Elsevier

Acta Tropica

Volume 115, Issues 1–2, July–August 2010, Pages 103-111
Acta Tropica

Consequences of polyparasitism on anaemia among primary school children in Zimbabwe

https://doi.org/10.1016/j.actatropica.2010.02.010Get rights and content

Abstract

The effect of concomitant infection with schistosomes, Plasmodium falciparum and soil transmitted helminths (STHs) on anaemia was determined in 609 Zimbabwean primary school children. P. falciparum, haemoglobin levels and serum ferritin were determined from venous blood. Kato Katz, formal ether concentration and urine filtration techniques were used to assess prevalence of Schistosoma mansoni, STHs and Schistosoma haematobium infections. The prevalence of S. haematobium, S. mansoni, P. falciparum, hookworm, Trichuris trichiura and Ascaris lumbricoides were 52.3%, 22.7%, 27.9%, 23.7%, 2.3% and 2.1%, respectively. The overall prevalence of anaemia and iron deficiency anaemia (IDA) were 48.4% (277/572) and 38.1% (181/475). Haemoglobin levels among children who had P. falciparum, S. haematobium and hookworm were lower than negative individuals, p < 0.001, p < 0.001 and p = 0.030, respectively. The prevalence of anaemia and IDA in co-infections was almost double that in single infection. Children with P. falciparum/STHs/schistosome and schistosomes/P. falciparum co-infections recorded higher prevalence of anaemia and IDA (80.8% and 57.4%, respectively) than other combinations, p < 0.001. Logistic regression revealed that, age group  14years, P. falciparum, S. haematobium light and heavy infections, and S. mansoni moderate and heavy infection, hookworm light infection were predictors of anaemia. This study suggests that integrated school based de-worming and malaria control have the potential to reduce the burden of anaemia.

Introduction

Concomitant infection with Plasmodium falciparum, STH and schistosomes is common in tropical and sub-tropical countries due to geographic overlap of climatic and socio-economic conditions that support survival of STHs, reproduction of malaria parasites’ vectors and schistosomiasis intermediate host snails (Tshikuka et al., 1996, Brooker et al., 2007, Midzi et al., 2008). In Africa alone, about a quarter of school children may be at risk of co-infection with P. falciparum and helminths (Brooker et al., 2006, Brooker et al., 2007). They are also at risk of anaemia that reduces their cognitive potential, retard growth and predisposes them to other diseases (WHO, 2001). Although the etiologic factors of anaemia are complex including dietary insufficiency of iron, haemoglobinopathies, other micronutrient deficiencies (vitamin A, B12, folate and riboflavin), several studies have demonstrated the contribution of parasitic infections to anaemia. Results from meta-analysis and community based studies on malaria provide compelling evidence that malaria contributes substantially to anaemia (Geerligs et al., 2003, Korenromp et al., 2004, Ronald et al., 2006, Clarke et al., 2008). Hookworm has been shown to be an important risk factor for anaemia (Stoltzfus et al., 1997, Brooker et al., 1999). Olsen et al observed that hookworm egg intensity as low as 300 eggs/g stool was negatively related to levels of haemoglobin and serum ferritin (Olsen et al., 1998). The mechanisms by which schistosomiasis cause anaemia have been described by Freidman et al. (2005). Whilst some extensive field studies have failed to demonstrate any significant effect of schistosomiasis infection on haemoglobin (Hb) levels (Befidi-Mengue et al., 1993), several other studies have highlighted a significant effect of schistosomiasis on Hb levels and anaemia (Stephenson et al., 1985, Prual et al., 1992, Koukounari et al., 2007).

Although schistosomes, STHs and P. falciparum are separately known etiological factors of anaemia with distinct mechanisms which reduce haemoglobin levels in human hosts (Menendez et al., 2000, Hotez et al., 2004, Freidman et al., 2005), data are still lacking on the effect of their coincidental infection on the level and severity of anaemia (Hotez et al., 2006, Midzi et al., 2008). Several studies have only explored the effect of single parasitic infections (Flemming et al., 2006, Koukounari et al., 2006), mixed infections with schistosomiasis and STH (Guyatt et al., 2001), STHs and P. falciparum (Koukounari et al., 2006) or multiple STHs infection on anaemia (Ezeamama et al., 2005). Studies on the impact of schistosomes, STHs and P. falciparum co-infection on anaemia, particularly in primary school children are relevant for the design and implementation of integrated control programmes aimed at reducing anaemia and other associated morbidities.

Zimbabwe is endemic for schistosomiasis, soil transmitted helminthiasis and malaria that pose a public health problem (Taylor and Makura, 1985, Chandiwana et al., 1989, Mutapi et al., 2000). This study was therefore conducted to determine the effect of malaria, schistosomiasis and STHs co-infection on the level of anaemia and also to identify predictors of anaemia among primary school children living in an area where P. falciparum, schistosome and STHs are co-endemic (Brooker et al., 2007).

Section snippets

Study area and population

The study was conducted in July 2004 among 609 primary school children (age range 5–15 years) living in Burma Valley commercial farming areas in Mutare district that is situated to the eastern part of Zimbabwe. The geographic position, climatic conditions and demographic information of the people living in the study area have been described elsewhere. The study participants were drawn from children who attended three primary schools (Valhalla, Msapa and Kaswa). The community from which the

Results

Six hundred and nine (609) children were recruited into the study and 50.4% of these were males. The overall mean (SD) age for the study population was 10.3 (2.3) years age range (6–17 years). The distribution of parasites and their egg intensities categorised according to WHO guidelines are shown in Table 1. S. haematobium was the most prevalent of all parasites investigated. Overall, 74.1% of children were infected with at least one of the parasites (P. falciparum, schistosomes or STHs).

Discussion

This study has shown an increase in anaemia, IDA and the corresponding decrease in Hb levels with increasing number of parasites infecting individuals. This is demonstrated in Table 3 where anaemia prevalence in co-infections is almost double the corresponding prevalence of anaemia in single infections with the highest prevalence of anaemia occurring in triple infections. The interaction of different mechanisms by which these different parasites reduce Hb levels in the host could be the cause

Conclusions

The results from our study have fundamental practical implications for control of anaemia and parasitic diseases of public health importance. Thus integrated helminths de-worming and control of malaria through prompt diagnosis, treatment of children and provision of insecticide treated bed nets in schools would reduce the resultant deleterious co-morbidity such as anaemia in school children living in co-endemic communities. However as this is still an understudied area, further studies

Authorship contributions

TM, NM, KCB, FM, NK contributed to the concept and design of the study protocol; NM, TM, SZ, DS, GH, JM carried out clinical assessment and parasitology; TM, NM, CMT, MPM, NK, FM carried out the analysis and interpretation of the data; NM, TM, CMT, MM, SZ drafted the manuscript. All authors read and approved the manuscript. TM and NM are guarantors of the paper.

Funding

The Ministry of Health and Child Welfare of Zimbabwe provided funds through the Essential National Health Research vote for the field data collection. The UNICEF/UNDP/World Bank/WHO Special Program for Research and Training in Tropical Diseases (TDR) provided financial support for laboratory data analysis. International Foundation for Science W/4231 to TM for parasitology and the Wellcome Trust (Grant no WT082028MA). Schistosomiasis Control Initiative (SCI), Imperial College, UK supported the

Conflict of interest

None declared.

Ethical consideration

The Medical Research Council of Zimbabwe approved the study. In addition, Provincial Medical and Education Directors and teachers granted permission. Inclusion of children into the study took place after free individual and parental informed consent. Children joined the study voluntarily and were free to drop out at any time they wished without prejudice.

Acknowledgements

We acknowledge the Secretary for Health and Child Welfare of Zimbabwe for providing financial support for field data collection activities, the Acting director, National Institute of Health Research for all the support, all school children from Burma Valley farming areas who participated in the study, the Provincial Medical, Education Directors for Manicaland and parents for granting us permission to conduct the study. We are also grateful to the technical staff from the National Institute of

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