Prevalence, infection intensity and associated risk factors of Intestinal Schistosomiasis among primary school Children in Lira District, Northern Uganda

Abstract Objective: The aim of this cross-sectional study was to determine the prevalence, infection intensity and associated risk factors of intestinal schistosomiasis among primary school children in Lira district, Uganda. The study was conducted among 532 primary school pupils aged 6-16 years from eight randomly selected primary schools (March-May 2017). Stool samples were collected and examined for schistosomiasis using Odongo-Aginya method. Data on socio-demographic characteristics and risk factors were obtained using questionnaires. Results: The overall prevalence of Schistosoma mansoni was 35.7% indicating a moderate infection. Both males and females were equally affected with S. mansoni . Ogur sub county had highest prevalence (65.0%) than others. Akangi (65.5%) and Akano (64.5%) primary schools both had highest prevalence compared to the others. With regard to risk factors, source of drinking water, sub-county location and primary school were associated with prevalence of infection whereas only school location and home distance to water source was associated with intensity. Participants who fetch water from spring, dam and wells had higher infection than those who fetch from boreholes. The study recommends provision of safe water, periodic treatment of school-aged children with praziquantel and public health education to reduce prevalence of S. mansoni .

is more widely distributed than S. haematobium, with highly endemic foci of infection around Lake Albert, Victoria and Kyoga, and along the Albert Nile [12,13,14]. Uganda has been described as a cradle of S. mansoni in Africa because the parasite is widely distributed than anywhere in the world, and the transmission pattern involves many snail hosts [12].
In developing countries, school children are particularly vulnerable to schistosomiasis because of their contact activities with contaminated waters, where they contract the infection. A study conducted along river Anyau in Arua recorded prevalence of S. mansoni of 62% [14]. Males were more infected than females, and school children had higher infection rates (71.1%) compared to the villagers (62.8%) living along the shores. Also, along the Albert Nile in Uganda, high prevalence of S. mansoni was recorded at 81.5% [15]. The residence of Rhino camp and Obongi fishing villages excreted high egg count of ≥ 500 Epg and the infection was highest in individuals aged 11-20 years [15].
Lira district is among the moderately burdened districts with schistosomiasis in Uganda [16] where MDA is administered every two years with praziquantel. However, published data indicating the actual prevalence among primary school children is lacking. This survey was undertaken to determine the prevalence, infection intensity and associated risk factors of intestinal schistosomiasis among primary school children in Lira district, Uganda.

Study area and period
The study was conducted in randomly selected primary schools in Lira District, Uganda, from March-May 2017.

Study design and population
A cross-sectional study design was conducted. All participants whose guardians or parents signed a written informed consent and who were available and registered in their school during the study period and who gave stool sample were included in the study. Children who were severely ill or who were on anti-helminthic drug or treatment within three weeks prior to data collection and study subjects who refused to provide stool samples at the time of sampling were excluded from the study.

Sample size determination
Sampled size was determined using Kish [17] formula considering: Prevalence rate (p) of 50%, 95% confidence interval and 5% margin of error. Adding 39% none response rate the total sample size was 532.

Sampling procedure and techniques
Eight primary schools were selected from four sub-counties (Table 1). Pupils aged [6][7][8][9][10][11][12][13][14][15][16] years voluntarily enrolled in the study. In each school, proportionate sample was allotted according to the number of the pupils in each class. The registration list was used as the sampling frame.

Study variables
Independent variables: socio-demographic and risk variables (gender, age, sub-county, primary school, water source, distance of home from water source).

Socio-demographic data and risk factors
School children participated in the study were interviewed with pre-tested questionnaires to collect information on socio-demographic data and associated risk factors. The questionnaire was prepared in English and translated to Luo. Pre-testing was done in 5% of school children that were not included in the study and appropriate correction applied.

Stool sample collection and processing
Each participant was provided with a wide-mouthed, clean, leak proof stool container labeled with participant's code, laboratory number, date of collection. Each participant collected approximately 10gm of stool and delivered to the laboratory within one hour.
Specimen processing and examination was done at LRRH laboratory using the Odongo-Aginya method [18,34]. The prepared slides were examined microscopically within 5 min of collection. Samples with eggs were recorded as positive while those without eggs were taken to be negative. For positive samples, eggs were counted and each average count was recorded as number of eggs per gram of feaces (epg). Intensity of infection was categorized by age group and gender into light (1-99 epg), moderate (100-399 epg), and heavy (epg ≥ 400) infections according to WHO [6].

Statistical analysis
Demographic data was analyzed using descriptive statistics. Chi-square in SPSS version25 was used to identify association between prevalence of schistosomiasis and risk factors.
To identify factors associated with the intensity of S.mansoni infection, we utilized a negative binomial generalized linear model with a loglink function.

Socio-demographic characteristics
A total of 532 participants aged 6-16 years were enrolled in this study. 267 (50.2%) were males and 265 (49.8%) were females ( Table 1). The mean age (± standard deviation) of the study participants was 12 years. The highest number of participants (290, 54.5%) were from the age group of 10-14 years and the least (74, 13.6%) was from 6-9 years.

Prevalence and intensity of S. mansoni infection
The overall prevalence rate of S. mansoni among primary school children was 35.7% (190/532). Males and females were nearly equally infected (36.0% versus 35.5% each).
With regard to age group, school children aged 6-9 years were the most infected (41.9%) compared to the other age groups although it was not statistically significant (

Discussion
In this study, the overall prevalence of S. mansoni infection among the school children was 35.7%. This is categorized as moderate risk [19]. This prevalence is low compared to those obtained from western Kenya (76.8%), and in Tanzania (64.3%) [24,26]. This low prevalence in Lira district could be due to the massive administration of preventive chemotherapeutic praziquantel (in Aromo subcounty only) and Albendazole to the school children by MOH Uganda two years prior to the study. This finding is similar with results from studies conducted among communities in islands of Lake Victoria, Uganda [20,21] and in Northwest Ethiopia and west Africa [22,23], respectively. Nevertheless, the prevalence obtained in this study is higher compared to 20.1%, 4.6%, 4.3% reported in Gulu municipality, Uganda [30] and in Jos, Nigeria [36], respectively. This could be attributed to differences in geographical locations and in control interventions.  [30]. However, in contrast to the present results, highest prevalence was found among the 6-10 years old (90.4%) in Ethiopia than in those 11-15 years 89.7% [28]. This might be attributed to the behavioral patterns of different age groups with respect to water contact activities and poor personal hygiene. Children aged 10-14 years were older and often got in contact with infected water bodies through various water activities such as swimming, fetching water, playing with shallow water and fishing, washing clothes and farming. However, children older than 14 years have lower risk of being infected as they are less likely to be engaged in recreational water-contact behaviors compared to younger children. Other studies have indicated that age acquired immunity to reinfection contributes to the drop in the prevalence rates among children aged 15 years and above [29].
Even though some studies reported that prevalence among males was higher than females [30], in the present study no difference was observed in the prevalence between males and females. This could be due to the socio-cultural set-up activities where both males and females are equally actively involved in water-related activities like swimming, fishing, grazing in the swamps, bathing and playing with shallow water, collecting rids from swamps and farming [30]. In Los, Nigeria, for example, prevalence of S. mansoni infections were higher in males (22.2%) than in females (3.7%) [31,35,36]. Declarations collection and for providing the necessary information. We thank all the study participants for their cooperation. We are grateful to Paul Okidi for assistance with data collection.

Competing interests
The authors declare that they have no competing interests

Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Consent for Publication
Not Applicable

Ethical approval and consent to participate
The study was approved by the Gulu University Research Ethics Committee (No. GUREC 04/03/2017). Permission to conduct this study was later granted by the DHO, DEO and management of selected primary schools in Lira district. Written (signed) informed consent and assent were sought from class teachers and each participant before conducting the interviews and sample collection. Data collected from each study participant and results of laboratory tests were kept confidential and codes rather than participant's name were used. Children found infected were treated with praziquantel for free.