Risk factors affecting the occurrence of urinary schistosomiasis and urinary tract infections in some communities of Ondo State, Nigeria

Schistosomiasis is the second most common socio-economically devastating parasitic disease after malaria (Akinneye et al. 2018), affecting about 240 million residents of developing countries. It is an acute and chronic disease caused by blood flukes of the genus Schistosoma. The World Health Organization (WHO) (2020) estimated that at least 220.8 million people required preventive treatment in 2017, while Lo et al. (2022) reported that schistosomiasis affects approximately 250 million people worldwide.

Nigeria has been reported to be the most endemic country in the world for schistosomiasis (Ajakaye et al. 2017; Nwele et al. 2017) and S. haematobium is widely spread mainly in riverine areas and communities around impoundment of river (dam) (Nwele et al. 2017).

The urinary tract is the second commonest site after the respiratory tract for bacterial infections (Ossai et al. 2014), with over 150 million cases per year (Ngong et al. 2021). Medina & Castillo-Pino (2019) reported that UTIs are the most common outpatient infections, with a lifetime incidence of 50–60% in adult women, and recurrence within 6 months is common. Glover et al. (2014) reported that between 25 and 35% of women do have a recurrence of UTI within 3–6 months. Urinary tract infection (UTI) is as a result of the presence of significant bacteria in urine. Significant bacteriuria is defined as a urine sample containing more than 10⁵ colonies/ml of urine in pure culture (Kehinde et al. 2011). Mixed infections of urinary schistosomiasis (US) and urinary tract infections (UTIs) caused by S. haematobium and bacteria respectively are reported among children in the tropics. Fincham et al. (2003) posited that bacterial infections normally take place when the mucosal barrier is broken down making the urinary tract an easy target for invading bacteria. The breakdown of the urinary tract mucosa can be as a result of the spiny eggs of the schistosomes.

Since both the presence of S. haematobium and bacteria in the urinary tract affect the normal functioning of the urinary tract and there have been studies that observed that people with urogenital schistosomiasis have higher rates of bacterial UTI than expected (Hsieh et al. 2014). It is, therefore, of great importance to study the association of the parasitic disease with bacterial infection, as this may in turn lead to increased cases of bladder cancer if co-treatment is offered to none of the cases. This study aimed to identify and evaluate the risk factors involved in US and associated bacterial infection in some communities of Ondo State, Nigeria.

The study was a part of a larger survey conducted among the dwellers of the selected communities viz: Ayede Ogbese in Akure North Local Government Area, Ita-Oniyan and Aponmu in Akure South Local Government Area, and Ipogun in Ifedore Local Government Area, all in Ondo State Nigeria. The selection of these communities was based on information from the Ondo State Primary Health Care Development Agency, that US was endemic in the study areas. These are rural communities that lived mainly on farming but Ogbese, a more populated community engages in other commercial activities like buying and selling in addition to farming. Apart from farming, some of the women engaged in local production of palm oil which made them have contact with the Schistosoma infested rivers regularly. The economic activities of the people include fishing, palm oil production, and cultivation of food and tree crops like cocoa, oil-palm, cashew, rubber, teak, gmelina, and different species of indigenous trees. These communities under study have rivers and streams that pass through them. River Ogbese is found in Ogbese, River Awo in Ita-Oniyan links up with the Aponmu community, and River Aponmu in Ipogun links up with Aponmu community. The inhabitants of these communities also use rivers as their source of water for recreational and domestic purposes.

Free and informed consent of the participants was obtained and the study protocol was approved by the Ethical Committee of the Ondo State Ministry of Health Akure, Ondo State, Nigeria on 3rd September 2018.

A structured questionnaire which covered the socio-demographic information and risk factors for US and UTIs was administered to the participants that consented to participate in the study by us. The questionnaires covered age, gender, marital status, educational background, occupation, religion, history of hospital admission, prior knowledge of UTI and schistosomiasis, history of painful urination, passing bloody urine, waist pain, having contact with the infected water, and duration of contact with the water. The study was carried out between September 2018 and October 2019.

Data generated were entered into a Microsoft excel spreadsheet of version 2010 and then analysed using Statistical Package for Social Sciences (SPSS) version 23.

Results were presented in form of tables and charts. Crosstabs and Pearson Chi square test was applied to assess the significance of the risk factors for schistosomiasis and UTI, and statistical significance was ascertained at p ≤ 0.05.

Of the five hundred and nine (509) participants, 246 (48.33%) were females (Table 1). The occurrence rates of 23.77 and 20.43% were recorded for US and UTI, respectively, while a 7.07% occurrence rate was reported for co-infection of both UTI and US. This has been reported in our previous studies that considered the occurrence of US and associated bacteria in part of Ondo State, Nigeria (Kone et al. 2022). In other words, 13.36 and 16.7% of the participants had UTI in non-schistosomiasis cases and US in non-UTI cases, respectively. From the same study, as portrayed in Tables 2 and 3, US was gender- and age-dependent (X²(1) = 23.934, p = 0.000) and (X²(7) = 85.991, p = 0.000), respectively, while UTI was not age- and gender-dependent (X²(7) = 6.577, p = 0.474 and (X²(1) = 1.086, p = 0.297), respectively. However, co-infection was age and gender significant (X²(7) = 22.008, p = 0.003) and (X²(1) = 4.901, p = 0.027), respectively (Table 2).

Occupation was significant for schistosomiasis but not significant for UTI (Table 4). Two hundred and thirty four (234) of the participants were students, and 90 of the 234 students had ova of S. haematobium. Passing bloody urine was equally significant for schistosomiasis (X²(1) = 112.440, p = 0.000), but it was not significant for UTI (X²(1) = 3.530, p = 0.060). Meanwhile, co-infection in relation to educational background and occupation of the participants was not significant (p = 0.156 and 0.544, respectively). However, schistosomiasis in relation to having prior knowledge of schistosomiasis was significant (p = 0.005). Another important factor was the duration of contact with the infected water bodies that was significant (X²(19) = 93.593, p = 0.000) and (X²(19) = 36.618, p = 0.009) for schistosomiasis and UTI, respectively. It was also established in our larger study (Kone et al. 2022) that US was gender-dependent (p = 0.000), but UTI was not dependent on gender (p = 0.297).

Further analysis to consider the correlation between the variable revealed that a positive relationship existed between the duration of contact with the water bodies and schistosomiasis, as many of them spent from 5 min to 3 h in the infected waters. Also, the relationship between the age group and UTI was a positive one while the relationship that existed between educational background of the participants and co-infection was a negative relationship. Gender was discovered to be a risk factor for schistosomiasis as the highest number of cases of schistosomiasis were males and this report was in consonance with the outcome of the study conducted in Ghana (Cunningham et al. 2020) and Gambia (Joof et al. 2021). Table 2 revealed that the highest cases of schistosomiasis were found among the school-aged children, i.e. 0–9 and 10–19 years. This corroborated the reports from various authors that have reported similar cases from different parts of the country (Abdulkareem et al. 2018; Akinneye et al. 2018; Noriode & Mafe 2018).

Findings also revealed that children of age ≥10 years were more infected among school-aged children and this was in agreement with previous reports (Sady et al. 2013; M'Bra et al. 2018), that children of age ≥10 were more infected than children of age ≤10 years. These age groups comprise of very active young people that are often involved in swimming, sporting, and fishing in rivers. This translated to mean that 74.38% cases of schistosomiasis in the communities were children of school age and 13.2% were artisans. Educational background of the participants as seen in Figure 1 in which 43.4 and 39.9% had primary and secondary education, respectively, while only 5.7% had tertiary education was a risk factor because the people that are not informed would definitely be deformed. In other words, 95.04% of the cases of schistosomiasis were people with only primary (63) and secondary (52) education.

A regular visit to the infected water was a major risk for both schistosomiasis and UTI. This result agrees with the findings of Nyati-Jokomo & Chimbari (2017) in which frequent contact with unprotected water was a factor for schistosomiasis transmission in Zimbabwe. Also, the report of Hajissa et al. (2018) corroborated the findings as they recorded activities that link people with water to be relatively associated with the infection. In addition, the reports of the study conducted by Angora et al. (2019) and Amuta et al. (2020) lend credence to the fact that swimming and fishing which are activities that predispose one to have long hours of contact with water are risk factors for schistosomiasis transmission. Knowledge of schistosomiasis was not hidden from the participants as 419 (82.32%) out of the total 509 had prior knowledge of schistosomiasis, unlike the participants of the research from Zimbabwe by Nyati-Jokomo & Chimbari (2017) in which the people were not informed. It is, therefore, evident that having knowledge of the disease did not stop the people from visiting the rivers.

For UTI, the presence of schistosome eggs was a predisposing factor because Uneke et al. (2009) posited that factors that can cause impairment in the defense mechanism that maintains the sterility of the normal urinary tract, are risk factors. The eggs caused wear and tear of the epithelium lining of the urinary tract thereby exposing it to bacterial invasion. Majority of the participants, even those that tested negative for schistosomiasis during the previous study, had at one time or another been infected by schistosomes but got treated through the government intervention of annual mass drug administration. Though schistosomiasis was treated, the UTI that developed as a result of schistosomiasis lingered on as it remained untreated. Another factor that was established as a risk factor for UTI was contact with water as it was significant (X²(1) = 4.577, p = 0.032). However, there is a dearth of information about the relationship that exists between UTIs and infected water. Boston Urogyn (2022) reported that swimming-related activities are the major risk factor for developing a UTI in the summertime. Because sitting around in a wet swimsuit can allow bacteria to grow, and the bacteria may find their way into the urinary tract, thereby causing infection. A lot of the bacteria present in the infected water could gain assess into the genitalia and attach themselves, ascend into the urethra and the bladder.

The risk factors involved in the development of schistosomiasis in the communities where gender as males were more prone to the disease than females. Age was another risk factor as it was discovered that children of age ≥10 were more infected than the older age groups. It was equally noted that 38.46 and 24.36% of the students and 28.07 and 15.79% of the artisan tested positive for US and UTI respectively. In addition, contact with the infected water and the duration of contact with water was among the predisposing factors to schistosomiasis and UTI because the longer the time spent in the waters, the higher the risk of contacting the infections.

We appreciate all the Community Heads of the study areas for their cooperation and special thanks go to Dr S. O. Oladejo, of the Department of Remote Sensing and Geographical Information System, School of Earth and Mineral Science, Federal University of Technology, Akure, Ondo State, Nigeria for his technical support.

The authors received no specific funding for this work.

All relevant data are included in the paper or its Supplementary Information.

The authors declare there is no conflict.