DOI: https://doi.org/10.21203/rs.2.12679/v1
Human schistosomiasis is a water-borne parasitic disease caused by Schistosome species. Infection is contracted through contact with contaminated water containing the infective cercariae [1,11]. Globally, it’s estimated that about 200 million people are infected with Schistosoma species in 74 tropical countries and that 500-600 million people are at risk of infection [2, 3,4,5]. Of the 200 million cases of infection, 120 million are symptomatic and 20 million have severe debilitating disease [6,7, 8,9,10]. In Uganda, Schistosoma 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 [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.
Methods
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 6-16 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).
Dependent variable: S. mansoni infection.
Data collection
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]. 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 associated risk factors. P-value ≤0.05 was considered statistically significant.
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. Aromo (218, 40.9%) and Agali (95, 17.9%) sub-counties had the highest and least number of participants, respectively.
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 (49.5% versus 50.5% each). With regard to age group, school children aged 10-14 years were the most infected (52.6%) compared to the other age groups although it was not statistically significant (Table 1). Prevalence of infection was significantly associated with sub-county location (χ2 = 60.4, df = 3, P <0.001) and primary schools (χ2 = 66.3, df = 7, P <0.001). Ogur sub county (80, 42.1%) had the highest prevalence and the least was from Barr and Agali sub-counties (27, 14.2%), respectively (Table 1). Among primary schools, Akangi and Akano both had the highest prevalence (40, 21.5%), and the least were from Okile (13, 6.8%) and Olilo (7, 3.7%), respectively. Also, the overall prevalence of S. mansoni infection was significantly associated with source of water (χ2 = 26.4, df = 3, P <0.001). Participants who fetch water from spring (85,44.7%) had highest infection rate than those who fetch water from other sources (Table 1). With respect to infection intensity, the individuals in the age group of 14-16 years and 10-14 years had heavy infections with epg of 600 and 565 eggs, respectively compared to those aged 6-9 years (Table 2). Among those who were positive for S. mansoni, 25.8% (49/190), 5.3% (10/190), and 68.9% (131/190) had light, moderate and heavy infections, respectively (Table 2). Both males and females had heavy infection with S. mansoni and mean egg count of 532 and 602, respectively.
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, 25]. 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 [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 [31] and Babile town, Nigeria [32], respectively. This could be attributed to geographical locations and difference in control interventions.
The prevalence of S. mansoni infection varied significantly with sub-county location and primary schools. Highest infections were recorded in Ogur sub-county and in Akangi and Akano primary schools (both in Ogur subcounty). This could be attributed to the numerous swamps around Ogur sub-county which contains a lot of infected snails (Byagamy pers. obs), and the absence of praziquantel treatment intervention in the area. Ogur subcounty was considered by MOH as a low prevalence area and MDA was administered only in Aromo subcounty. Similar variation in infection prevalence of S. mansoni by geographical location has been reported in previous studies in Gulu, northern Uganda [30], which have been attributed to variation in intensity of parasite transmission and frequency of exposure to cercariae contaminated water bodies [30].
Children aged 10-14 years were more infected (52.6%) than children aged 6-9 years (16.3%) with a decline among 15-16 years (31.6%). Studies conducted elsewhere have reported similar results, for example, in Jos, Nigeria, children aged 10-14 years were more infected with intestinal schistosomes (11.1%) than those in other age groups [31]. Similarly, in Gadabuke district, north central Nigeria, those aged 8-14 years was more infected (62.8%) than < 8 years [33]. 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, 31], 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%) [31,36,37]. Another report of higher prevalence rate in boys was given in Gulu municipality, Uganda (boys: 65.2%; girls: 34.8% [30]. The results of this survey further contradicted the findings at Northwest Ethiopia (boys:33.7%; girls: 42.2%) [22] and in Tanzania (boys 61.65%; girls 65.80%) [27] which could be due to different geographical locations and socio-cultural factors in those communities.
The high infection rate among children who collect water from the spring (44.7%) compared to those who fetch water from other sources could be because spring is an open source that is prone to contamination with feaces containing eggs of schistosomes. This finding is in agreement with several previous studies [33,31,34]. Fishing and swimming keep children in water for a prolonged time, which increases the chances of cercarial skin penetration.
Finally, the findings in this study have shown that almost 5.3% of the S. mansoni infections are heavy intensity infections and approximately 68.9% are of moderate intensity. This finding is higher than the one in Gulu Municipality which showed only 20.1% moderate infection [35]. This difference may be due to repeated exposure of school children to water bodies infested with infective stage in Lira district. Additionally, children aged 14-16 and 10-14 years had heavy infections compared to their younger counterparts (6-9). This might be due to the fact that older children frequently go to the open water sources to play and fetch water as reported elsewhere [38]. These children spend more time in the infested waters compared to their younger ones, thus increasing the exposure time for infection of S. mansoni.
Overall, this study showed that Lira District is endemic for S.mansoni. Therefore, there’s urgent need for provision of safe water, periodic treatment of all school-aged children with Praziquantel and public health education to reduce the prevalence of S. mansoni.
This study was conducted among school children in Lira district and the school-aged children in the community were excluded. Furthermore, a single stool sample was collected and analyzed, which may underestimate the prevalence of schistosomes as the chance of detecting parasites increases with examining multiple samples.
DEO District Education Officer
DHO District Health Officer
GUREC Gulu University Research Ethics Committee
epg Egg per gram of stool
LRRH Lira Regional Referral Hospital
MOH Ministry of Health
SPSS Statistical Package for Social Scientists
WHO World Health Organization
Authors’ contributions
BJP, MGM, RE, AH and EIOA conceived the study. BJP collected data, performed laboratory analyses and wrote the draft of the manuscript. BJP and MGM did statistical analyses of data. All authors’ read and approved the final manuscript.
Authors’ details
1Department of Biology, Faculty of Science, Gulu University, P.O. Box 166, Gulu, Uganda.
2Health Department, Lira District Local Government, P.O. Box, 49, Lira, Uganda.
3Department of Environmental and Biological Sciences, University of Eastern Finland, P.O. Box 111, 80101 Joensuu, Finland.
4Department of Microbiology and Immunology, Faculty of Medicine, Gulu University, P.O. Box 166, Gulu, Uganda.
Acknowledgements
The authors would like to extend their deepest appreciation to the school head teachers and the staff of LRRH and Lira district local government for their cooperation during data 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
Declarations
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.
Funding
Table 1 Socio-demographic characteristics and risk factors associated with S. mansoni infection in Lira district, northern Uganda (n = 532)
Variable |
Infection, n (%) |
|
χ2 (df) |
P value |
|
Positive |
Negative |
|
|
Gender |
|
|
|
|
Male |
94 (49.5%) |
171 (50.0%) |
0.014 |
0.907 |
Female |
96 (50.5%) |
171 (50.0%) |
|
|
Age (years) |
|
|
|
|
6-9 |
31 (16.3%) |
190 (55.6%) |
1.448 |
0.485 |
10-14 |
100 (52.6%) |
109 (31.9%) |
|
|
15-16 |
59 (31.1%) |
43 (12.6%) |
|
|
Sub county |
|
|
|
|
Aromo |
56 (29.5%) |
162 (47.4%) |
60.375 |
P<0.001 |
Ogur |
80 (42.1%) |
43 (12.6%) |
|
|
Barr |
27 (14.2%) |
73 (21.3%) |
|
|
Agali |
27 (14.2%) |
64 (18.7%) |
|
|
Primary school |
|
|
|
|
Oketkwer |
27 (14.2%) |
84 (24.6%) |
66.329 |
P<0.001 |
Akore |
29 (15.3%) |
78 (22.8%) |
|
|
Akano |
40 (21.5%) |
22 (6.4%) |
|
|
Akangi |
40 (21.5%) |
21 (6.1%) |
|
|
Barr |
18 (9.5%) |
31 (9.1%) |
|
|
Okile |
13 (6.8%) |
35 (10.2%) |
|
|
Abongorwot |
16 (8.4%) |
31 (9.1%) |
|
|
Olilo |
7 (3.7%) |
40 (11.7%) |
|
|
Water source |
|
|
|
|
Borehole |
63 (33.2%) |
190 (55.6%) |
26.355 |
P<0.001 |
Dam |
6 (3.2%) |
7 (2.1%) |
|
|
Spring |
85 (44.7%) |
91 (26.6%) |
|
|
Well |
36 (18.9%) |
54 (15.8%) |
|
|
Distance of home from water source |
|
|
|
|
Less than 500m |
42 (22.1%) |
69 (20.2%) |
9.084 |
0.059 |
500≤1000m |
36 (18.9%) |
65 (19.0%) |
|
|
1000≤1500m |
55 (28.9%) |
135 (39.5%) |
|
|
1500≤2000m |
36 (18.9%) |
39 (11.4%) |
|
|
≥2000m |
21 (11.1%) |
34 (9.9%) |
|
|
Table 2. Intensity of infection with S. mansoni by age groups and gender
Light (1-99 Epg) |
Moderate (100-399 epg) |
Heavy (>400 epg) |
Total |
|
Age groups |
No. (mean egg count) |
No. (mean egg count) |
No. (mean egg count) |
|
6-9yrs |
12 (84) |
19 (240) |
0 |
31 |
10-14yrs |
22 (72) |
71 (244) |
7 (565) |
100 |
15-16yrs |
15 (72) |
41 (207) |
3 (600) |
59 |
Sub Total |
49 |
131 |
10 |
190 |
Gender |
|
|
|
|
Male |
32 (72) |
78 (239) |
6 (532) |
116 |
Female |
17 (84) |
53 (234) |
4 (602) |
74 |
Sub Total |
49 |
131 |
10 |
190 |
Infection intensity (%) |
25.8 |
68.9 |
5.3 |
100 |