Prevalence and intensity of intestinal schistosomiasis among the adult population, and water and sanitation conditions: a community-based cross-section study at Muleba District

Background Intestinal schistosomiasis is one of the serious public health problems in all age groups and can lead to considerable morbidity and mortality especially to communities with an inadequate supply of safe water and sanitation services. Objective This study was conducted to establish the current burden of intestinal schistosomiasis among adults in the Muleba District and assessment of water and sanitation conditions that might inuence the transmission of intestinal schistosomiasis. Methods A community-based cross-sectional study was conducted between July and August 2020. A total of 328 stool samples were collected and processed using formal-ether concentration and Kato-Katz methods. Water and sanitation data were collected using a questionnaire interview conducted among participants. Participants were randomly selected from four villages. Data were analyzed by using Statistical Package for the Social Sciences software version 23.


Introduction
Intestinal schistosomiasis is one of the neglected parasitic diseases that cause signi cant morbidity and mortality in the tropical and subtropical regions of Africa, Asia, and Latin America. Several species of Schistosoma including Schistosoma mansoni (S.mansoni), S. japonicum, S. intercalatum, and S. mekongi are responsible for causing intestinal schistosomiasis in different settings. However, S.mansoni accounts for more cases of intestinal schistosomiasis compared to the rest of the intestinal Schistosoma species [1]. Globally, 54 million people are infected with S.mansoni and 393 million people are at risk of acquiring intestinal schistosomiasis caused by S.mansoni [2].
Pre and school-aged children and adults with occupations such as shing, farming, and irrigation involving contact with infested water are considered at higher risk of acquiring the infection. However, school-aged children carriers the highest burden of the infection and contribute signi cantly to the transmission of intestinal schistosomiasis [3].
Chronic intestinal schistosomiasis among the vulnerable population is associated with stunting growth in children, cognitive dysfunction in children, and hepatosplenic diseases including splenomegaly, hepatomegaly [4,5]. The transmission of intestinal schistosomiasis is associated with several factors such as inadequate water supply, poor environmental sanitation, unhygienic practices, and low socioeconomic status in poor and rural communities [6][7][8].
Intestinal schistosomiasis caused by S.mansoni is endemic in Tanzania with uneven distribution [9]. Prevalence and intensity of S.mansoni in Tanzania range from 40-100% in different regions and in communities where farming and shing are the main sources of income, exposure of adults in infested water becomes inevitable and hence in uences the high prevalence of intestinal schistosomiasis in adults compared to school children [9][10][11]. The global control of intestinal schistosomiasis has been focused on the school-aged children through the use of praziquantel while other vulnerable populations that serve as the reservoir of infection are left out [12].
The previous studies conducted along the Lake Victoria basin found that in Muleba district there was higher prevalence of inestinal schistosomiasis among adult population compared to the school aged children [13,14].
Evidence indicates that there is ongoing transmission of intestinal schistosomiasis among the adult population [13]. Hence, there is a need to establish the burden of intestinal schistosomiasis among the adult population and associated risk factors. Therefore, this study was conducted to establish the current burden of intestinal schistosomiasis among adults in Muleba District and assessment of water and sanitation conditions that might in uence the transmission of intestinal schistosomiasis. The ndings will provide information on the current infection status among adults and its association with water and sanitation that will help in the planning of control strategies.

Description of the study area
Muleba district is among the six districts of the Kagera Region in Tanzania. The district is bordered to the north by the Bukoba Urban and Bukoba Rural districts, to the south by the Biharamulo District, to the east by Lake Victoria and to the west by the Ngara and Karagwe districts. The 2012 Tanzania population and housing census reported a total population of 540,310 (267,858 males and 272,452 females) across an area of 3,518 km 2 in Muleba district [15]. The residents of the Muleba district practice diverse economic activities, key among them being; farming, shing, livestock rearing and mining. The climatic conditions of Muleba district are warm and mostly cloudy. Over the course of the years, its temperature varies between 17°C and 26°C that favour the survival of intermediate snail host (Biomphalaria). Muleba district was selected because of the history of the high prevalence of intestinal schistosomiasis and inadequate level of water, sanitation and hygiene which favour transmission of intestinal schistosomiasis [13].

Study design and population
A quantitative cross-section study was conducted from July to August 2020. This sub-study was a part of a large project that aimed to assess the magnitude of geohelminths and associated factors among the adult population in the Muleba District. The study population was adults, both males, and females in the Muleba District.

Sample size determination and sampling procedure
The sample size for this study was calculated from a formula which is given by Creswell [16]. The sample size for this study was 383 adults from 383 households. The study participants were sampled through a three-stage cluster sampling technique. The rst stage involved a simple random selection of one endemic district whereby the Muleba district was selected. The second stage involved the selection of representative rural wards whereby out of the 11 endemic rural wards, 3 rural wards (Ikuza, Mazinga, and Nyakabango) were randomly selected. The third stage involved the selection of representative villages from the selected rural wards. From each rural ward, 2 villages were selected by simple random sampling whereby Chakazimbwe and Kasenyi villages were selected from the Ikuza ward, Kimoyomoyo and Mulumo villages were selected from Mazinga ward, and Msalala and Nyakabango villages from Nyakabango ward. The households in each village were selected randomly, and in each selected household, only one member was randomly chosen to participate in this study.

Sample collection and laboratory analysis
Prior to stool collection, study participants were oriented on the stool collection procedures. Then plastic containers with applicator sticks were labeled with identi cation numbers and distributed to study participants for them to provide 5g of a fresh stool sample. Stool samples were then collected and immediately xed with 10% formalin to preserve the eggs of S. mansoni and taken to the parasitology laboratory at the Muhimbili University of Health and Allied Sciences for examination. To determine the prevalence and intensity of S.mansoni, the samples were processed and examined for the presence or absence of eggs/ova. Stool samples were processed using formolether concentration (FEC) techniques and the positive samples were quanti ed by Kato-Katz (KK) technique as described in the World Health Organization (WHO) bench aids for the diagnosis of parasitic diseases [17].
Examination for the presence of S.mansoni eggs/ova were done using Olympus CX 31 microscope.

Questionnaire survey
A structured questionnaire developed in English and then translated to Kiswahili was administered to all adults included in this study by well-trained interviewer. The questionnaire aimed to collect data on the socio demographic characteristics, water, sanitation and hygiene practices of the study participants.

Inclusion and exclusion criteria
The inclusion criteria included all adults residing in the Muleba district and who agreed to participate in this study by signing the informed consent. Adults who were sick from schistosomiasis during stool collection, adults who used anthelminthic (praziquantel) within one month before the commencement of data collection, and who refused to sign informed consent were excluded from the study.

Ethical consideration
Ethical clearance was obtained from Institutional Review Board of Muhimbili University of Health and Allied Sciences (IRB#: MUHAS-REC-06-2020-309) before commencement of the study. Permission to conduct the study in Muleba District was requested from the local authorities. Participants were informed about the objectives, procedures, potential risks and bene ts of the study as well as individuals' right to withdraw from participation at any time during the study without negative consequences. Also, a written informed consent was sought from respondents after giving them su cient information. The participants who were found positive for S.mansoni were referred to the nearby health facilities for appropriate treatment.

Data analysis
The data was entered and analyzed using Statistical Package for Social Sciences version 22. All categorical variables were summarized to obtain the frequency and proportions. The prevalence of S.mansoni was calculated according to sex, age groups, village of residence and occupations. The intensity of S.mansoni was reported as the arithmetic mean of eggs per gram (EPG) and then categorized based on WHO classi cations for S.mansoni; (0) negative, (1-99) light infection, (100-399) moderate infection, (> 400) heavy infection [18]. The binary logistic regression test was done to determine the association betweeen independent variables (sociodemographic characteristics, water and sanitation variables) and dependent variable (prevalence of S. Manson infectioni). Pvalue less than 0.05 were considered statistically signi cant.

Results
Socio-demographic characteristics of study participant A total of 328 adults (response rate of 85.6%) from 383 selected households in the six selected villages consented to provide stool samples for intestinal schistosomiasis examination and participation in interviews. The participants' average age was 31.7 (± 8.6) years with the higher percentage (66.8%) fall under the young adults (18-35 years) group. Most of the participants were male (61.3%), shermen (36.6%), and attained primary school education level (61%) ( Table 1). Selected villages were either in the islands or located along the shore of Lake Victoria.

Water and sanitization condition of study communities
The majority of the participants (75%) have reported always have water available, with more than half of participants (59.1%) using unimproved water sources (unprotected dug wells, unprotected springs, and surface water). Also, the majority (83.5%) reported spending less than 30 minutes from their households to the water sources, queue for water collection, and return to their households. Of 328 households surveyed, 293 (89.3%) had toilet facilities. However, only (72.9%) were using the toilets (Table 2).

Schistosomiasis prevalence, intensity and associated factors
The overall prevalence of intestinal schistosomiasis (Schistosoma mansoni) was 11% as determined by FEC method. The prevalence was higher among participants from households without toilets, with rare availability of water and takes more than 30 minutes to fetch water. Also, the prevalence was higher in participants from households fetching water from improved sources and not using toilets (Table 3). intensity of infection reported that water is always available at his household but it's from an unimproved source. Also, reported to live in households with toilet facility but not using it (Table 3). Participants from households without toilet facilities had four times higher risk of S. mansoni infection compared to participants from households with VIP toilet facilities (OR = 4.10, p = 0.001) ( Table 3).

Discussion
Globally, schistosomiasis control solely based on the provision of praziquantel PC to school-aged children (SAC). SAC are targeted because they are considered as a group at higher risk of schistosomiasis infection [19]. Despite, more than 15 years of praziquantel distribution to the vulnerable population who are known to be the source of schistosomiasis transmission to the communities still, there is ongoing transmission even to the adult population which indicates the disease is still a public health problem in Kagera region (where Muleba district is located) [20]. The ndings of our study are in line with the results of the previous study conducted more than ve years ago, suggesting consistent Schistosoma mansoni transmission in Muleba [20]. The recorded prevalence indicates that the populations in the studied areas are at moderate risk of acquiring intestinal schistosomiasis [19]. The prevalence of S.mansoni infection among the adult population could be attributed to occupational exposure to schistosomiasis transmission risk factors. Many adult people in the studied areas were farmers and sherman at high risk of schistosomiasis infection as they are at a higher chance of being exposed to contaminated water and poor sanitation condition. The majority of infected participants had a light intensity of infection. The light intensity of infection indicates a low burden (morbidity and mortality) of infection [19].
Provision of PC was observed to reduce the rate of schistosomiasis prevalence in the short term and does not protect against subsequent infection (reinfection) especially in intestinal schistosomiasis [19,21]. Therefore, relying on PC and ignoring other control measures such as water, sanitation, health education, and snail control was found not su cient to interrupt schistosomiasis transmission. Unimproved water sources and sanitation facilities are important factors contributing to the persistent transmission of intestinal schistosomiasis [7]. Water availability and access in the six villages is not a problem, but the majorities are taking water from unimproved sources. However, our ndings show that there is no association between the water source and the prevalence of intestinal schistosomiasis. A similar result was reported in a study conducted in Kenya [22]. Prevalence of intestinal schistosomiasis is higher among participants in areas with di cult access to water (rare availability of water and using more than 30 minutes to fetch water) ( Table 3). The higher prevalence could be because many people with di cult access to water tend to do most of the water-related chores nearby water sources to reduce the water fetching workload (reduce the number of trips to carry water and carry water only for drinking and cooking). Among water-related chores that could result in fecal contamination of water sources and expose people to contaminated water include washing of soiled clothes, open defecation (contaminate water source through fecal washing during rain/ ooding), and hygienic bathing [8]. Surprisingly, we noted the higher prevalence of S. mansoni infections among participants from households using water from improved sources. However, this is possible as the transmission does not occur within the house rather than outside. Therefore, people may get infected during their socio-economic activities outside of their homes [8].
We found the type of toilet facility to be a signi cant factor for the transmission of intestinal schistosomiasis. Participants from houses without toilet facilities had a signi cantly higher prevalence of intestinal schistosomiasis compared to those from households with toilet facilities. In contrast to the ndings recorded in Kenya [22], our results showed that the prevalence of intestinal schistosomiasis is signi cantly associated with the household's type of toilet facility (Table 3). Despite availability of toilet facilities in most of visited households (pit latrines and VIP), majority of interviewed adults participants responded that they do not use toilets. Most of the non-toilet users preferred the use of bushes (open defecation). A study conducted in India reported that the main reasons why people do not use toilets are a preference to open defection, lack of privacy (feel shy), and use of sanitation facility (toilet) was considered inconvenient [23]. It was showed elsewhere that possibility of open defecation in farming communities is high due to lack of sanitation facilities in the farms [22]. Results from stool examination showed a slightly higher prevalence of S. mansoni among participants who do not use toilets compared to those using toilets for defecation. It could be because most people practicing open defecation preferred to do it in bushes surrounding water sources as these areas offer both privacy and water for hygienic bathing [8]. Defecating nearby water bodies and hygienic bathing in water bodies may contaminate the water with feaces contain Schistosomes eggs resulting in the perpetuation of schistosome transmission.

Conclusion
The results of this study show that the adult population in Muleba had a higher prevalence of S. mansoni and continue to act as a reservoir of the infection. More than 75% of Schistosoma infected participants are farmers and shermen, indicating occupational exposure. Therefore, adults and occupationally exposed populations have to be considered for inclusion in intervention campaigns. The majority of water sources in the studied areas are unimproved ones. Most of the surveyed households have improved sanitation facilities. Participants from the few houses without sanitation facilities bear the higher burden of the disease. Despite, the high coverage of sanitation facilities, people do not prefer to use them. The prevalence of infection is higher among non-toilet users. It gives an alert for a call on behavioral change intervention.