Anaemia among school children of different socioeconomical status in a city of Southern Brazil

Abstract

Background: Iron deficiency is one of the leading causes of anaemia, with those most affected being children and women of childbearing age, in Brazil there is a scarcity of studies involving the local prevalence of anaemia. Aim: To evaluate anaemia and associated factors in schoolchildren in Santa Cruz do Sul through the analysis of biochemical and haematological markers and parasitological examination of faeces. Subjects and methods: School children from 10 to 12 years of age were evaluated through complete blood count, serum ferritin, C-reactive protein and stool parasitological examination, as well as socio-demographic characteristics and prophylaxis with ferrous sulphate in childhood. Results: It was found that 13.0% of the population was anaemic, girls were very slightly overrepresented among the anaemic children. Only 5.3% had altered haematocrit levels; 26.6% had low Mean Corpuscular Volume levels; 18.4% had low ferritin levels; 2.4% had increased C-reactive protein levels, and 21.7% had altered eosinophils. As for the socioeconomic level, classes A2 and D presented lower haemoglobin levels, as well as class D presenting lower ferritin levels, although without statistical significance. Only 6.0% of the population presented iron-deficiency anaemia and 46.0% of the schoolchildren had used ferrous sulphate supplementation in childhood. Conclusion: The prevalence of anaemia in the studied municipality is low, probably due to the high municipal human development index. Epidemiological studies are essential to characterise the population in a systematic form, to prevent future problems.

Keywords:

• Anaemia
• school children
• haematology
• socioeconomic status
• supplementation

Introduction

Anaemia, defined as a low concentration of haemoglobin in the blood, is considered a public health problem ([WHO] World Health Organization 2015), affecting about two billion people globally. It is the most common nutritional problem, with a major impact on human health and on social and economic development, occurring more than 89% in developing countries (WHO 2011; Kassebaum 2016).

Iron deficiency is one of the leading causes of anaemia, with those most affected being children and women of childbearing age (Disease, Injury Incidence, & Prevalence Collaborators 2016). In Brazil there is a scarcity of studies involving the local prevalence of anaemia, however, available data show that 33% of Brazilian children aged zero to 83.9 months have anaemia, suggesting a serious public health problem (Nogueira-de-Almeida et al. 2021). A systematic review and meta-analysis revealed that iron deficiency anaemia in Brazilian children under 5 years of age was approximately 40%, remaining beyond acceptable levels for this population group (Silveira et al. 2021). Other authors revealed an average prevalence of iron deficiency anaemia in pre-school children (under 5 years old) in Brazil between the years 2008 to 2018 of 31.9% (Corbucci et al. 2019). In Brazilian women of reproductive age (10 to 49 years) the prevalence of iron deficiency anaemia was 25%, and therefore a public health problem in Brazil, especially in the North and Northeast regions (Macena et al. 2022).

Nutritional deficiencies (folate, vitamin B12, folic acid, riboflavin, iron), poor vitamin absorption, blood loss, chronic infections, and intestinal parasitic infections are contributing factors to the disease (Shaw and Friedman 2011; Camaschella 2019). Diets from cereal or legume-based meals (usually, rich in phytates) or beverages containing iron-binding polyphenols, as well as reduced consumption of meat, fish, and poultry, are risk factors (Mantadakis et al. 2020).

Haem iron with high bioavailability (up to 25%) is derived from haemoglobin and myoglobin found in diets rich in meat. Plants and dairy foods contain nonheme iron. The adequate intake of vitamin C is also important to prevent anaemia, but in low-income populations these foods are limited and scarce due to socioeconomic status. In these circumstances, fortification of foods with iron may be a favourable alternative due to its low cost and may consequently reduce the prevalence of iron deficiency and anaemia (Mantadakis et al. 2020).

Intestinal parasitosis is also associated with anaemia in children and adolescents up to 14 years of age. In Brazil the average prevalence of anaemia associated with parasitoses was about 11.4% in the South Region, 13.1% in the Northeast Region, and 3.5% in the Midwest Region; in the North Region, no statistical association was made between the presence of anaemia and parasitoses (Moraes et al. 2019).

During childhood, anaemia has been associated with growth retardation, high risk of infections, and poor cognitive and motor development, which can lead to low productivity at work years later (Best et al. 2010; WHO 2017). Once the underlying cause is diagnosed, appropriate treatment should be performed to prevent worsening and unpleasant consequences on the patient’s quality of life (Amicis et al. 2021).

In Brazil, the supplementation of iron and folic acid in flour is mandatory, but the direct administration of iron to children is only recommended by the National Iron Supplementation Program. Despite the Brazilian government’s efforts to combat iron deficiency anaemia, the problem still persists, due to a large number of social inequalities in the different regions of the country (Nogueira-de-Almeida et al. 2021).

Due to the indisputable epidemiological importance, especially in schoolchildren, the objective of the study was to determine the prevalence of anaemia through haematological and biochemical markers and correlate them with socioeconomic status.

Subjects and methods

Materials and Subjects

This study has a quantitative and prevalence approach, cross-sectional design, and a descriptive and analytical character. It is a cut-out of an Umbrella Project, called “School children’s Health - Phase III”, approved under the opinion of the Research Ethics Committee (REC) of the University of Santa Cruz do Sul (UNISC) with number 714.216. This clipping was approved with opinion number 607.665.

Santa Cruz do Sul has an estimated population for 2021 of 132,271 people, and a demographic density of 161.40 hab/km² according to IBGE/2010 estimates. The large municipality is in the central region of Rio Grande of Sul. The municipality’s Municipal Human Development Index for education, longevity, and income is 0.74, 0.85, and 0.75, respectively ([IBGE] Instituto Brasileiro de Geografia e Estatística 2010).

Basic education can be accessed in four private and sixty-six public institutions (state and municipal networks), with about 5,432 students enrolled. The schooling rate from 6 to 14 years old is 98.3%, based on the last census. Table 1, prepared based on information from the 2012 School Census, shows the numbers of students, according to the network in which they are enrolled (IBGE 2010).

Table 1. Students enrolled in the final years of elementary school in the state and municipal networks, urban and rural part-time in the city of Santa Cruz do Sul/RS.

School Location
Urban State	3.036
State Rural	51
Municipal Urban	1.742
Municipal Rural	603
Total	5.432

Source: IBGE, 2012

The study sample was composed of 207 subjects aged between ten and twelve years, enrolled in six schools (four municipal, one state, and one private) in the urban area of Santa Cruz of Sul. The sample distribution among the schools was proportionally based on the number of students in the age group in each school, respecting the gender proportion. The selection of these students was made by simple random drawing from the existing database.

The blood collection occurred between June and August 2014. Blood collection for the evaluation of haematological markers, biochemistry, and iron stores was by a trained professional on a prescheduled day. Four mL of blood were collected from each child and stored in properly identified vials.

The evaluation of anaemia was carried out by means of the complete blood count (CBC) and the body’s iron stock was evaluated by the serum ferritin test. The C-reactive protein (CRP), an inflammatory marker whose iron storage results could be masked if the individual had infections, was used. A parasitological stool examination (PSE) was also performed to check for possible parasitic infections, since it is a contributing factor to high prevalence of anaemia. The CBC was performed in the Exercise Biochemistry Laboratory, using a Sysmex XS-800i analyser, as well as the PSE (macroscopic and microscopic methods). Serum ferritin was measured by the chemiluminescence method, following the manufacturer’s instructions (Architect System), and PCR was evaluated by the quantitative method, using automatic equipment from Biossistems, model A15, both were performed in a private Clinical Analysis Laboratory.

The socioeconomic level was determined by means of a form standardised by the Brazilian Association of Research Companies that performs the Brazil Economic Classification. We described the family income according to social class, where class A1 are the families that have a combined income of everyone in the house of R$ 14,366; class A2: R$ 8,099; class B1: R$ 4,558; and so on, as described in Table 2.

Table 2. Family Income by Social Class.

Class	Points	Average Family Income (Gross Value in R$)
A1	42 to 46	14,366
A2	35 to 41	8,099
B1	29 to 34	4,558
B2	23 to 28	2,327
C1	18 to 22	1,391
C2	14 to 17	933
D	8 to 13	618
E	0 to 7	403

Source: [ABEP] Associação Brasileira de Empresas de Pesquisa 2008

The age range was chosen because there are few studies in this age group and because the supplementation with ferrous sulphate, in Brazil, was implemented in 2005, when these students were small and would be eligible to join the program. Based on these data it can be ascertained whether supplementation has a positive influence on the prevention of anaemia or not.

The analysis of prophylactic treatment with ferrous sulphate supplementation during childhood by means of the qualitative nominal variable - “yes” or “no” and by means of the quantitative discrete variable - time (days or years) was also performed in order to verify if the Brazilian public policy was effective or not.

All students who were within the age range and who agreed to participate in the research by signing the Free and Informed Consent Term and whose parents agreed by signing the Free and Informed Consent Term were included.

The prevalence of anaemia is classified in relation to its importance as a public health problem, considering the estimated prevalence at the levels: severe (≥40.0%); moderate (20.0 − 39.9%); mild (5.0 − 19.9%); and normal (≤ 3.9%). Individuals with normal reference values should have haemoglobin levels >12 g/dL, haematocrit >34%, Mean Corpuscular Volume (MCV) >80fL, ferritin 30-120ng/mL, CRP ˂1mg/L, eosinophils ˂0.5 × 10³ cells/μL and red blood cell distribution (RDW) range <14% (WHO 2001).

Statistical analysis

Statistical analyses were performed with the Statistical Package for Social Sciences (SPSS) software, version 23.0, and graphs were constructed with GraphPad Prism software, version 4.0. For non-normally distributed data in the analysis of continuous variables, the Kruskal-Wallis and Mann-Whitney tests were employed. The significance level was p < 0.05.

A sample size of 196 subjects was calculated to estimate the proportion of occurrence of the outcome anaemia with a 10% range for the confidence interval (with the addition of 10% for possible losses and refusals this number should be 218). The calculation (using Wald’s method) considered a 95% confidence level and a 15% expected percentage for anaemia (referred to by Klinger et al. 2013 and González Quiroz et al. 2020). This calculation was performed using the online version of the PSS Health tool (Borges et al. 2020).

Results

In the study population, consisting of 207 schoolchildren, it was observed that 117 of the individuals (56.5%) studied were female and the mean age was 11.2 ± 0.9 years. As for the socioeconomic level, there was a prevalence of B2 class with 75 students (36.2%) (Table 3).

Table 3. Sociodemographic characteristics of the schoolchildren participating in the study.

	Mean ± SD	N
Age (years)	11.2 ± 0.9	207
Sex	%	N
Male	43.5	90
Female	56.5	117
Social class	%	N
A1	0.0	0
A2	3.4	7
B1	9.7	20
B2	36.2	75
C1	28.0	58
C2	18.4	38
D	4.3	9
E	0.0	0

The study showed the prevalence of anaemia in 13.0% (27 schoolchildren) of the sample, girls were very slightly overrepresented among the anaemic children (59.3%), considering only the haemoglobin levels. The prevalence of anaemia between ages was 37.0% (10 years old), 26.0% (11 years old) and 37.0% (12 years old). There were also altered values of serum ferritin (18.4%), haematocrit (5.3%), MCV (26.6%), CRP (2.4%), RDW (3.9%), and eosinophils (21.7%) which indicate possible parasitic infections or even possible allergic states (Table 4). Of these individuals, 3.4% had undergone PSE, showing negative results in all.

Table 4. Hematological characteristics of the schoolchildren.

		Normal Reference	School children with results below the reference values
	Mean ± SD	Value	(%)	N
Haemoglobin (g/dL)*	12.8 ± 0.8	> 12	13.0	27
Haematocrit (%)*	37.9 ± 2.1	> 34	5.3	11
Corpuscular Volume Mean (fL)*	82.4 ± 3.7	> 80	26.6	55
Ferritin (ng/nL)**	63.9 ± 35.1	30-120	18.4	38
C-Reactive Protein (mg/L)**	0.2 ± 0.2	< 1	2.4	5
Eosinophils (X10^3 cel/µL)*	0.4 ± 0.9	< 0.5	21.7	45
RDW (%)	37.2 ± 2.0	< 14	3.9	8

The mean haematological variables were also compared between the groups with low ferritin level (˂30 ng/mL), normal level (30–120 ng-mL) and high ferritin level (≥120 ng/mL), demonstrating that the haemoglobin, erythrocyte and haematocrit levels were significantly different between the groups, progressively increasing towards the group with ferritin >120 ng/mL. The study showed that 6.8% of the sample had ferritin ˂30 ng/mL and VCM ˂80 fL, indicating the possibility of iron-deficiency anaemia.

Figure 1 shows the relationship between social class and haemoglobin (A), ferritin (B), MCV (C), and eosinophil (D) levels. The haemoglobin level was low in social class A2, followed by class D. The ferritin level was low in social class D, however, without statistical significance. It was found that social class D presented significantly lower MCV levels compared to classes A2 and B1. Social classes B1 and B2 presented significantly higher levels of eosinophils than class D.

Figure 1. Association between social class and haemoglobin (A), ferritin (B), Corpuscular Volume Mean (C), and eosinophil (D) levels. p = significance level according to Kruskal-Wallis test. Mean plus or minus standard error of the mean.

Figure 2 shows haemoglobin levels compared with ferritin levels - low ferritin levels (˂30 ng/mL), normal ferritin levels (30–120 ng/mL), and high ferritin levels (≥ 120 ng/mL). It was revealed that the prevalence of anaemia was 44.7%, 6.4%, and 0.0%, respectively, among individuals with 120 ng/mL ferritin.

Figure 2. Association between haemoglobin levels according to ferritin levels P = significance level according to Kruskal-Wallis test.

Figure 3 shows the association between haemoglobin levels and eosinophil levels, revealing that individuals with altered eosinophil levels (≥0.5 × 10³ cells/μL) tend to have higher haemoglobin levels, however, without statistical significance.

Figure 3. Association between haemoglobin levels and eosinophil levels. p = level of significance according to Mann-Whitney U test.

73.6% of parents or guardians answered whether their children had received ferrous sulphate supplementation (prophylactic treatment) at some point during childhood and, of these, 46.0% had used supplementation. Only 24.5% answered the duration of supplementation, which was, on average, 60 months.

Discussion

In this representative study of the population of schoolchildren aged between ten and 12 years, the prevalence of anaemia of 13.0% was verified, considered by WHO (2021) as a mild public health problem. However, anaemia is one of the biggest public health problems in Brazil. Data in regions close to our study, such as in the metropolitan region of Curitiba, reported 2.2% of anaemia (Spezia et al. 2018), in educational units on the outskirts of Londrina, 41.3% was reported (Miglioranza et al. 2002), in an emergency care unit in the city of Santa Maria it was 29.2% (Garcia et al. 2016) and in the city of Santa Cruz do Sul (Brazil) it was 14.3% (Klinger et al. 2013). In more distant Brazilian regions, such as in public schools in Maceio, anaemia was observed in 9.9% (Santos et al. 2002), and 24.5% of students enrolled in the public school system in Salvador had anaemia (Borges et al. 2009). The comparison with other studies considered only the prevalence and gravity of anaemia, without considering the social-economic status of the locality of where the study was performed. However, it is known that differences persist in Brazil, conditioned by high social inequality and income distribution between the layers of society.

Girls were very slightly overrepresented among the anaemic children (59.3%), in the studies by Chalise et al. (2018); El-Shafie et al. (2020), and Shaban et al. (2020) prevalence was observed among girls and in the studies by Vázquez et al. (2019) and Kothari et al. (2019) in boys.

The anaemia showed rates among the children of 10 years old, 11 years old and 12 years old, which may be explained by the occurrence of the growth spurt at this stage (Fujimori et al. 1996). A study conducted by El-Shafie et al. (2020) revealed that children aged <9 years had higher prevalence of anaemia. In contrast, Shaban et al. (2020) evidenced that older children (≥13 years old) were more prone to anaemia.

It is noteworthy that, for the development of anaemia, several factors must be considered, especially when it comes to the sex of the individual, since it is in adolescence (between ten and 19 years) that the period of human development occurs and puberty sees accelerated somatic growth, the occurrence of peak growth stature (growth spurt), biological maturation (bone and sexual) (Frutuoso et al. 2003), menarche and the consequent loss of blood (Frutuoso et al. 2003; WHO, 2017).

Annual geospatial estimates from 2000 to 2018 of anaemia prevalence in women of reproductive age (15 to 49 years) in 82 low- and middle-income countries demonstrate widespread moderate improvements in overall anaemia prevalence. In 2018, anaemia prevalence was highest in West African, Middle Eastern, and South Asian countries, including Gambia, Senegal, Mali, Yemen, and India (Kinyoki et al. 2021).

High prevalences of anaemia are directly related to the socioeconomic level of the population, food availability, access to health services, housing quality (Frutuoso et al. 2003), having no drinking water or access to water outside the home, and little access to sanitation facilities (Kothari et al. 2019). In this study, the low haemoglobin level was observed in social class A2, which may be due to unhealthy eating habits, followed by class D, which may be related to lack of food, as well as the water supply and little access to sanitary facilities, since the percentage of people registered in the single register in the municipality without adequate water supply, sanitary sewage and garbage collection are, respectively, 8.52%, 7.58% and 2.91% (AtlasBr, 2022). Furthermore, it is important to highlight that we have a small number of families belonging to class A2 (3.4%) and this fact can influence our results.

A marginally significant association of haemoglobin with eosinophil alteration was also shown, similar to other studies, which observed a prevalence of anaemia in populations with lower socioeconomic strata, with little access to food and/or presence of parasitic infections (Mengistu et al. 2019; Tariku et al. 2019; El-Shafie et al. 2020; González Quiroz et al. 2020). In our study, no parasites were identified, in contrast to information in the literature.

The study also exposed that 6.8% of the students presented iron-deficiency anaemia, corroborating other studies (Perng et al. 2013; Silva and Costa 2014; Shaban et al. 2020).

Prophylactic treatment is a strategy to mitigate anaemia, since supplementation has the advantage of producing rapid changes in nutritional status, besides being able to target more vulnerable groups (Azeredo et al. 2010). A study by Kothari et al. (2019) revealed that children who did not receive iron supplements had a higher prevalence of anaemia, suggesting that supplementation presumably has a protective effect.

A systematic review and meta-analysis confirmed that the prophylactic use of iron is a protective factor against anaemia. The iron supplementation reduced the chance of children presenting this nutritional deficit by 0.86 (95% CI: 0.76 − 0.98) (Paixão et al. 2022). However, despite being a protective factor, there is still low adherence to supplementation, around 20% to 40%, in Viçosa (MG) and Vitória da Conquista (BA), respectively. This fact may be linked to the inadequate distribution of this medication in the cities, the lack of prescription by health professionals, or even inefficient administration by caregivers (Magalhães et al. 2018).

It should also be considered that Santa Cruz do Sul is a city of Germanic culture and the cuisine of the region has a large amount of breads and cakes, which have a large contribution of iron via flour. In addition, the same population has a large intake of animal protein (Prá et al. 2011). Moreover, in 2010, the Human Development Index (HDI) of Santa Cruz do Sul was 0.773, which places this municipality in the High Human Development range (HDI between 0.700 and 0.799). The dimension that most contributes to the municipality’s HDI is longevity, with an index of 0.852, followed by income, with an index of 0.782, and education, with an index of 0.693. It is suggested that income and education are protective factors against anaemia.

In this study, no families from social class E and few families from social class D were observed, indicating a high socioeconomic level. The dietary pattern of the population and the socioeconomic level, despite a not so high coverage of supplementation, seem to contribute to the low prevalence of malnutrition and anaemia, explaining the results found in this study. A study conducted with female adolescents with a high prevalence of anaemia showed that most parents were farmers and housewives, and with regard to education, most could not read and write (Mengistu et al. 2019). Similarly, the study by Kothari et al. (2019) revealed a strong relationship between anaemia prevalence in children whose maternal education was low - no formal education and families living in rural areas.

Life habits are directly related to the socioeconomic level of families, as they allow the acquisition of different forms of food, and families with better financial conditions tend to buy more industrialised products, when compared to children whose family receives government assistance and study in public schools where meals follow the National School Feeding Program (PNAE) (Silva et al. 2019). Due to the increased consumption of industrialised foods, there is a reduction in the purchase of foods such as vegetables and fruits and an increase in stuffed biscuits and industrialised juices. Libanio et al. (2019) show that the prevalence of consumption of industrialised foods is much higher in the southern region of Brazil when compared to the rest of the country, especially in children aged 5 to 9 years.

Iron needs during the first years of life are very high since iron is an essential micronutrient for life and acts mainly in the synthesis of red blood cells (RBCs) and in the transport of oxygen in the body, therefore, in order to provide additional iron preventatively, strategies have been created for the prevention and control of anaemia, through medication supplementation with iron salts (Brasil 2013).

Limitation

A limitation of the study is the lack of iron dosage and transferrin saturation, parameters that would allow greater knowledge about the amount of iron present in the body. In addition, there are many controversies in the literature regarding reference values for haemoglobin and ferritin in children - there is no standard reference value. Thus, anaemia as well as iron-deficiency anaemia may be considered overestimated in this study because we used haemoglobin ˂12 g/dL and ferritin ˂ 30 ng/mL.

Conclusion

The prevalence of anaemia in schoolchildren was 13.0% and girls were very slightly overrepresented among the anaemic children, featuring a mild public health problem. Some haematological parameters were altered, and it was possible to relate these to the socioeconomic level. The lower haemoglobin levels were found in social classes A2 and D and low ferritin levels in class D. The low prevalence of anaemia was possibly related to HDI, mainly the income and education.

Anaemia is a public health problem and specific policies are needed to reduce the problems related to development of this disease. In Brazil there is a scarcity of studies involving the prevalence of local anaemia in this population, and they are rarely published in scientific journals. Epidemiological studies are essential to characterise the population in a systematic form, especially in schoolchildren, to prevent future problems. More comprehensive studies on the prevalence of anaemia in children, at school age, should be conducted since the mapping and diagnosis of the reality allow us to propose strategies for reducing the problem.

Authors’ contributions

All authors contributed to the analyses and interpretation of data or drafting of the manuscript, as well as critical analysis to the intellectual content. They agree to be responsible for all aspects of the work, and have read and approved the final manuscript.

Aknowledgements

Thanks to all the research participants and all the individuals involved in the production and curation of this data. Special thanks to Professor Dr. Miria Suzana Burgos (in memoriam), for all her dedication, research collaboration, enthusiasm, and fight for the health of schoolchildren.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

The author(s) reported there is no funding associated with the work featured in this article.