1 Introduction

Schistosomiasis infection is caused by trematode worms of the genus Schistosoma, which infect hosts primarily during contact with water [1]. The two predominant species of this genus endemic to the sub-Saharan region are Schistosoma haematobium and Schistosoma mansoni, the etiologic agents of urinary and intestinal schistosomiasis infections, respectively. The presence of snails, which serve as the intermediate host, and humans, the final host, is necessary for the transmission patterns of these illnesses. Each intermediate host is species-specific: Bulinus spp. is the intermediate host for S. haematobium, whereas Biomphalaria spp. is the intermediate host for S. mansoni [2].

Schistosomiasis infection is of public health importance because it is a widespread parasitic disease endemic to tropical and subtropical areas [3]. Schistosomiasis, also known as bilharziasis, remains one of the most neglected parasitic infections affecting the human population, particularly school-aged children [4]. The condition has been estimated to affect more than 230 million people globally, and 700 million people are at risk of infection [5, 6]. Most people affected by this parasitic infection live in the sub-Saharan region, where 85% of all annual cases are reported [3, 7]. Schistosomiasis infection ranks second to malaria in terms of the number of deaths, accounting for 280,000 deaths yearly [8, 9].

In Nigeria, both S. haematobium and S. mansoni have been reported, and the former is more widely distributed [10]. Approximately 29 million people have been estimated to have been infected with S. haematobium in Nigeria, whereas 101.3 million are at risk of the infection [11, 12]. The high prevalence of S. haematobium in Nigeria poses a public health problem, particularly in school-aged children between the ages of 5 and 15 years [10, 13], owing to their proclivity for engaging in domestic activities and frequent contact with contaminated water, such as through group swimming and fishing in snail-infested water bodies after school. Nigeria's communities frequently engage in these activities [14]. Most studies of schistosomiasis infections have focused on students in primary school, whereas few studies have been conducted on Almajiri students. These are school-aged children who attend “tsangaya,” informal Quranic schools, where they study the Holy Quran away from their homes under the supervision of an Islamic scholar. They are typically socioeconomically disadvantaged and engage in menial labor to supplement their income [15]. Because they are unsupervised, they may be more susceptible to diseases and infestations than elementary school students. The different river bodies in the Zaki Local Government Area (LGA) in Bauchi State may predispose residents to urinary schistosomiasis.

S. haematobium is responsible for multiple infections, such as hematuria, dysuria, nutritional deficiency, and growth retardation [9]. The high incidence of urinary schistosomiasis infections in Nigeria and other sub-Saharan nations, as with other parasite infections, are associated with a lack of safe drinking water, inadequate sanitation, poverty, and a lack of understanding of infection risk, particularly in rural areas [10, 16, 17]. Despite the danger posed and the high incidence of urinary schistosomiasis reported in parts of Nigeria, information on this infection in the present study area is scarce. Therefore, this cross-sectional study was conducted to determine the incidence of urinary schistosomiasis infection among formal and informal primary school pupils in the study area. In addition, the study assessed the risk factors contributing to the occurrence of infection.

2 Materials and Methods

2.1 Study Area

The research was performed in the Zaki LGA of Bauchi State. A cross-sectional study was undertaken between June and November 2021 to investigate the prevalence of urinary schistosomiasis infection among pupils in three primary schools. The area is geographically located between latitudes 11° 54′ 43" and 12° 31′ 30" North of the equator and longitudes 10° 09′ 25" and 10° 43′ 52" East of the Greenwich meridian, and occupies a total land area of 1476.72 km2 (Fig. 1). It has a sparse population. Rainy seasons span June to September, and are followed by dry seasons, which span October–March. Farming, fishing, trading, artisan work, and government service are among the most common economic activities in this locality. Basic infrastructure, such as electricity, good roads, and pipe-borne water are insufficient at numerous levels.

Fig. 1
figure 1

The study area

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2.2 Sample Size

The sample size for this investigation was determined with the Cochrane formula [18], with a prevalence estimate of 2.5% [19]:

$$N = Z^2 p (1-p)/d^2,$$

where Z = 1.96, p = 2.5% (0.025) is the prevalence expected according to a previous study, d is the precision or margin of the error (5%, d = 0.05), and N is the sample size. A minimum sample of 37.44 was calculated. However, the sample size calculated was adjusted to 300 as the baseline sample size of our study to avoid bias in the selection of the school children.

2.3 Sample Collection

Urine samples from 300 school children between the ages of 5 and 13 years in the study area were analyzed for the presence of S. haematobium eggs. The collection of urine samples occurred between 10 am and 2 pm, when the excretion is usually maximal [2]. Each student was given a clean plastic screw-capped 30 ml universal sample bottle and provided instructions for sample collection. The urine samples were labeled accordingly. For parasitological analysis, all samples collected were taken to the Department of Biological Sciences Laboratory, Bauchi State University Gadau for analysis.

Structured questionnaires were administered to the children to assess socio-demographic and determinant factors such as sex, age, parental occupation (of father), playing in shallow water, and fishing.

2.4 Sample Analysis

Centrifugation and sedimentation techniques were used to analyze the samples [20]. After 10 ml of urine was allowed to sediment for 1 h, it was centrifuged at 2000 rpm for 2 min. A drop of sediment was placed on a clean glass slide and covered with a coverslip after the supernatant was discarded. Microscopically, the sediment was examined with × 10 and × 40 objective lenses to identify S. haematobium eggs, as distinguished by a terminal spine. Urine samples containing S. haematobium eggs were classified as positive, whereas those without schistosome eggs were considered negative [20].

2.5 Data Analysis

All collected information was imported into Microsoft Excel 2019 and analyzed in SPSS version 24. The associations between the dependent and independent variables were evaluated with Chi-square, bivariate, and multiple logistic regression analyses. The strength of the association was determined with the odds ratio (OR) with a 95% confidence interval. P values less than 0.05 were considered statistically significant.

3 Results

3.1 Socio-Demographic Characteristics and Prevalence of Schistosomiasis

The incidence of urinary schistosomiasis among school children in the study area was 29.7%. Of the 300 school children enrolled, 100 (33.33%) were from each of the three primary schools (private, public, and Almajiri schools). The highest prevalence was observed in the Almajiri school (59.6%), followed by the public school (31.5%), whereas the private school had the lowest prevalence (9.0%). The observed differences in the prevalence of urinary schistosomiasis infection varied significantly (χ2 = 48.73, df = 2, P = 0.001) among the schools (Table 1).

Table 1 Socio-demographic features of the prevalence of schistosomiasis by school type, sex, age, and parental occupation in the study area
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A total of 216 boys and 84 girls were enrolled in the study. Urinary schistosomiasis infection was higher among boys (94.4%) than girls (5.6%). The observed differences in the prevalence of urinary schistosomiasis infection according to sex were statistically significant (χ2 = 31.44, df = 1, P = 0.001). We enrolled 90 students 5–8 years of age, 142 students 10–14 years of age, and 68 students 15 years of age or older. The highest urinary schistosomiasis infection rate was recorded among the 10- to 14-year-old age group (52.8%), followed by the 5- to 9-year-old age group (27.0%). The group 15 years and above had the lowest infection rate (20.2%). However, the results showed no statistically significant differences in the prevalence of urinary schistosomiasis among the age groups (χ2 = 1.52, df = 2, P = 0.47).

Most of the students' parents were farmers (175), followed by civil servants (71), and the fewest were traders (54). A high prevalence of urinary schistosomiasis was observed among children whose parents were farmers (71.9%), followed by traders (16.9%). The lowest infection rate was identified among children whose parents were civil servants (11.2%). Statistically significant associations between urinary schistosomiasis and parental occupation were observed (χ2 = 12.35, df = 2, P = 0.002), as shown in Table 1.

3.2 Risk Factors Associated with Urinary Schistosomiasis

Of the 300 children observed, 117 (39.0%) had a habit of playing in shallow water sources, and 108 (36.0%) engaged in fishing. Of the study participants, 46 (15.3%) had experienced itching, and 144 (48.0%) had observed blood in their urine. The recorded water sources were rivers, boreholes, and taps, whose domestic usage was 85 (28.3%), 99 (33.0%), and 116 (38.7%), respectively. Children who used a borehole as a water source had the highest infection rate (43.8%), followed by those who used rivers as a water source (39.3%). Meanwhile, children who used tap water as a water source had the lowest infection rate (16.9%). All risk factors were significantly associated with infection (P < 0.05), except itching symptoms (P = 0.90) (Table 2).

Table 2 Frequency of risk factors associated with urinary schistosomiasis among primary school children in Zaki, Nigeria
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3.3 Binary Logistic Regression and Multiple Regression Analyses

The binary logistic and multiple logistic regression analysis results for the factors associated with schistosomiasis infection are presented in Table 3. In the bivariate logistic regression analysis, male students [COR (95% CI): 10.05 (3.91–25.85)]; students attending public school [COR (95% CI): 4.47 (1.92–10.40)] or Almajiri school [COR (95% CI): 12.97 (5.69–29.51)]; children whose parents were farmers [COR (95% CI): 3.52 (1.69–7.34)] and traders [COR (95% CI): 2.35 (0.96–5.74)]; children who played in shallow water [COR (95% CI): 9.81 (5.51–17.46)] or engaged in fishing [COR (95% CI): 5.19 (3.05–8.83)]; children with blood in the urine (hematuria) [COR (95% CI): 8.18 (4.49–14.90)]; and children who used rivers [COR (95% CI): 4.71 (2.36–9.43)] and boreholes [COR (95% CI): 4.38 (2.23–8.60)] as a source of water were significantly more likely to have schistosomiasis infection. However, in the multivariable logistic regression analysis, only sex, play in shallow water, and blood in the urine were significantly associated with schistosomiasis infection. Multiple logistic regression analysis indicated that only male sex [AOR (95% CI): 8.12 (2.17–30.45)], playing in shallow water [AOR (95% CI): 5.14 (2.17–30.45)], and blood in the urine [AOR (95% CI): 9.64 (4.79–20.66)] were significantly associated with schistosomiasis infection.

Table 3 Bivariate and multiple logistic regression analyses of variables associated with risk factors for urinary schistosomiasis in the study area
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4 Discussion

The findings from the present study indicated that urinary schistosomiasis is endemic to the Zaki LGA in Bauchi State. The 29.7% prevalence of this infection observed among school children indicated moderate risk at the community level, according to the WHO definition [21]. The present study’s moderate prevalence of urinary schistosomiasis (more than 10% but less than 50%) reflect substantial residential exposure to contaminated water bodies.

The study area is characterized by small pond areas used for household activities, farming, and swimming. The observed prevalence of urinary schistosomiasis was lower than that in studies conducted in various parts of Nigeria, such as Ogun State (58.1%), southwestern Nigeria, Kwara (58.7%), and Benue State (55.0%), north-central Nigeria [11, 22, 23]. Similar findings have been reported in other regions of the world, including Senegal (57.6%), South Darfur (56.0%), and Mali (51.2%) [8, 20, 24]. However, other studies conducted in other parts of Nigeria, such as Maiduguri (northeastern), Anambra (southeastern), Dutsen-Ma (northwestern), and Kano (northwestern), have observed a lower prevalence of 14.5%, 15.7%, 17.3%, and 17.8%, respectively [6, 25,26,27]. A lower prevalence of urinary schistosomiasis has also been reported by other authors from different parts of the world, such as Gbalégba [3] in Mauritania, Ouedraogo [28] in Burkina Faso, Niangaly [29] in Mali, Kapito-Tembo [7] in Malawi, and Sudan [30], at 4.0%, 7.6%, 8.8%, 10.4%, and 13.8%, respectively. The difference in urinary schistosomiasis infection between the present and previous studies might be attributable to variations in geographical location and environmental factors across the countries [1]. The level exposure to water bodies contaminated with cercariae might also account for the variance in the prevalence rate.

The present study also indicated a statistically significant difference in the prevalence of urinary schistosomiasis infection according to sex. The multivariate logistic regression analysis indicated that boys were eight times more likely to be infected with urinary schistosomiasis than girls [AOR (95% CI): 8.12 (2.17–30.45)]. The high prevalence of urinary schistosomiasis infection in boys was believed to be due to their exposure to various water-associated activities, such as playing in shallow water and fishing. The findings from the present study strongly suggest that the aforementioned environmental risk factors are significantly associated with urinary schistosomiasis infection in the study area. Children who played in shallow water appeared to be at high risk of contracting schistosomiasis infection: they were five times more likely to be infected than those who did not play in shallow water [AOR (95% CI): 5.14 (1.97–13.37)]. Similarly, the low prevalence of the infection observed in girls was attributed to their low exposure status, because most girls stay close to their mothers at home and help with domestic chores.

This result is consistent with the findings observed by Bawa et al. [27] in Dutsin-Ma, Katsina State; Houmsou et al. [31] in Benue State; and Bello et al. [32] in Wurno, Sokoto State, who have reported a significant association between the occurrence of urinary schistosomiasis infection and sex. This finding is consistent with those from previous studies from various parts of the world, such as Zanzibar and South Darfur [20, 33] but contradicts the findings of other authors, such as Ekpo et al. [22] in Abeokuta, southwest Nigeria, and Bakhit et al. [34] in Khartoum, North Sudan, who have observed that girls had a higher prevalence rate of urinary schistosomiasis than boys.

Analysis according to different types of schools in the study area indicated that the prevalence of urinary schistosomiasis infection was higher among Almajiri school (informal school) children, at 54 (54.00%), followed by public primary school children, at 28 (28.00%). The lowest prevalence rate of urinary schistosomiasis infection was observed in children in private primary school, at 8 (08.00%). The higher rate of schistosomiasis infection found among Almajiri students than students at private and public schools indicated that education plays a major role in preventing or controlling infection. According to the current study, respondents whose father's occupation was farming were three times [COR (95% CI): 3.52 (1.69–7.34)] more likely to contract the disease than those whose fathers worked in civil service. This finding is consistent with those reported by Atalabi et al. [35] in Katsina State, northwest Nigeria. Peasant farmers are less likely to be literate than civil servants, on average. The high infection rate observed among the Almajiri pupils might also be associated with their lack of knowledge regarding the infection risk, inadequate living conditions, and poor personal and environmental hygiene.

The highest prevalence rate of infection observed in Almajiri school might be attributable to the lack of access to operational public tap water, thus compelling students to rely solely on open water sources. The finding that students at Almajiri school had the highest prevalence of urinary schistosomiasis infection, as compared with students at public and private schools, might have been because these students are typically underprivileged and left unattended, and consequently engage in more water-contact activities. The elevated infection rate might also have been associated with Almajiri schools enrolling only boys, who may tend to be mobile, bold, and likely to come into contact with infected water bodies.

Furthermore, this study found that water source plays a significant role in transmitting urinary schistosomiasis infection. The children who used boreholes and rivers as water sources had the highest infection rates. The high prevalence of schistosomiasis infection observed among children using boreholes as water sources was attributed to their exposure to other sources of water that might predispose them to infection, because boreholes are not open water sources that can be contaminated with S. haematobium. Children who use rivers as water sources were 4.7 times more likely to be infected with urinary schistosomiasis than those who used tap water [COR (95% CI): 4.71 (2.36–9.43)]. However, multiple logistic regression analyses indicated no associations between schistosomiasis infection and water source as a risk factor in the Zaki LGA of Bauchi State.

Factors such as playing in shallow water, sources of water, and fishing can make children susceptible to this infection if the water is contaminated with larval (cercarial) parasites. The larval parasites invade human skin that comes into contact with contaminated freshwater [36]. Another risk factor, blood in the urine among children in the study area, was associated with urinary schistosomiasis infection. Children who observed blood in their urine were nine times more likely to be infected than those who did not [AOR (95% CI): 9.64 (4.79–20.66)].

No significant relationship was observed among age groups, although the prevalence of urinary schistosomiasis increased with age. The highest occurrence of urinary schistosomiasis was found in the age group of 10–14 years (52.8%), in agreement with findings reported by Abdulkareem et al. [37] in Kwara, who observed a higher occurrence of schistosomiasis infection (49.4%) among school children between the ages of 11 and 14 years. This finding suggests that children in this age group engage in more water activities, such as playing in shallow water, swimming, and fishing, than the other age groups in the survey. A similar finding has been reported in Ebonyi State, southeast Nigeria and Plateau State, north-central Nigeria, where the highest prevalence of urinary schistosomiasis was observed among the 10- to 14-year-old age group [38, 39].

In agreement with these findings, Enugu State, southeast Nigeria has reported the highest prevalence of the infection in the age group of 13–15 years (52.8%), as compared with the younger group 5–8 years of age (24.2%) [40]. The higher urinary schistosomiasis infection rates recorded in the present study was also in agreement with findings reported by Angelo et al. [15] in Tanzania, in which children 12–14 years of age had the highest prevalence. However, these findings are contrary to those reported by Muhammad et al. [41] in Sokoto State, northwest Nigeria, where younger children were more at risk of being infected with schistosomiasis.

The exposure levels among different age groups of children might explain the differences in the prevalence of urinary infections. The high prevalence observed in school children 12–14 years of age in the present study might have resulted from an increase in the duration of water-associated activities involving contaminated water. Likewise, the lowest prevalence of disease observed in school children 5–8 years of age might have resulted from their lower exposure to water-associated activities.

Our study indicated that some socio-demographic and environmental factors are essential in transmitting this infection in the study area. The findings were in line with those from the previous reports from other parts of Nigeria [35, 42] and other countries [5, 20] where urinary schistosomiasis infection is endemic. However, the present study has several limitations, including a lack of measurement of the intensity of urinary schistosomiasis infection. Another limitation was the use of the sedimentation technique. Although the WHO has recommended this technique [20], its lack of sensitivity can result in underestimation of the prevalence of urinary schistosomiasis infection. Despite these limitations, this study indicated that urinary schistosomiasis infection among school children is endemic to the study area.

5 Conclusion

Our findings demonstrated a moderate prevalence of S. haematobium infection among primary school children in Zaki LGA, Bauchi State. Therefore, there is a need for mass chemotherapeutic intervention with praziquantel from the government and international agencies, particularly in Almajiri primary school children, to significantly decrease the prevalence rate of infection among school-aged children. In addition, a safe and potable water supply, and the need to maintain adequate hygiene conditions should always be advocated. These aspects are all important in maintaining appropriate health conditions.