Prevalence of Intestinal Parasites and Schistosoma mansoni and Associated Factors among Fishermen at Lake Tana, Northwest Ethiopia

Background Intestinal parasites and Schistosoma mansoni infections adversely affect the health of humans in the world especially in sub-Saharan African countries including Ethiopia. Fishermen who spend most of their time in water bodies are supposed to be at high risk of schistosomiasis and other water-born parasites. However, the magnitude of these parasitic infections and their determinant factors are not well addressed. Methods A cross-sectional study was conducted at Lake Tana among 388 fishermen from March to May 2021. Questionnaire data was collected through face to face interview. Stool sample from each participant was processed by the Kato-Katz and spontaneous tube sedimentation techniques. Data were analyzed using SPSS version 26. Results One hundred sixty four (42.3%) and 88 (22.7%) participants were infected by intestinal parasites and Schistosoma mansoni, respectively. One hundred twenty two (31.4%) and 42 (10.8%) participants were infected by soil-transmitted helminths and intestinal protozoa, respectively. Attending only primary school (AOR = 2.02, p = 0.014) or being illiterate (AOR = 2.54, p = 0.004) and not washing hands before meal (AOR = 2.23, p = 0.007) were significantly associated with intestinal parasitic infections. Illiterate educational status (AOR = 2.37, p = 0.022), fishing by bargee (AOR = 2.43, p = 0.005), fishing ≥4 days per week (AOR = 2.27, p = 0.029), swimming habit (AOR = 3.03, p = 0.030), and participation in irrigation (AOR = 3.09, p ≤ 0.001) predispose fishermen to S. mansoni infection. Conclusion Intestinal parasites and S. mansoni infections are highly prevalent among fishermen at Lake Tana basin. Low education level and frequent water contact predispose fishermen for intestinal parasites and S. mansoni. Therefore, health education to fishermen on intestinal parasites and S. mansoni infection and regular deworming should be advocated.


Introduction
Intestinal parasitic infections (IPIs) are major public health problems in developing countries [1]. An estimated 3.5 billion people are infected, and 450 million people are ill due to intestinal parasites (IPs) worldwide [2]. Among the intestinal helminth, soil-transmitted helminths (STH) comprising Ascariasis lumbricoides, hookworms, and Trichiuris trichiura accounted the highest prevalence in sub-Saharan Africa [3,4]. Lack of proper sanitation and hygiene, the habit of eating raw vegetables and not washing hands before meal, lack of provision of safe water, open defecation, and insufficient health care are the risk factors for the high prevalence of IPIs [1,2,5,6].
Not only IPIs but also schistosomiasis, caused by the genus Schistosoma, is the most neglected parasitic diseases in sub-Saharan countries. Schistosomiasis affects over 250 million people, and 780 million people are at risk of infection worldwide, of which more than 90% of the infections occur in Africa notably in sub-Saharan Africa [7][8][9]. The global disease burden of schistosomiasis is estimated to be 3.5 million disability-adjusted life years lost [8,10]. S. mansoni and S. heamatobium are the two species found in Ethiopia with S. mansoni being the most prevalent species in the country [11,12]. In Ethiopia, about 5.01 million peoples are infected and 37.5 million are at risk of the disease schistosomiasis [11,13]. Fishing and irrigation activities, existence of snails, washing clothes and fetching water in infested water, open defecation practice, and being fishermen are the predisposing factors for schistosomiasis [7,8,[13][14][15][16].
Fishermen who are performing their day to day activities in the water bodies are believed to be at high risk of S. mansoni infection. In the present study area, there are many people who are living by fishing in Lake Tana which is a potential infectious area for schistosomiasis. In addition, open defecation is a common problem around the Lake where fishermen are performing their daily activities due to the absence of community latrine. Possibility of acquiring IPs and S. mansoni infections is expected to be high due to the above risk factors; however, there is a scarcity of information about IPs and S. mansoni infection rate and their associated factors among fishermen who are working in Lake Tana. Therefore, the aim of this study was to assess the prevalence and associated factors of IPs and S. mansoni infections among fishermen in Bahir Dar zuria and Dera district kebeles bordering the Lake Tana.

Materials and Methods
2.1. Study Design, Area, and Period. A cross-sectional study was conducted in Bahir Dar zuria and Dera district kebeles around the Lake Tana basin from March to May 2021. Bahir Dar zuria district is located around Bahir Dar town, the capital city of Amhara Regional State, 565 km northwest of Addis Ababa. The mean altitude of the district is 1,800 m above sea level and the temperature of the district ranges from 10 to 32°C with annual rainfall of 800-1250 mm [17,18]. Dera district is located in South Gondar administrative zone, 602 km away from Addis Ababa. The mean altitude of the district is 2077 m above sea level. The area's mean annual rain fall and mean annual temperature were 1300 mm and 26°C, respectively.

Sample Size Calculation and Selection of Study
Participants. The sample size (n) was calculated using single population proportion formula. Since there is no previous data conducted in the study area, we used a prevalence of 50% (p = 0:5), 95% confidence level (Z α/2 = 1:96), and 5% margin of error (d = 0:05) to calculate the sample size.
After adding 10% (38) for nonrespondents, the final sample size was 422. Among the nine districts bordering Lake Tana two districts (Bahir Dar zuria and Dera district) were selected by simple random sampling technique. The study participants in each district were proportionally allocated by considering the total number of fishermen in each district. So, 308 fishermen from a total of 598 fishermen from Bahir Dar zuria district and 114 fishermen from a total of 220 fishermen from Dera district were included. Study participants were selected by systematic random sampling technique from the sample frame of the lists of fishermen in the fishermen association registration book. Fishermen in Bahir Dar zuria and Dera districts who were actively engaged in fishing activities for the last six weeks during the study period and volunteered to participate were included in the study. Fishermen who had taken treatment for intestinal parasites and S. mansoni infection two months prior to or during the data collection time were excluded from the study.

Data Collection and Processing.
A structured questionnaire was used to obtain data on sociodemographic characteristics and factors associated with IPIs and intestinal schistosomiasis by trained laboratory technicians. Approximately, five grams of fresh stool sample was collected using labeled, clean, dry, and leak-proof container in a nearby toilet. The stool specimen was transported to Bahir Dar University, College of Medicine and Health Sciences, parasitology laboratory following specimen transport guideline for parasitological examination. The stool specimen was processed using the Kato-Katz (KK) and spontaneous tube sedimentation techniques (STST).
In STST, approximately three grams of fresh stool sample was weighed and homogenized in 10 ml of normal saline solution. The mixture was filtered through surgical gauze into a 50 ml falcon tube, and more saline solution was added up to 50 milliliters. Then, the falcon tube cap was tightly closed and shaked for 30 seconds and left to stand for 45 minutes. The supernatant was discarded; the sediment was taken by a Pasteur pipette, and duplicate smears were prepared and examined microscopically for any parasite stages detected from stool [19].

Quality
Control. Before data collection, training was given to data collectors about data and stool sample collection protocols. Pretest was conducted among 22 participants (5% of the sample size) in order to check the validity of the questionnaire and laboratory-based data collection process. Standard operating procedures were followed during stool specimen collection, transportation, processing, examination, and recording. Each smear was examined by two laboratory technicians, and discordant results were resolved after  (Table 4).

Factors Associated with Intestinal Parasitic
Infections among Fishermen. In the multivariate logistic regression, the odds of IPIs among fishermen who attended only primary school was 2.02-fold (AOR = 2:02; 95% CI: 1.16-3.55, p = 0:014) higher than those who have attended secondary school and above. The odds of IPI among fishermen who were illiterates was 2.54 times (AOR = 2:54; 95% CI: 1.35-4.77, p = 0:004) higher than those who have attended secondary school and above. The odds of IPI increased by 2.23 times (AOR = 2:23; 95% CI: 1.25-3.96, p = 0:007) in participants who do not wash hands before meal as compared to those who wash their hands before meal (Table 5).

Discussion
Intestinal parasitic and S. mansoni infections are common problems in many developing countries including Ethiopia. In the present study, the overall prevalence of IPs among fishermen at Lake Tana was 42.3% which is higher than a previous result of 4.1% in Burkina Faso [21]. However, the    [22], 51.3% in Addiremets town [23], and 50.2% Abaye Deneba [24] all from Ethiopia. The difference in prevalence reports might be due to variations in age of study participants and sample size. About 54.7% and 48% of participants in studies from Jimma [22] and Abaye Deneba [24] were children, respectively, who are more exposed to IPs than adults due to poor sanitation.
Intestinal protozoan parasite infections are common in areas where poor sanitation and hygiene are practiced. In the present study, the prevalence of E. histolytica/dispar and G. lamblia was 7.5% and 3.6%, respectively. This is higher than a study finding in Addiremets town [23]. This might be due to differences in laboratory techniques as the previous study used direct microscopy whereas STST which has higher sensitivity is used in the present study.
The prevalence of STHs (31.4%) in the present study is higher than a study report of 26.5% in Addiremets town [23], but lower than prevalence of 67.3% from Bushulo vil-lage, southern Ethiopia [25]. The variation might be due to the difference in hygiene and sanitation that facilitates the transmission of the infection. The prevalence of hookworm (19.6%) in the present study was in consistent with prevalence of 23.1% in Addiremets town [23] but lower than findings of 43.3% from Uganda along the Lake Victoria [26]. On the other hand, hookworm prevalence in the present study was higher as compared to results from Hawassa (5.76%) [16] and Abaye Deneba (0.4%) [24]. These differences might be due to the variations in the frequency of soil contact and shoe wearing habit. Variations in the diagnostic approach might also be attributive for differences in prevalence across studies. For instance, three morning stool samples were collected and examined in the previous study from Uganda whereas single stool sample was collected and examined in the present study.
Infection frequency of A. lumbricoides (11.9%) in the present study was higher than study findings of 8.3% from Abaye Deneba [24] and 3.4% in Addiremets town [23], but  [16]. This difference might be due to variations in hygiene and sanitation of study participants and endemicity of A. lumbricoides.
Schistosomiasis is one of the most challenging parasitic infections in resource-limited countries. The prevalence of S. mansoni in the present study was 22.7% which is comparable with 26.3% prevalence from Addiremets town [23], 26.3% in Jimma [22], and 26.6% in Egypt [27]. This result was also higher than the results of 13.9% obtained from Brazil [28] and 16.35% in Burkina Faso [21], but lower than 29.21% prevalence in Hawassa [16], 41.3% in Abaye Deneba [24], 47.85% in Tanzania [29], 88.6% in Uganda Mayuge district [26], and 57.2% in Mukono district of Uganda [30]. The variation might be due to differences in laboratory techniques used, the variations in S. mansoni and snail distribution and fish catching places in Lakes. For instance in the present study, the majority of fishermen catch fish far from the border of the lake despite infection of cercaria mainly takes place near the border.
In the present study, the mean EPG of A. lumbricoides among fishermen was 1352.15 which was comparable with 1349.04 EPG from Hawassa [16], but lower than 5292 EPG in Addiremets town [23]. The mean EPG of hookworm species in the present study was also 116.13 which is higher than findings of 99.36 EPG from Hawassa [16] and lower than 563 EPG from Addiremets town [23]. The intensity of S. mansoni infection in the present study (171.91 EPG) is higher than previous findings of 158.88 EPG from Hawassa [16], but lower than 218 EPG from Addiremets town [23], 236.2 EPG from Uganda [26], and 183.21 EPG from Tanzania [29]. This difference might be due to differences in the endemicity parasites, treatment seeking behavior, and working environment.
In present study, being illiterate (p = 0:004) and attending only primary school (p = 0:014) were significantly associated with the prevalence of IPIs among fishermen. This report is in agreement with previous findings from Nahavand, Western Iran [31]. Infections of IPs among fishermen who did not wash their hands was also higher than those who washed their hands before meal, which is consistent with previous study reports [5,32]. This can be justified as educated people will have better awareness about the transmission and prevention of IPs.
In the present study, S. mansoni infection among illiterate fishermen was higher than those who have attended high school and above. This finding is supported by a previous study report in Uganda which shows S. mansoni infection increased with declining education level [33]. This might be due to low level of knowledge or awareness on the transmission of S. mansoni among illiterates.
Schistosomiasis is a water-based disease transmitted by direct contact with cercaria infested water. Fishing by bargee increases the odds of S. mansoni infection by 2.08-fold than fishing by boat. This might be due to the possibility of frequent water contact while fishing. Because the bargee cannot protect water from squeezing to inside part of the bargee. In the same way, fishing ≥4 days per week and swimming habit in Lake Tana in this study were also significantly associated  [16]. In the present study, the odds of S. mansoni infection among fishermen who participated in irrigation was 3.09 times higher than those who did not participate in irrigation. This finding is consistent with a study conducted in Hintallo-Wejerat, North Ethiopia [34]. This could be justified as our skin might be exposed to cercarial stage of S. mansoni during collecting water from the Lake and performing the irrigation activities with barefoot and bare hands. Assessment of the IP and S. mansoni infection status among fishermen in Lake Tana for the first time is the strength of the present study, while failure in detecting the source of infection, sanitary status in and around the lake was the limitations.
In conclusion, the prevalence of IPs and S. mansoni infection is high among fishermen at Lake Tana. Most of the infections of S. mansoni, A. lumbricoides, T. trichiura, and hookworm species were with light intensity. Being illiterate or attending only primary education and having no hand washing habit before meal are significantly associated with IPIs. Being illiterate, fishing by bargee, fishing ≥4 days per week, swimming, and participating in irrigation activities are independent predictors of S. mansoni infection. Therefore, health education on IPs and S. mansoni infection transmission and prevention, and regular deworming to fishermen should be advocated among fishermen along the Lake Tana Basin. Further studies are recommended to assess the source of infection for fishermen and sanitary status around Lake Tana.

Data Availability
The original data for this study is available from the corresponding author.

Ethical Approval
Ethical clearance was obtained from the Bahir Dar University College of Medicine and Health Sciences institutional review board (Protocol number: 151/2021). Permission letter was obtained from the Amhara Public Health Institute, and support letters were obtained from West Gojjam and south Gondar zonal health departments; Dera and Bahir Dar zuria district health offices. The results of participants were kept confidential. Fishermen infected with any intestinal parasites and S. mansoni were linked to the nearby health institution for treatment.