Prevalence of S. mansoni Infection and Associated Risk Factors among School Children in Guangua District, Northwest Ethiopia

Methods A cross-sectional study design was employed. Four hundred twenty-two participants were selected. Data was collected through observation and interview with structured questionnaire. Stool specimens were collected and examined using two-slide Kato-Katz method. The data were analyzed using SPSS version 23. Logistic regression was fitted for analysis. Variables with p value <0.25 in the univariate logistic regression analysis were entered into the multivariable logistic regression model. Those with <0.05 were identified as significantly associated risk factors. To assure the quality of the data, training was given for data collectors and supervisors, and the tools were pretested on 5% of the sample size. Results 404 (95.7%) school children were enrolled in the study. The overall prevalence of S. mansoni was 12.6%. School children in the age group 5-9 years old (AOR (95% CI): 22.27 (3.70-134.01), p = 0.001), age group 10-14 years old (AOR (95% CI): 4.58 (1.14-18.42), p = 0.032), grade levels 5-8 (AOR (95% CL): 14.95 (4.297-52.03), p = 0.001),who swim frequently (AOR (95% CI): 11.35 (2.33-55.33), p = 0.003), and those who cultivate near the irrigation area (AOR (95% CI): 7.10 (2.31-21.80), p = 0.001) were significantly associated with high risk of S. mansoni infection. Conclusion and Recommendation. From the finding of the current study, it can be concluded that the prevalence of Schistosoma mansoni in the study area is relatively high. Age of fourteen and younger years old, swimming in the river, and irrigation practice were the main risk factors of S. mansoni infection. Thus, therapeutic interventions as well as health education are desirable.


Introduction
Schistosomiasis or bilharzia is an acute and chronic parasitic disease caused by a blood fluke (trematode worm) belonging to the genus Schistosoma [1]. There are five schistosome species causing the disease, namely, S. haematobium, S. mansoni, S. japonicum, S. mekongi, and S. intercalatum [2]. The most clinically important species are Schistosoma mansoni and Shistosoma haematobium [1]. S. mansoni causes intesti-nal schistosomiasis, and it is endemic in sub-Saharan Africa [3]. It is predominant in most parts of the country [4].
In Ethiopia, a number of epidemiological studies showed that intestinal schistosomiasis due to S. mansoni infection is widely distributed in several localities of the country with varying magnitudes of prevalence as high as 90% in school children [5]. In Ethiopia, about 5.01 million people are thought to be infected with schistosomiasis and 37.5 million to be at risk of infections [6].
S. mansoni infection is transmitted through contact with fresh water polluted with human excreta containing schistosoma eggs, when the egg hatch in fresh water and releasing free swimming miracidia, which infect aquatic snail Biomphalaria pfeifferi. Biomphalaria pfeifferi is an intermediate host for S. mansoni to complete its life cycle and then release cercariae into the water, and human can be infected during contacts with water for various domestic purposes [7,8]. It is more widespread in poor rural communities particularly in places where fishing and agricultural activities are dominant [9]. Domestic activities such as washing clothes and fetching water from contaminated Rivers/Lakes are the main risk factors for S. mansoni infection, which is a potential for children to be infected. Poor hygiene and recreational activities like swimming and fishing also increase the risk of infection in children [10].
In Ethiopia, S. mansoni infection is one of the prevalent parasitic diseases reported across many regions, causing considerable morbidity. In northern Ethiopia, in Alamata district, studies revealed 73.9% prevalence of S. mansoni infection [11].
Higher rates of infections were observed in males than females due to the frequent water contact behavior of male [12]. Due to they have higher participation in bathing, swimming and irrigation activities [13].
Effective control of the disease requires determining its prevalence rate and identifying risk factors of infection in high-risk population groups [12]. It was important to conduct this research as the study site was appropriate for the study due to the presence of irrigational farming for agricultural product on the river, which is suitable for the intermediate host of S. mansoni. Efforts have been made to document the distribution of S. mansoni infection nearly at all corners of the region. However, it cannot be said that the distribution of the disease is fully mapped out, as there are recent discoveries of new transmission foci possibly associated with expansion of water development projects and human movement [14].
Studies that indicate the prevalence of S. mansoni infection and other intestinal parasites in different areas are crucial for identifying communities at high risk for parasitic infections and for formulating suitable prevention and control measures. The current study aimed to determine the prevalence of S. mansoni infection and associated risk factors among school children in two settings of Guangua district, northwest Ethiopia. The findings will help in strengthening the information available so far and encourage policy makers to design effective strategies to combat S. mansoni infection.

Study Area and Design.
A cross-sectional study was conducted from February to May 2018 to determine the prevalence of S. mansoni infection and associated risk factors among school children in Guangua district, northwest Ethiopia. Guangua district is found in Agew Awi Zone, Amhara region. Guangua is bordered on the south and west by the Benshangul-Gumuz region, on the north by Dangla, on the northwest by Faggeta Lekoma and Banja Shekudad, and on the east Ankasha Guagua; the Dura River, a tributary of Abay River, defines parts of its western bordered. The district has 20 rural kebeles and 64 primary schools with an elevation of 1650 m above sea level. The average annual rain fall is 1896.6 mm with an average temperature of 25°C. The total population of the district is 142, 947. The economic base of the majority of the population (93.7%) of the district is agriculture.
Multistage sampling was employed to select the study subjects. The study was conducted in Anguay kebele which have two schools. During the study period, the total number of children attending Kibi and Gichgich was 1650 and 921, respectively. The sample size was allocated into two schools based on their total number. This kebele was selected purposively as it is a nearby kebele to the irrigation site in Dura River. The students were stratified by grade level from 1 to 8 in both schools. The numbers of the study participants were selected by systematic sampling technique in each class using their class rosters as sampling frame.

Inclusion and Exclusion
Criteria. All school children who gave consent to participate in the study and who had no any history of taking antihelminthes drug during the data collection or with in the last three months were included in the study. While children who were absent on the day of data collection and who did not gave consent were excluded to participate.

Variables.
The dependent variable is the S. mansoni infection status.
The independent variables were Socio demographic status, water contact habit, defecation practice and latrine availability, shoe wearing habit, irrigation practices, availability of dams, distance between their homes and water bodies, and knowledge about S. mansoni infection, its transmission, and prevention method.

Data Collection Tool.
A structured interview questionnaire was used to collect data on socio-demographic characteristics and associated risk factors of S. mansoni infection. The questionnaire was first developed in English and translated into the local language, Amharic, and then translated back to English to check consistency.

Sample Collection and Examination.
A labeled, clean, dry, and leak-proof stool cup was used to collect a stool specimen of about 3 g from each student with an applicator stick, and it was preserved in 10% formalin solution. Then, the stool samples were transported to Bahir Dar University Biomedical Research Laboratory and were processed by Kato-Katz technique, using fixed quantity of sieved 41.7 mg of 2 Journal of Parasitology Research stool on holed template. They were mounted on slides and covered with malachite green saturated cellophane [9]. Finally, the smeared slides were examined under microscope using 10× and 40× for detection of eggs of the parasite.
2.6. Data Analysis. Congregated data were double entered into and analyzed using SPSS version 23 software. Descriptive statistics was carried out to measure relative frequencies and percentages of the variables. Chi-squared tests (χ2) were used to determine the association between variables and to test statistical significance differences. Logistic regression analysis was performed to examine associations between variables. Odds ratios (OR) were calculated with 95% confidence interval (CI). Variables having significance at p values 0.25 in univariate test were selected for multivariate logistic regression analysis to identify the most important predictors of Schistosoma mansoni risk factors based on the test from logistic regression [16]. The associations were considered to be statistically significant when p values are less than 0.05.

Data Quality Control.
All the necessary reagents, chemicals, and instruments were checked by known positive and negative samples before processing and examination of samples of the study participants. Training was given for data collectors and supervisors. Also the specimens were checked for the serial number, quantity, and procedure of collection. Before the actual data collection, pretest was conducted involving 5% of the sample size that were not part of the sample population in the actual study to ensure the validity of the data collection tool. The smear samples were reexamined by other laboratory experts, which was blinded for the first examination results.

Ethical Considerations.
Ethical approval was obtained from the research and community service coordinating office of Science College, Bahir Dar University. Permissions were obtained from school administration/school director office to conduct the study after explaining the purpose and objective of the study. Informed written and oral consent was also obtained from the parent/guardian of the children/their home room teachers. All the data obtained from each study participant was kept confidential. Children found positive for Schistosoma mansoni were treated with the WHO standard procedure. Participants who were found infected during the study were provided prescription to take the drug in the nearby pharmacy.

Socio-Demographic Characteristics of Study Participants.
A total of 422 school children were invited to participate, among these, 404 (95.7%) individuals were enrolled in the study, and the remaining 18 individuals were refused to participate. Of the total subject, 227 (56.2%) were male, and 177 (43.8%) were female. The highest proportion of participants 185 (45.8%) were found to be within the age range of 10-14 years. About 269 (66.6%) participants were from grades 1-4, and the remaining 135 (33.4%) were from grade levels 5-8. The parents of majority students (297 (73.5%)) were uneducated (Table 1).

Risk Factors
The majority of 304 (75.2%) participants washes their clothes and utensils in the River, amongst those 45 (14.8%) were positive for S. mansoni infection. With regard to swimming habits in the rivers, the prevalence of S. mansoni infection was higher in those who swim always 29 (38.2%) and followed by some times 18 (6.8%) and not at all 4 (6.3%). In this study, respondents who cross the water bodies (37 (22.6%)), who were involved at irrigation practices (43 (22.8%)), and who live at areas where there are dams in their locality (28 (17.4%)) were found to be positive for S. mansoni infection. In terms of distance between their homes and water bodies, the highest prevalence was observed in near distance (<1 KM) 37 (18.6%) compared to far distance (≥1 KM) 14 (6.8%). School children who had no the habit of shoe wearing (38 (16.3%)) and absence of latrine in their homes (42 (17.1%)) were more infected with S. mansoni (Table 2).
This result showed that more than half (253 (62.6%)) of the study participants did not know about the disease, S. mansoni, and its transmission methods among these (41 (16.2%)) were positive. Sixty one percent of study participants had no knowledge about the burden of S. mansoni infection, of those majority (42 (16.7%)) were affected. More than half (250 (61.9%)) of the respondents defecate in open field. Among S. mansoni positive individuals, majority of them were defecates in open field (43(17.2%)) compared to those who did not defecate in open field (8 (5.2%)) ( Table 2).

Multivariate Analyses of S. mansoni Infection and Its
Associated Factors. In multivariate analysis, the significant independent predictors of S. mansoni infection in this study were the age group 5-9 years and age group 10-14 years, grade level 5-8, always swimming in the River, having irrigation practice, and crossing the water bodies, while the remaining variables were not observed to have any significant association with S. mansoni infection (Table 3).

Discussion
The overall prevalence rate of S. mansoni among study participants in the current study was 12.6%. It is comparable with the study finding in an endemic area of Niger River basin (12.5%) [17] and Agaie, Niger State (10.17%) [18] of Nigeria, and Dembia (15.4%) [19] and (11.4%) Wondo District of Ethiopia [20].   Journal of Parasitology Research However, it was higher than the prevalence among preschool children in Gondar town (5.9%) [21], among the school children in Côte d'Ivoire (6.1%) [22], and in the White Nile River Basin of Sudan (5.9%) [23]. Higher prevalence of S. mansoni in the current study could be due to the existence of Dura River where the local community uses for washing clothes, taking baths, and fetching water for domestic purpose. The river may serve as a potential source of infection for S. mansoni. Moreover, the weather condition in the area is relatively warmer and more humid which favor the existence and reproduction rate of the snail. The other possible cause might be related with the differences in children's behavior to water contact and level of awareness about the prevention and control of S. mansoni infection.
The prevalence in the current study was lower than the overall prevalence of S. mansoni infection among school children in districts of north Gondar (Chuahit, Sanja, Debark, and Maksegnit) (33.5%) [24], nearby rivers in

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Jimma town (28.7%) [25], in rural area of Bahir Dar (24.9%) [26], in Jimma Zone (27.6%) [27], southern Ethiopia (25.8%) [28], and Mekelle city (23.9%) [12]. This study was also much lower as compared to the finding in Sanja area, Amhara region (82.8%) [29], and Damot Woide dis-trict, Wolaita Zone (81.3%) [14]. The variations in the prevalence may be due to some factors such as difference in water contact habit, toilet utilization, and ecological distribution of snails in the study area (the presence of fast running rivers (Dura) in the current study may lead to low  Journal of Parasitology Research availability of vector snails, since snails mainly prefer stagnant or slow-moving water bodies). The snail (Biomphalaria pfeifferi), responsible for the transmission of S. mansoni infection, is more prevalent in areas 2000 m above sea level [30]. The variations in the prevalence in this study might also be due to factors which are related with the characteristics of intermediate snail hosts.
In the current study, polyparasitism was observed other than the S. mansoni infection. Even if they perform sanitation; it is not enough in preventing schistosoma infection [31]. On the other hand, S. mansoni and other parasite infections will never be a public health problem if there are appropriate improvements of hygiene and sanitation standards [32]. The presence of adequate sanitation does not necessarily guarantee its use. The bulk of Schistosoma specious eggs reach directly into the water usually by children during bathing and swimming. The use of adequate sanitation systems for urine and faeces has reduced schistosomiasis within short periods of time, while it takes longer for other helminths such as Ascaris lumbricoides and Trichuris trichiura [31].
Though a study in two the settings of Côte d'Ivoire [22] reported similar prevalence rates for boys and girls in Kenya [33], many studies showed contrasting finding in the prevalence of S. mansoni infection by sex [32][33][34]. The finding of the current study also showed higher prevalence of S. mansoni infection in males than in female. It is in agreement with the studies done in Wolaita Zone of Ethiopia [14] and the findings in Niger [35] and central Sudan [36]. Male children may have higher exposure of contact with cercariae contaminated water bodies than females while helping their family in outdoor activities such as herding cattle.
Unlike a study in Sanja area of Amhara, Ethiopia [29], which reported a similar prevalence of S. mansoni across the age group of school children, the current finding showed that students in the age group of 14 years old and younger were at a higher risk of acquiring S. mansoni infection than those with the age range of 15-19. It was in line with previous studies done in Ethiopia [29,36]. This might be due to their chance of playing in the field which increases the probability of contact with cercaria contaminated water bodies.
In the current study, the prevalence of S. mansoni infection was significantly associated with the frequency of swimming in the river. The chances of positive S. mansoni infection were eleven times higher in individuals who always swim in the river compared to those who never swim. This was in agreement with studies done in Hawassa and Gorgora of Ethiopia [33,37].
The current study revealed that water contact habit through irrigation practice and crossing the water bodies in their way to school are associated with high prevalence of S. mansoni infection; this was in line with the study at Wolaita Zone, Southern [14] and Gondar town of Ethiopia [21], and south Côte d'Ivoire, and central Côte d'Ivoire [38], which reported that water contact at stream crosses and herding cattle near the stream increase the risk of S. mansoni infection.
This study also showed that working in an irrigated field is significantly associated with S. mansoni infection. This is in agreement with the findings of the studies at Dudicha and Shesha Kekel localities [39], with different water source users in Tigray region of Ethiopia [40] and southeastern Brazil [41]. Distance from the water bodies was also associated with S. mansoni infection. Children who live near to the water bodies were more infected with S. mansoni than those who live far. It was in agreement with previous findings of a study in Cote d'Ivoire [42]. This study also showed that the prevalence of S. mansoni infection was associated with shoe wearing habit. This is in line with the findings of a study in Jiga town [43]. This could be due to the agricultural-based economy of the community; closer distance with water bodies and continuous barefoot water contact inhabit increase the chance of contact with water bodies that contain S. mansoni cercariae.

Conclusion and Recommendation
S. mansoni infection was the major problem among school children in the current study. Students having fourteen and younger years old, students who frequently swim in the river, having irrigation practice, and cross the river bodies were at a higher risk of S. mansoni infection. Hence, it is recommended to focus on raising the awareness of the school children about the prevention and control measures of S. mansoni in the locality. In addition, responsible bodies on irrigational practices should work on the regular cleaning of water canals which favor the reproduction of the snail.

OR:
Odd ratio AOR: Adjusted odds ratio COR: Crude odds ratio CI: Confidence

Data Availability
The datasets used and analyzed during the current study are available from the corresponding author on reasonable request (in SPSS code).

Ethical Approval
The study was reviewed and approved by the Ethical Review Committee under the research and community service coordinating office of College of Science, Bahir Dar University. Informed written and verbal consent was obtained from 7 Journal of Parasitology Research the study participants and all participants who agreed to take part in the survey signed a consent form.

Conflicts of Interest
The authors declare that they have no conflict of interest.

Authors' Contributions
BT contributed to the design of the study, analyzed the data, and wrote the first draft of the manuscript. DT contributed to the design of the study, collected the data, and critically reviewed the manuscript. MA participated in the designing of the study and coordinating the data collection process. DS and MT was involved microscopic analysis of the sample and critically reviewed the manuscript. All authors read and approved the final draft of the manuscript.