence interval, and 10% non-response rate .
Two public primary schools and two private primary schools were randomly selected and sampling was proportionally allocated to the selected schools and finally, systematic random sampling was employed to select study subjects using student registration book as a sampling frame. Only children that had informed consent from their parents/caregivers were included in the study.
Socio-demographic data was collected by using a questionnaire & interview of respondents. Complete Blood Counting (CBC) was used to determine the hemoglobin status of the children. Students (senior lab students) collected the blood and brought it to the University of Burao laboratory to analysis them where CBC machine is available. Anemia was defined as Hb < 11.5 g/dl for SC aged 6 - 11 years, and Hb < 12 g/dl for children aged 12 - 14 years. These verities of anemia were categorized as mild (Hb between 10 and 11.4 g/dl for 6 to11years, and between 10 and 11.9 g/dl for 12 to 14 years), moderate (Hb between 7 and 9.9 g/dl), and severe (Hb < 7 g/dl) for 6 to 14 years of age SC based on the adjusted Hb concentration recommended by the WHO scheme . Stool examination was also done for each participant in the present study, fresh stool sample was collected following the standard operating procedures (SOPs) in clean and labeled leak-proof stool cups. The stool specimen was transported in screw-capped cups in 10% formalin to the laboratory. Intestinal helminthe was detected microscopically by direct saline wet mount preparation and formalin-ether concentration method within 2 - 8 hours after collection at the University of Burao, Biomedical and Laboratory Sciences Laboratory. Data was entered and analyzed using SPSS statistical software for Windows version 21. Anthropometric data was analyzed using ANTHROP Plus.
Bivariate logistic regression and multivariable logistic regression were used to identify independent predictors of anemia in school adolescent girls. Statistical significance was set at p < 0.05.
Hemoglobin level of the school-age children was tested and overall prevalence of anemia is 23.1% (CI: 18.1%, 28.1%) with the mean and standard deviation of 12.7 ± 1.59). Out of the anemic children, 20.4% were mild and 2.3% and 0.4% were moderate and severe, respectively. While, approximately (77%) were normal children (Figure 1).
Socio-demographic characteristics of the respondents
About 285 of children aged between 6 and 14 years participated in this study with 93.4% of response rate, these children were obtained from four primary schools (two public and two private schools). According to the age of the children, 187 (65.8%) of them were the age group between 6 - 11 years and 97 (34.2%) were the age group between 12 - 14 years (mean ± SD = 10.6 ± 1.95). majority of the participants 180 (63.2%) were females and 105 (36.8%) were males.
About 188 (66.4%) of the children were studying in grades between 1 up to 4 and 95 (33.6%) were studying between 5 - 8 classes. Majority of the households, 234 (83%) consist of more than six people and only 48 (17.0%) consist of family members less than or equal to six (Table 1).
Figure 1. Showing the percentage of prevalence of anemia based on the hemoglobin status of school-age children among public schools in Burao, Somaliland, 2020 (n = 285).
Table 1. Distribution of socio-demographic characteristics of school-age children in public schools in Burao, Somaliland, 2020 (n = 285).
About 38 (13.6%) of educational status of children’s fathers were illiterate and 101 (36.1%) can read and write only, where 34 (12.1%), 43 (15.4%), and 50 (17.9%) had the educational status of primary level, secondary level and college and above level, respectively.
According to educational status of children’s mothers, about 88 (31.9%) were illiterate and 77 (22.9%) can only read and write while only 9 (3.3%) reached college and above (Table 1).
Majority of children’s mothers, 200 (72.5%), were housewife and about 41 (14.7%) of children’s fathers were unemployed and 54 (19.4%), 74 (26.5%) and 41 (14.7%) were government employees, private/company employee and daily laborer, respectively.
Majority of the respondent, 97 (34.0%) were from SH. Ibrahim School and 86 (30.2%), 49 (17.2%) and 53 (18.6%) of the children were from Al-Mustaqbal, 21-November and Candlelight schools, respectively. About 273 (96.1%) of the children’s both parents were alive where the rest, 11 (3.9%), lost at least one of the parents (Table 1).
To determine the associated socio-demographics factors of anemia, bivariate logistic regression was done and based on that analysis, the year of studying (grade) and education of children’s mothers were associated with anemia with the P value less than 0.25. Children in class year (grade) between 1 - 4 were more likely to be anemic (COR = 2.12; 95% CI: 1.09, 4.12) and children from illiterate mothers were more likely to be anemic (COR = 3.30; 95% CI: 1.80, 6.05) (Table 2). Using mosquito nets and current stool examination were also associated with anemia with P-value less than 0.25. Children who used mosquito nets were associated with anemia (COR = 1.51; P-value 0.167; 95% CI: 0.84, 2.71). Children who had parasites in their stool were more likely to be anemic (COR = 4.22; 95% CI: 1.08, 16.38) (Table 2).
Using mosquito nets and current stool examination were also associated with anemia with P-value less than 0.25. Children who didn’t use mosquito nets were associated with malaria infection and subsequently with anemia disease (COR = 0.167; 95% CI: 0.84, 2.71). Children who had parasites in their stool were more likely to be anemic (COR = 4.22; 95% CI: 1.08, 16.38) (Table 3).
Table 2. Distribution of bivariate logistic regression about socio-demographic factors of school-age children with and without anemia in public schools in Burao, Somaliland, 2020 (n = 285).
NOTE: *reminds the significance of the variable (P-value < 0.25).
Table 3. Distribution of bivariate logistic regression about history of parasites, prevention of malaria, and source of water of school-age children with and without anemia in public schools in Burao city, Somaliland, 2020 (n = 285).
NOTE: *reminds the significance of the variable (P-value < 0.25).
BMI for age Z score, average use of organ meat, and average use of flesh meat were associated with anemia using bivariate logistic regression P-value less than 0.25. Children with low MBI for age (wasting) were associated with anemia (COR = 0.58; 95%: 0.26, 1.28) and children that consume organ meat more than once a week were at high risk of anemia (COR = 1.87; 95% CI: 1.04, 3.37). Children who consume organ meat less than once a week were at high risk of anemia (COR = 1.87; 95% CI: 1.04, 3.37), similarly, children who consume flesh meat less than once a week were also at high risk of anemia (COR = 2.03; 95% CI: (1.10, 3.76) (Table 4).
Seven independent variables were significant on bivariate binary logistic regression with a p-value of <0.25 and all were entered into the multivariate logistic regression model to identify independently associated factors with anemia after controlling confounding factors with p-value < 0.05. Accordingly, education of children’s mother, average use of organ, meat, and stool examination were identified as statistically independent associated factors of anemia. Children from illiterate mothers were 2.37 times more likely to be anemic than children whose mothers were literate (AOR = 2.37; 95% CI: 1.14, 4.94). Children who consume organ meat less than once a week are 2.16 more likely to be anemic compared to those who consume organ meat at least once or more in a week (AOR = 2.19; 95% CI: 1.05, 4.43). Children who had parasites in their stool were 5.21 times more risk to be anemic (AOR = 5.21; 95% CI: 1.10, 24.62) (Table 5).
Table 4. Distribution of bivariate logistic regression about nutrition-related factors of school-age children with and without anemia in public schools in Burao city, Somaliland, 2020 (n = 285).
NOTE: *reminds the significance of the variable (P-value < 0.25).
Table 5. Multivariable logistic regression analysis showing factors associated with anemia among school-aged children in public schools in Burao, Somaliland, 2020 (n = 285).
NOTE: *reminds the significance of the variable (P-value < 0.05).
The main objective of this study was to assess the prevalence and factors associated with anemia among school-age children in primary schools in Burao. According to WHO cut point, anemia is considered as a public health problem when the prevalence is more than 5%. However, the magnitude of the problem is defined as mild, moderate, and severe when the prevalence is 5.0% - 19.9%, 20.0% - 39.9%, and ≥40%, respectively , respectively. Accordingly, 23.1% prevalence of anemia in SC means that the problem is a moderate public health problem in the study area. This indicated that a considerable number of children in the community were suffering from anemia. Anemia is negatively correlated with educational outcomes & levels in parents and schools children’s, leading to poor learning outcomes, such as loss of concentration in class, impaired academic achievement, and discontinuation of education in addition to other major contributing factors in the prevalence of anemia such as malnutrition, infected by parasites. So that emphasis should be given to reduce the prevalence of anemia in children.
The prevalence of anemia was similar and comparable to the study done in Filtu town, Somali region in Ethiopia which identified anemia as 23.6%. The reason for close similarity could be due to their living sitting and culture are very alike . Studies done in Cape Verde, China, and two studies from Saudi Arabia [Najran and Riyad] had prevalence of anemia of 23.8%, 24.9%, 22.5% and 22.3%, respectively    . These studies were in agreement with the current study. The current study had a higher prevalence of anemia among school-age children compared to studies done in Gonder town in Ethiopia with a prevalence of 15.5% , 16.2% in Morocco  and a study from Indonesia with a prevalence of 14% . The prevalence of anemia in this study was lower than those of studies done in other African countries, such as Kenya (28.8% - 35.3%) , Nigeria (82.6%) , Mali (58%) , Mozambique (54%) , Ghana (41%) , Tanzania (57%)  Sudan (88.3%)  and Egypt (59.3%) . It was also lower than the findings of studies conducted in Asian countries, like Gaza strip, Palestine (35.3%) , and western China 34% .
The discrepancy may be attributed to the differences in study settings the latter were carried out in rural areas and our study it was in city. In addition, the consumption of mothers & schools children iron-rich foods, for example, red meat, the iron-rich staple food particularly in cows and kamala’s meats in Somaliland might have contributed to the low prevalence of anemia in the our study area. In this study we found that children who consume red meat less than once a week are 2.16 more likely to be anemic compared to those who more consume red meat at least once or more in a week. Studies from Riyadh in Saudi Arabia and Turkey also have found that anemia was associated with eating meat  .
Maternal education was found to be significantly associated with anemia among school-age children. Children whose mothers were illiterate were 2.3 times more likely to be anemic compared to children from literate mothers. The findings of this study are similar to the study done in Gonder town in Ethiopia that identified anemia in school-age children to be significantly associated with lower maternal education .
Studies from in Kenitra, Northwest of Morocco, also identified a significant relationship between maternal education and school-age child anemia . Similarly, a study done in Northwest Ethiopia determined that children from illiterate mothers were more likely to be anemic . On the other hand, a similar study was done in Rural China’s Elementary Schools that revealed a strong association between paternal education and anemia in this age group .
Overall, we discussed that specially maternal educational status plays a major role in child health, nutrition, growth and development. Uneducated mothers may not understand the nutritional requirements of children easily and follow the recommended child feeding practices. In addition, parents lack of education negatively affects the socio-economic status of households which in turn limits food purchasing power. Hence, children’s access to heme iron sources, animal products, is limited.
In current study intestinal parasite in stool was significantly associated with anemia in school-age children where children who had parasites in their stool were 5.21 times more risk to be anemic. Similar result was found in the study done in Filtu town, Somali region in Ethiopia . Studies from Arba Minch in Ethiopia, rural Upper Egypt, and Nigeria identified that the parasite in stool was significantly associated with anemia in this age group   . We explained that might be due to nutritional competition, RBC destruction and parasite and feeding absorbed food of host, and loss of appetite caused by worms. These parasites also cause impaired nutrient uptake by a direct damage of the intestinal mucosal wall.
5. Limitations & Strengths of Study
One of the strengths of this study it was community-based and can provide information about both enrolled SAC. The study also tried to address multifactorial associated with anemia including investigation of the presence of intestinal parasitic infections. While, the first limitation of this study was we didn’t differentiate specific causes of anemia, such as TIBC, vit.B12, folate, RBC morphology and measure the level of ferritin was not identified. Second limitation unfortunately there is no local previous studies in same subject in Somaliland republic.
In this current study, Anemia was found to be a mild public health problem among SC. It was strongly associated with low maternal education levels, malnutrition, dieting habit, parasites infections & monthly income. Hence, focused policies and strategies of government towards school children should be designed to reduce anemia among low income & low education groups. Moreover, health education that enhances the knowledge of women about child feeding practices should be given regularly. On top of that, further studies using a larger sample size and including the assessment of all anemia diagnostics tests and subclinical infections are required to be conducted to identify the cause-effect relationships of anemia with its contributing factors.
The researchers in this study would like to express their appreciation and deep gratitude to the presidency of Burao University for their moral supporting, also all thanks to the Principles and teachers of schools who gave us all facilities and helped us in collecting samples and also were highly appreciate the laboratory technicians in Burao University who helped us in the diagnosed of clinical samples.
 Sachdev, H., Gera, T. and Nestel, P. (2005) Effect of Iron Supplementation on Mental and Motor Development in Children: A Systematic Review of Randomized Controlled Trials. Public Health Nutrition, 8, 117-132.
 Glazer, Y. and Bilenko, N. (2010) Effect of Iron Deficiency and Iron Deficiency Anemia in the First Two Years of Life on Cognitive and Mental Development during Childhood in Hebrew. Harefuah, 149, 309-314.
 Hurtado, E.K., Claussen, A.H. and Scott, K.G. (1999) Early Childhood Anemia and Mild or Moderate Mental Retardation. The American Journal of Clinical Nutrition, 69, 115-119. https://doi.org/10.1093/ajcn/69.1.115
 Ai, Y., Zhao, S.R., Zhou, G., et al. (2012) Hemoglobin Status Associated with Performance IQ but Not Verbal IQ in Chinese Preschool Children. Pediatrics International, 54, 669-675. https://doi.org/10.1111/j.1442-200X.2012.03648.x
 Greisen, G. (1986) Mild Anemia in African School Children: Effects on Running Performance and an Intervention Trial. Acta Paediatrica Scandinavica, 75, 662-667.
 Gutema, B., Adissu, W., Asress, Y. and Gedefaw, L. (2014) Anemia and Associated Factors among School-Age Children in Filtu Town, Somali Region, Southeast Ethiopia. BMC Hematology, 14, 13. https://doi.org/10.1186/2052-1839-14-13
 Semedo, M.R.L., Santos, M.M.A.S., Baião, M.R., Luiz, R.R. and da Veiga, G.V. (2014) Anemia and Associated Factors among School-Age Children in Cape Verde, West Africa. African Journal of Food, Agriculture, Nutrition and Development, 14, 9511-9528.
 Luo, R.F., Zhang, L.X., Liu, C.F., Zhao, Q.R., Shi, Y.J., Miller, G. and Yu, E. (2011) Anemia among Students of Rural China’s Elementary Schools: Prevalence and Correlates in Ningxia and Qinghai’s Poor Counties. Journal of Health, Population and Nutrition, 29, 471-485. https://doi.org/10.3329/jhpn.v29i5.8901
 Aedh, A., Elfaki, N. and Sounni, E. (2019) Iron Deficiency Anemia and Associated Risk Factors among Teenagers in Najran, Saudi Arabia. International Journal of Medical Research & Health Sciences, 8, 108-114.
 Gad, A., Al-Quaiz, J., Khoja, T. and As-Sharif, A. (2013) Anemia among Primary School Children (5-12 Years) in Riyadh Region, Saudi Arabia: A Community-Based Study. The Canadian Journal of Clinical Nutrition, 1, 27-34.
 Getaneh, Z., Enawgaw, B., Engidaye, G., Seyoum, M., Berhane, M., Abebe, Z., et al. (2017) Prevalence of Anemia and Associated Factors among School Children in Gondar Town Public Primary Schools, Northwest Ethiopia: A School-Based Cross-Sectional Study. PLoS ONE, 12, e0190151.
 Achouri, Y.A., Sbaibi, R., Ahami, A. and El Hioui, M. (2015) Prevalence of Iron Deficiency Anemia among School Children in Kenitra, Northwest of Morocco. Pakistan Journal of Biological Sciences, 18, 191-195.
 Andriastuti, M., Ilmana, G., Nawangwulan, S. and Kosasih, K. (2020) Prevalence of Anemia and Iron Profile among Children and Adolescents with Low Socio-Economic Status. International Journal of Pediatrics and Adolescent Medicine, 7, 88-92.
 Pullan, R.L., Gitonga, C., Mwandawiro, C., Snow, R.W. and Brooker, S.J. (2013) Estimating the Relative Contribution of Parasitic Infections and Nutrition for Anaemia among School-Aged Children in Kenya: A Subnational Geostatistical Analysis. British Medical Journal Open, 3, e001936.
 Onimawo, I., Ukegbu, P., Asumugha, V., Anyika, J., Okudu, H., Echendu, C., et al. (2010) Assessment of Anaemia and Iron Status of School Age Children (Aged 7 ± 12 Years) in Rural Communities of Abia State, Nigeria. African Journal of Food, Agriculture, Nutrition and Development, 10.
 Hall, A., Bobrow, E., Brooker, S., Jukes, M., Nokes, K., Lambo, J., et al. (2001) Anaemia in Schoolchildren in Eight Countries in Africa and Asia. Public Health Nutrition, 4, 749-756. https://doi.org/10.1079/PHN2000111
 Eltayeb, M.S.E., Elsaeed, A.E., Mohamedani, A.A. and Assayed, A.A. (2016) Prevalence of Anaemia among Quranic School (Khalawi) Students (Heiran) in Wad El Magboul Village, Rural Rufaa, Gezira State, Central Sudan: A Cross Sectional Study. The Pan African Medical Journal, 24.
 Salama, R.A. and Labib, M.R. (2016) The Prevalence of Anemia among Informal Primary School Children: A Community Based Study in Rural Upper Egypt. Epidemiology, Biostatistics and Public Health, 13, 165-176.
 Keskin, Y., Moschonis, G., Dimitriou, M., Sur, H., Kocaoglu, B., Hayran, O. and Manios, Y. (2005) Prevalence of Iron Deficiency among Schoolchildren of Different Socio-Economic Status in Urban Turkey. European Journal of Clinical Nutrition, 59, 64-71. https://doi.org/10.1038/sj.ejcn.1602035
 Tariku, E., Abebe, G., Melketsedik, Z., Gutema, B., Megersa, N. and Sorrie, M. (2019) Anemia and Its Associated Factors among School-Age Children Living in Different Climatic Zones of Arba Minch Zuria District, Southern Ethiopia. BMC Hematology, 19, 6. https://doi.org/10.1186/s12878-019-0137-4