Prevalence and risk factors of anaemia in paediatric patients in South-east Nigeria.
Studies have shown that malaria, [10-12] HIV, [13, 14] iron deficiency, [15,16] glucose-6 phosphate dehydrogenase (G6PD) deficiency, sickle cell anaemia (SCA) [10,11] and intestinal helminths  are potential causes of anaemia. Over the years in Nigeria, different intervention programmes have been adopted based on common causes of anaemia, with the aim of preventing and controlling childhood anaemia. [18,19] In spite of these interventions, the prevalence of anaemia remains high. Therefore, there may be some benefits if the main contributors to anaemia among ill children are determined. In addition, evaluation at the micro or small-unit level rather than national or global level will help in the design of a cost-effective intervention that can reduce anaemia-related morbidity and mortality in that locality.
Anaemia among ill children, especially those <5 years old, is associated with higher morbidity and mortality than in apparently healthy children. Our objective was to determine the prevalence of anaemia and causative factors among <5-year-old paediatric patients in South-East Nigeria. The outcome of this study will facilitate the design of an effective management protocol for anaemic children <5 years of age who present to health facilities in South-East Nigeria.
Study site and population
This study was conducted in the children's outpatient clinic (CHOP) and children's emergency room (CHER) of the University of Nigeria Teaching Hospital (UNTH) in Enugu, Nigeria. UNTH is a three-tier health facility that receives patients from both urban and rural areas. It is strategically located in the semitropical rainforest of Nigeria with an estimated annual rainfall of more than 1 520 mm and a temperature that varies between 22.4[degrees] and 30.8[degrees]C.  The malaria transmission rate is high all year round, with an average rate of more than 15% in both wet and dry seasons.
The study was a cross-sectional, hospital-based, descriptive study. All children aged between 6 and 59 months who visited the CHOP or CHER were consecutively recruited over a period of 12 months between February 2009 and January 2010. The sample size was calculated at 283 patients with Epi-Info software version 6.04 (Centers for Disease Control and Prevention (CDC), USA), using the prevalence of anaemia among children aged 6-59 months of 21.7%,  with a 95% confidence limit.
The UNTH ethical committee gave ethical approval before the study was commenced. Written informed consent was obtained from the parents/caregivers of participating children. The results of the investigations were acted upon according to local protocol; children with anaemia diagnosed by immediate haemoglobin estimation were referred to appropriate units, where they were reviewed, investigated and managed with haematinics and/or blood transfusion as appropriate.
A clinical research form (CRF), including a questionnaire, was administered by face-to-face interview with the respondents. The CRF was pilot-tested in a health centre in Enugu, after which certain revisions were made prior to the study. The information collected was on socioeconomic data, physical examination and anthropometric measurements. Blood and stool samples were also collected.
Socioeconomic status (SES) was determined according to parental educational level, and occupation according to Oyedeji. Social classes I and II were categorised as higher social classes, and III-V as lower classes.
Weight was measured using a Seca floor scale (Seca Corporation, USA) for children [less than or equal to] 24 months, and a Harson weighing scale (Harson Scales Company, USA) for children >24 months old. Recumbent length was measured using a SECA 416 measuring board for children <2 years old, while height was measured using a stadiometer for those aged [greater than or equal to] 2 years. Each measurement was repeated to get the mean. Those children whose weight-for-age, height-for-age, and weight-for-height were below the 3rd centile of the World Health Organization (WHO) Child Growth Standard Chart were classified as underweight, stunted and wasted, respectively, while those above the 3rd centile but less than the 97th centile were classified as having normal nutrition. Children above the 97th centile for weight-for-height were classified as overweight/obese.
Haemoglobin concentration was determined using the Hemocue method (HemoCue HB 301).  The WHO and CDC proposed cut-off for anaemia in children aged 6 months - 5 years was used to categorise the children. Children with haemoglobin (Hb) [less than or equal to] 10 g/dL were classified as anaemic.
Blood smears for thick blood film were stained with Giemsa stain for malaria parasitaemia. The slides were viewed for the presence or absence of asexual Plasmodium falciparum parasites by a trained microscopist.
Total iron-binding capacity and serum iron were determined by standard direct total iron-binding capacity (TIBC) assay  and the ferrozine colorimetric method, respectively.  A serum iron level of <9 [micro]mol/L and total iron-binding capacity of >80 [micro]mol/L were taken as cut-off points for iron deficiency.
The patients' HIV status was determined using the Determine HIV 1/2 (Abbott Diagnostic Division, The Netherlands) rapid kits. G6PD status was determined using the standard methaemoglobin reduction test.  Haemoglobin genotype was determined by electrophoresis of the patient's blood on cellulose acetate membrane at the alkaline pH of 8.9. 
The stool sample was examined for parasite ova using the Kato-Katz method. Presence or absence of hookworm ova was defined as infection or non-infection, respectively.
Data were double-entered and verified in Epi-Info version 6.04 and analysed using SPSS version 15.0 statistical software (IBM, USA). The children were categorised into anaemic (Hb [less than or equal to] 10g/dL) and non-anaemic groups. Means and standard deviations were used to summarise quantitative variables (age of children) and proportions of categorical variables were analysed using the [chi square] test and Yates correction (where necessary). The prevalence of each variable was determined for each group (anaemic and non-anaemic). The p-value (p < 0.05) was used to determine statistically significant associations.
Socioeconomic and demographic characteristics of the subjects
Most (92.8%) of the respondents (caregivers) were mothers, and most (69.5%) of these had tertiary education. The presence of anaemia correlated inversely with educational level of the parents/caregivers (p = 0.04). The predominant occupation of the caregivers was civil service (33.7%), followed by being unemployed (24.6%). There was a significant association between occupation of the caregivers and anaemia. One-third of caregivers (35.4%) was classified as being of low SES. There was no significant association between SES and anaemia.
Of the 652 children who participated, 581 children had complete questionnaires with investigation results, and these comprised the analysed sample. Male children were in a slight majority (54.9%). The overall prevalence rate of anaemia was 49.2%.
The prevalence of anaemia among children between the ages of 13 and 36 months was high (51%), and this was statistically significant (Table 1).
Malaria was present in 138 anaemic children (48.3%) and 118 nonanaemic children (40.0%) (relative risk (RR) = 1.20, p = 0.03) (Table 2). Low serum iron was detected in 121 anaemic children (42.3%) and 57 non-anaemic children (19.3%) (RR = 1.66, p = 0.01), while a high TIBC was found in 33.9% of anaemic children compared with 13.9% of controls (RR = 1.65, p = 0.01). G6PD deficiency was detected in 71 anaemic children (24.8%) and 49 non-anaemic children (16.6%) (RR=1.26, p = 0.02).
HIV seropositivity was detected more frequently in anaemic children (13.3%) than non-anaemic children (7.1%) (RR = 1.33, p = 0.02).
Haemoglobin genotype SS was not found more frequently in anaemic children (n = 7, 2.4%) than non-anaemic children (n = 3, 1.0%) (RR = 1.44, p = 0.34).
Hookworm ova were detected in three anaemic children (1.0%) and one non-anaemic child (0.3%) (RR = 1.51, p = 0.32).
Table 3 shows that 45 anaemic children (15.7%) and 48 nonanaemic children (16.3%) were stunted, (RR = 0.98, p = 0.82). No association was found between wasting and anaemia (RR = 0.76, p = 0.10) or between underweight and anaemia (RR = 0.88, p=0.51).
Twenty anaemic children (7.0%) and 10 non-anaemic children (3.4%) had a mid-upper arm circumference (MUAC) [less than or equal to] 12.5 cm. No significant association was found between low MUAC and anaemia (RR = 1.38, p = 0.07)
In this study, the anaemia prevalence among paediatric patients <5 years of age was high, especially among children 13-36 months old. This is similar to what has been reported in other studies, [17, 27] and has been suggested to be a result of: malaria infection with poor immunity to malaria in this age group; nutritional anaemia due to poor complementary feeding practices; [7, 28] increase in body demand due to rapid growth; and increased activity due to achieved motor milestones. Anaemia was not associated with gender or SES. Different studies have reported contrasting views on the association between anaemia and gender, [27, 29] as well as SES. [30,31] The reasons for these differences are not clear. The fact that this study was hospital based might have contributed to the observed differences. Most ill children from all socioeconomic groups might have sought care from different sources by the time they seek healthcare from the hospital. This delay in access of healthcare allows the underlying illness enough time to cause anaemia as a complication.
Malaria was significantly higher among anaemic paediatric patients, a finding reported by other studies [12-14] but which is in contrast to expectation, as the region has seen an overall reduction in malaria burden.  A possible explanation for this may be that although there has been an overall reduction in malaria burden in the community, the malaria burden in ill children <5 years old has not changed much. The practice of self-medication  may have contributed to delay in appropriate health-seeking behaviour, and may have allowed enough time for malaria to cause anaemia through different mechanisms. 
Iron deficiency was also found to be significantly associated with anaemia. This is similar to some previous studies, [17,18] but contrary to the findings of Callis et al.  and Cardoso et al.  Iron-deficiency anaemia is sinister in young children.  The International Nutritional Anaemia Consultative Group (INACG) and WHO have recommended daily iron supplementation both for treatment and prophylaxis, especially for groups at risk.  This intervention seems to be adequately implemented among pregnant women who attend antenatal care and among sickle cell anaemic children attending routine follow-up clinic visits, but little or no activity is noted among otherwise well children. This study has revealed the need to improve the practice of daily iron supplementation, especially for children <5 years of age.
There was a low prevalence of hookworm infections among both anaemic and non-anaemic paediatric patients <5 years of age. This supports other studies that reported no association between anaemia and the prevalence of hookworm in children <5 years of age, [14,19] but in older age groups  the prevalence of hookworm infections increases. The findings of this study support the design of the anthelminthic programme, which excludes children <5 years of age from treatment; according to the Deworm the World Initiative, the implementation of the deworming programme should be school based.  However, there is still need for further study to determine the prevalence of other intestinal helminths among paediatric patients <5 years old. Although helminths may not be causing anaemia, they could contribute to other morbidity in young children.
Among the investigated paediatric patients, the prevalence of G6PD deficiency was high, and was significantly associated with anaemia, which contrasted with SCA--another haematologic genetic disorder that was found to have a low prevalence and no significant association with the prevalence of anaemia. This lack of association contrasts with the common assumption. However, it is insightful to note that although the prevalence of anaemia among SCA patients may be high, the prevalence of SCA among anaemic children was low. Therefore, the possibility of SCA being the contributing factor to anaemia among anaemic paediatric patients is very remote. This should influence the prioritisation of investigations, especially in sub-Saharan regions, where the poverty rate is high and iron deficiency is very common.
In this study, HIV prevalence among anaemic paediatric patients was low, at 13%, but it was significantly associated with anaemia. This is different from what other studies have reported. [13,15,16] Few studies have investigated the prevalence of HIV among anaemic children <5 years of age. The current finding does not disprove the potential of HIV to cause anaemia, but highlights that HIV/AIDS is not among the common causes of anaemia among paediatric patients.
Indicators of malnutrition were not found to be significantly associated with anaemia in paediatric patients in this study. This association has been reported by Callis et al.  but contrasts with the findings of Bernal et al.  and Ngnie-Teta et al.  There is no clear explanation for these reported differences, but it is likely that anthropometric measurements poorly reflect micronutrient status such as those of iron and folate, which are better assessed biochemically. [39,40]
A limitation of the study was the lack of bacteriological studies. A blood culture would have shown the prevalence of sepsis among children with anaemia, since bacterial infection is common in sub-Saharan African regions.
This study has shown that multiple factors contribute to anaemia in paediatric patients in Nigeria. Among these multiple causes, malaria and iron deficiency remain the major contributing factors. Therefore, in every child that presents with anaemia, an effort should be made to exclude malaria and iron deficiency. Furthermore, boosting malaria control programmes and promotion of iron supplementation programmes can reduce the burden of anaemia in Nigeria.
Acknowledgements. We are grateful to all the caregivers who allowed their children to be part of the study. The authors are thankful to the resident doctors in the Department of Paediatrics for their collaboration in the work.
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M D Ughasoro, MBBS, MPh, MSc (Health Economics), FWACP; I J Emodi, MBBS, FMCPaed;
H U Okafor, MBBS, FWACP, FMCPaed; B C Ibe, MBBS, FWACP, FMCPaed
Department of Paediatrics, College of Medical Sciences, University of Nigeria, Enugu, Nigeria
Corresponding author: M D Ughasoro (firstname.lastname@example.org)
Table 1. Age distribution of subjects diagnosed with anaemia Age groups (months) Anaemic, n (%) 6-12 76 (26.5) 13-36 146 (51.0) 37-59 64 (22.3) Table 2. Risk factors associated with childhood anaemia Anaemic children (N=286), Relative risk, Risk factors n (%) % (CI) p-value Malaria (n=256) 138 (48.3) 1.20 (1.01-1.41) 0.03 Serum iron (<9 [micro]mol 121 (42.3) 1.66 (1.42-1.93) 0.01 /L) (n=178) TIBC (> 80 [micro]mol/L) 97 (33.9) 1.65 (1.41-1.92) 0.01 (n=138) G6PD deficiency (n=120) 71 (24.8) 1.26 (1.05-1.50) 0.02 HIV seropositivity (n=59) 38 (13.3) 1.33 (1.08-1.65) 0.02 Haemoglobin genotype (SS) 7 (2.4) 1.44 (0.93-2.13) 0.34 * (n=10) Hookworm (ova) (n=4) 3 (1.1) 1.51 (0.86-2.71) 0.32 * CI = confidence interval. * Yates correction. Table 3. Anthropometric measures for the subjects Anaemic children (N=286), Relative risk, Variables n (%) % (CI) p-value * Stunting (<3rd centile) 45 (15.7) 0.98 (0.78-1.23) 0.82 (n=93) Wasting (<3rd centile) 18 (6.3) 0.76 (0.52-1.11) 0.10 (n=47) Underweight (<3rd centile) 17 (5.9) 0.88 (0.61-1.27) 0.51 (n=39) MUAC [less than or equal 20 (7.0) 1.38 (1.06-1.80) 0.07 to] 12.5 cm (n=30) * Correlates with anaemia in children.
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|Author:||Ughasoro, M.D.; Emodi, I.J.; Okafor, H.U.; Ibe, B.C.|
|Publication:||South African Journal of Child Health|
|Date:||Jan 1, 2015|
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