Schistosoma mansoni infection and its association with nutrition and health outcomes: a household survey in school-aged children living in Kasansa, Democratic Republic of the Congo

Introduction Schistosomiasis (SCH) is an important public health problem in developing countries and school-aged children are the most affected. This study explored health and nutritional status and their correlation with SCH in children attending primary school (3rd to 6th class) living in the area of Kasansa in the Democratic Republic of Congo. Methods Across-sectional household survey was carried out in Kasansa health area in February 2011. Children whose parents reported to attend primary school (3rd to 6th class) were included. Socio-demographic characteristics, information on morbidity history and risk factor were collected using a semi-structured questionnaire. S. mansoni and malaria infection were assessed using the Kato-katz technique and rapid diagnostic test, respectively. Haemoglobin concentration was also performed using a portable HemoControl device. Bivariate and multiple logistic regressions were used to assess risk factors for S. mansoni. Results A total of 197 school aged children participated in the study with a median age of 12 years and 53.8% of them were boys. The overall health status of the children was poor with very high prevalences of S. mansoni infection (89.3%), malaria infection (65.1%), anaemia (61.4%) and stunting (61.0%). Regular contact with river water was the most important risk factor (OR: 11.7; p<0.001) related to SCH infection. A low haemoglobin concentration was significantly associated with a SCH infection (OR: 12.3; p=0.003) and egg load was associated with stunting (OR: 12.4; p=0.04). Children from farmers were more at risk for low school performance (OR: 5.3; p=0.03). Conclusion High prevalence of Schistosoma mansoni and malaria infection was observed in the study population living in Kasansa area. Moreover, they presented a high burden of anaemia, chronic malnutrition and low school performance. An integrated disease control and management of these diseases and their consequences, endorsed by surveillance, is needed.


Introduction
Schistosomiasis (SCH) remains a serious public health problem in developing countries with a humid tropical climate [1,2]. It is listed as one of the neglected tropical diseases (NTD) and is poverty related [3,4]. It is the second most prevalent tropical disease, after malaria, causing severe morbidity in large areas of the world [5].
Approximately 800 million people may be at risk of infection worldwide and more than 200 million are infected, leading to the loss of up to 4.4 million disability-adjusted life years (DALYs), of which 90% are in sub-Saharan Africa [6,7]. Poor communities without access to safe water and adequate sanitation are more infected since agricultural, domestic and recreational activities expose them to infested water [8,9]. When in contact with fresh water, the cercaria, the larva of the schistosome, penetrate the skin; enter the capillaries and lymphatic vessels to migrate further to the mesenteric system or vesical plexus where they develop to adult worms in the blood vessels [10]. The morbidity of SCH is mainly caused by detrimental inflammatory reactions to the eggs trapped in the tissues of the gastrointestinal or genitourinary tract [2]. Most persons infected with schistosomes do not suffer from severe hepatosplenic disease (caused by S. mansoni and S. japonicum) or bladder calcification and hydronephrosis (caused by S. haematobium), but from less dramatic morbidities. Therefore, the overall impact on DALYs lost due to the lower grade pathologies is higher than those lost due to severe, sometimes life threatening pathologies [11].
Of all age groups, school aged children (aged between 6 and 15 years) are the most exposed because they are traditionally responsible for water-related household chores and because they often spend their free time swimming [12]. This age group also suffers the most. Chronic infection has alarming effects on their growth and also contributes to chronic anaemia, diminished school performances and even cognitive disorders [11]. Children with heavy worm burden and poor nutritional status are most likely to suffer from cognitive impairment [13]. Moreover, chronic SCH infection is commonly associated with anaemia [14]. A recent study conducted in the health wone of Kasansa showed that school aged children living in this area are highly infected by SCH [15]. In some areas, the prevalence of SCH infection was up to 94%. This high burden may have severe implications on the children's health status but unfortunately this study did not assess these. The aim of the present study is filling this gap and assessed the SCH related morbidity in the hyper-endemic health area that was reported with a prevalence of >90%. Some risk factors associated to SCH infection and associations with other health outcomes such as malnutrition, anaemia and low school performance were also assessed.

Ethical considerations
Ethical clearance was obtained from the ethical committees of the

Study design
This was a cross-sectional, household survey in which children attending primary school (3 rd to 6 th class) were targeted. At the time of the study, all children were at home since it was holidays.
Therefore the household survey was organized and the children were only included when they were present in the household and reported to attend primary school. The investigators went to the central point of Kasansa and a spinning bottle was used to randomly choose the direction to follow for door to door visits. The sample size was based on the WHO guidelines on SCH surveys [16] and 203 children that reported to attend primary school (3 rd to 6 th class) were included during a household survey. Age, sex, weight and height were recorded for each participating child. Information on morbidity history (previous abdominal pain, diarrhea, blood in the stool and previous treatment of SCH), risk factors (social economic status, behaviour, sanitary conditions, exposure habits) and school attendance, were also obtained from the parents or caretakers by standard questionnaires. A stool sample was collected from each participating child to determine the presence and intensity of SCH and the other intestinal helminths. A finger prick blood sample was taken to determine haemoglobin concentration and malaria infection.

S. mansoni infection
Kato-Katz technique [17] was performed for the detection of SCH infection. One stool sample was provided and slides of Kato-Katz

Haemoglobin concentration and anaemia
Haemoglobin (Hb) concentration was determined using a portable photometer (HemoCue® Hb 201) according to the manufacturer's instruction. The WHO thresholds were used for classification [18,19]: children were anaemic if Hb concentration was <11.5g/dl for children 7-11 years of age, <12.0g/dl for 12-14 years of age, <12.0g/dl and <13.0g/dl for respectively females and males older than 15 years.

Malaria infection
Malaria infections were detected using the commercial rapid diagnostic test (RDT) SD Bioline® Malaria Ag Pf/Pan (Standard diagnostics®, Korea) according to manufacturer's instructions.

Data analysis
Data were double-entered and validated in EPI INFO version 3.5.1 software and analysed using STATA version 12.0 (STATA Corp, Lakeway, College Station, Texas, USA). Categorical variables were expressed as proportions while quantitative variables were presented as the mean ± standard deviation (SD) or median ± interquartile range (IQR) if the data were not normally distributed.
WHO AnthroPlus software was used to calculate anthropometric indices' z-scores and determine the nutritional status of the schoolaged children. Age in months, height in cm and weight in kg were used to calculate the following indicators: 1) height-for-age Z score (HAZ) to assess stunting; 2) weight-for-age Z-score (WAS) to assess underweight in children <10 years old and 3) body-mass-index-forage Z-score (BAZ) to assess thinness. According to the 2007 WHO growth reference for school-aged children and adolescents, stunting, underweight and thinness were defined as <-2 SD HAZ, WAZ and BAZ respectively. Severe stunting, underweight and thinness were defined as <-3 SD HAZ, WAZ and BAZ respectively. Overall, 91.8% of the children lived in a household with daily expenses per person less than 1 USD.

Parasitic infection Prevalence and intensity of S. mansoni infection
The prevalence of SCH infection was 89.3% (CI 95%: 84.9-93.6), egg density was high in 55.3% of the children, 22.3% had moderate and 11.7% had a light egg density in the stool. In the 3 months prior to the visit, 73.6% of the children reported to suffer from abdominal pain, 50.2% had diarrhea and 41.6% had blood in the stool. Additional analysis of these symptoms associated with S. mansoni was performed; however, none of these parameters were found to be significantly associated with SCH infection.

Prevalence of malaria infection
The prevalence of malaria infection was 65.1% (CI 95%:58.1-72. 3) in the study population although 54.3% reported to have slept under an Insecticide-treated Bed Net (ITN). Nearly all households started using ITN after 2010 (99.0%) and the majority indicated that they received the ITN from the HZ of Kasansa (85.9%) in 2011 during the national campaign. Other sources of ITN were the health center (14.8%), and a minority had bought them from the local market (5.6%).

Anaemia and nutritional status of school-aged children
The proportion of children that presented anaemia was 61.4% with a median haemoglobin concentration of 11.3g/dl (IQR: 10.5-12.3).
The weight parameter (WAZ) of the nutritional status can only be calculated in children younger than 10 years old (n=23) was within healthy parameters, with 3 cases being underweight (13.0%) and 3 cases being severely underweight (13.0%) ( Table 2). The thinness parameter (BAZ) was also within healthy parameters for the majority of the children but 29.8% were too thin. The proportion of children with stunting was 61.0% of which 35.9% presented severe stunting. Boys were more affected by stunting than girls ( Figure 2).

School performance status
Class distribution of the children was as followed: 60 children

Risk factors related to S. mansoni infection and the related burden as anaemia, stunting or low school performance
The first model assessed risk factors related to S. mansoni infection.
Gender, age, presence of latrine, the profession of the household chief and water contact were included in the analysis (Table 3).
Only contact with water from the nearest river and water from the source were associated with SCH infection. Water contact to the source and well were predictors for SCH infection both for bathing The second model assessed correlates of anaemia (Table 4). The variables associated with a decrease of Hb concentration were gender (p=0.02), SCH infection (p=0.003), intensity of SCH egg load (p<0.001), self-reported presence of blood in the stool (p=0.001) and stunting (p<0.001). When correlation between anaemic status (binary outcomes) and SCH infection was analyzed, self-reported blood in the stool (OR=2.2; p=0.0.01), and severe stunting (OR=2.8; p=0.004) were retained as associated (Table 4).
These associations were maintained when multivariate analysis was performed. The AOR were 2.3 (p=0.008) and 1.7 (p=0.007) respectively for self-reported blood in the stool and severe stunting.
The third model assessed correlates of stunting (Table 5). Males presented an OR of 2.1 (p=0.01) and weak SCH infection was protective against stunting (OR=0.3; p=0.04)). Children older than 13 years presented 5.3 times more odds to have stunting (Table 5).
The last model assessed correlates of low school performance (Table 6). Only children from farmers had significantly lower school performance (OR: 5.3; p=0.03). When daily expenses were less than 1 USD an OR was found of 2.2 but it was not significant (p=0.1).

Discussion
The present cross-sectional study of children attending primary school (3 rd  Malawi, respectively [21][22][23]. Children whose parents are farmers might be more at risk, however, this was not observed in this study. Surprisingly, malaria infection was not found to be associated with anaemia in this study; however, stunting or severe stunting was significantly associated with anaemia and reduced Hb concentration. Therefore, it is possible to consider that this anaemia is not associated with malaria but to a chronic process. The high prevalence of schistosomiasis suggests that this illness contributes to these complications [11]. Stunting was also highly prevalent in the study population (61.0%), and boys were more affected than girls (AOR=2.3) (Figure 2). Age was also a significant factor for stunting. As the children grow older they are more at risk to develop stunting (OR from 2.5 to 5.3) which is a logic consequence of a poorly varied diet over a longer period of time. Light egg load was weakly associated to stunting; however, in the multivariate analysis only gender and age were strongly associated to stunting (Table 6). The limitation of the study was the fact that the children were enrolled during a household survey. They were enrolled when they reported to attend 3 rd to 6 th class of primary school. A selection bias could have occurred compared to selecting the children at school. Therefore, the class distribution was not equal. Older children (15)(16)(17) years old) were also found to attend primary school, however, in this environment, it is common that school attendance is not regular, accumulating a delay.

Conclusion
In conclusion, besides unacceptable prevalence of pathologies like schistosomiasis and malaria, children of Kasansa health area attending primary school also demonstrated a high burden of anaemia, chronic malnutrition and low school performance. Poverty might exacerbate the situation. It is therefore important to perform additional studies to demonstrate the causalities and better distinguish opportunities for control mechanisms for these diseases.
Results of this study may be used to direct public health professionals to identify specific intervention strategies against SCH that match the need of the population and therefore may be more effective. One option is to compare the population before and after schistosomiasis mass treatment. Another option is to compare two populations similar in all aspects except that one has schistosomiasis and the other does not; this is difficult to realize. Preventions measures such as snail control, integrated with population drug treatment can contribute to the reduction of schistosomiasis prevalence in Kasansa health area; however, morbidities such as anaemia, malnutrition and low school performance can persist due to the recurring low-level reinfection; so, the treatment may need to continue for a long period to maintain the disease control.
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