Parasitic infections constitute a major health problem worldwide, especially for countries in tropical or subtropical regions. These infections are caused by helminths and protozoa while a variety of conditions contribute to the prevalence of parasitic diseases, such as unsanitary living conditions, inadequate disease control, lack of health education, regional and ethnic customs conducive to parasitic infections, climatic conditions, and compromised immune systems among others [1,2]. Schistosomiasis is a water-borne trematode infection. Humans are usually infected by contact with contaminated fresh water, such as during water collection, washing, bathing, playing, fishing, or cultivating crops, and suffer from hematuria and anemia, enlargement of the liver and spleen, and growth retardation [3]. More than 206.4 million people required preventive chemotherapy for schistosomiasis in 2016, and approximately 200,000 deaths occur due to schistosomiasis globally each year [4]. Sudan is one of the most highly prevalent countries for schistosomiasis worldwide. There have been several epidemiological surveys of schistosomiasis from Sudanese school aged children in the River Nile State [5,6], southern Sudan [7], Central Sudan [8], South Kordofan State [9], and White Nile State [10–12]. However, epidemiological surveys of schistosomiasis in village residents are rare.

Intestinal helminthiasis is the most common infections in developing countries including sub-Saharan Africa and East Asia. Intestinal helminthiasis is mainly caused by consumption of contaminated water, infected soil, and inadequate sanitation and hygiene [1]. Moreover, a lack of access to facilities for safe disposal of human waste can result in intestinal helminthiasis and disease [13]. High prevalence of intestinal helminthiasis was reported among school children in sub-Saharan African countries [1,13,14]. However, only a few reports were conducted on the prevalence of intestinal helminthiasis in Sudan [6,15,16]; it is also especially difficult to obtain information regarding the infection status of intestinal helminths among village residents in the rural river basin area.

Sudan has wide river basin areas because of the crossings of the Nile Rivers and a large irrigated agriculture sector along the river banks. Due to this geographical environment, schistosomiasis has affected the people of Sudan for centuries. Intestinal helminthiasis may also be prevalent because of the lack of sanitary facilities at rural villages. On account of the lack of reports on schistosomiasis and intestinal helminthiasis in village residents living at the rural river basin area, we conducted this study to investigate the infection status of Schistosoma species and intestinal helminths among village residents of the rural river basin area in Sudan’s White Nile State according to gender, locality, and age groups.

Schistosomiasis is the second most common neglected tropical disease (NTD) after soil-transmitted helminths (STH) infections in sub-Saharan Africa. Sudan is also located in sub-Saharan Africa and human schistosomiasis is of considerable public health importance in the country. In school children-based surveys of schistosomiasis in Sudan, the prevalence of S. haematobium and S. mansoni infections were 73% and 70%, respectively, in the Upper Nile region [7] and 23.7% and 0%, respectively, in South Kordofan State [9]. In White Nile State, egg positive rates of S. haematobium and S. mansoni were 45.0% and 5.9%, respectively [11], and were 28.5% and 0.4%, respectively [12]. Community-based studies in Sudan reported that the prevalence of S. mansoni infections was 27.4% in villagers of the New Halfa Agricultural Scheme of Kassala State, but no data on S. haematobium was provided [18]. These results indicate that there is a wide variation in the distribution of Schistosoma species and schistosomiasis prevalence depending on survey sites. The variations may be explained by variable ecological conditions of surveyed sites, socioeconomic conditions of the surveyed populations, control programs implemented, the study design itself, and so on. In the present study, the prevalence of S. haematobium and S. mansoni infections was 35.6% and 2.6%, respectively, in the White Nile River basin area. Throughout the Nile basin of Sudan, S. haematobium is predominantly transmitted compared with S. mansoni [9–12]. Across Sudan however, S. mansoni infections were more prevalent in the Kassala State only [18]; this difference may be due to the snail ecology of Kassala State. Furthermore, compared with the reported prevalence in the White Nile State, our study provided S. haematobium infection rates of 49.6% in the ≤15 age group, which was higher than the previous reports of 21.4% [10], 45.0% [11], and 28.5% for school children [12]. Moreover, our reported prevalence of S. haematobium infection among village residents (35.6%) was higher than the 14.0% previously reported [19] for villagers in the White Nile State. These findings suggest that village residents—both children and adults—in these 2 rural river basin areas have been continuously in contact with S. cercariae-contaminated water despite the control measures that have been implemented in the White Nile State.

The current study demonstrated that the prevalence of schistosomiasis was higher in men and individuals ≤15 years old than in women and individuals >15 years old. This finding agrees with several previous studies conducted in endemic areas [5,12,18,20]. The association between gender and schistosomiasis may be attributed to religious and sociocultural reasons or to water contact behavior. In Sudan and many other Muslim countries, women are prohibited from bathing in open water sources, whereas the men frequently play and swim during their leisure time and thus schistosomiasis prevalence among men is significantly higher [5,12,18,21,22]. However, some studies have reported no significant differences between the genders because women are also responsible for fetching water and washing clothes and utensils at these water sources and thus have similar exposure to men [10,11,23]. Meanwhile, according to the stratified age groups, higher schistosomiasis prevalence was observed for those ≤15 years old, which includes pre-school and school-aged children. This finding is consistent with previous reports from different endemic areas [5,10,20]. In most endemic areas, schistosomiasis prevalence increases with age up to 10–15 years old, followed by a decline in older ages [5,20]. This could be explained by the fact that children of this age are more mobile and often go into the water near the village either to assist their parents in agricultural activities or to swim and play in the canals, which are likely to be contaminated with infective stages of schistosomiasis or other parasitic diseases [5,11].

In this study, we also compared the infection status of Schistosoma species between the Al Hidaib and Khour Ajwal villages, which are neighboring rural communities adjacent to the White Nile River and have very similar ecological conditions. However, our reported prevalence of schistosomiasis in Khour Ajwal was significantly higher than in Al Hidaib. This may be due to several factors; one critical difference is that a large, clean water supply system was installed in the Al Hidaib village and has been in use for many years, whereas there is no clean water supply system for Khour Ajwal and thus residents used river water. Consistent with our results, a previous study also reported that a facility for clean drinking water in Al Hidaib contributed to the improvement in health and life quality of the village residents by preventing waterborne diseases, including schistosomiasis [12]. Furthermore, the use of water purification systems was critical in reducing Cryptosporidium infections, a type of water borne pathogen, among inhabitants [16].

Infection intensity is a better indicator of morbidity than schistosomiasis prevalence because disease progression is associated with the daily deposition of parasite eggs into host tissues [8,24]. In this study, we used urine sedimentation method to detect and quantify the S. haematobium eggs. That is why urine filtration system is blocked easily due to many foreign substances in the urine collected at the survey sites (such as fallen bladder cells and so on, and the associated paper is Reference [19]), and it is higher detectability even if low number of parasites, and it is also economic than urine filtration method. According to previous reports from Sudan, the intensities as mean EP10 of S. haematobium were 12.9 in White Nile State [10], 25.5 in South Darfur [25], 87.7 in Central Sudan [8], 55 in White Nile State [11] and 40.1 in River Nile State [5]. In the present study, the intensity average geometric mean, median, and mean±standard deviation (SD) were 18.9, 20, and 67.78±119.49 EP10 (range, 2–800 EP10), respectively, in S. haematobium-infected individuals and 71% were light infections (EP10<50). Compared with the previously reported intensities of urinary schistosomiasis in Sudan, our results were similar or little less with those for the White Nile State [10,11]—albeit exact comparisons are difficult to achieve. We also analyzed S. haematobium infection intensities according to gender, locality, and age group and found that the tendency of S. haematobium infection intensities was in line with prevalence by gender, locality, and age group. The intensity geometric mean of men (22.2 EP10) was significantly higher than that of women (17.0 EP10), which was consistent with other reports [5,26]. On the other hand, Afifi et al. [18] reported that the intensity of S. mansoni infections among women (293.4 EPG) was higher than in men (187.6 EPG), although prevalence of infection among men (41.4%) was much higher than for women (13.9%). Moreover, based on age groups, we found that the intensity geometric mean of individuals ≤15 years old (20.2 EP10) was significantly higher than for individuals >15 years old (12.9 EP10). However, it was reported that high S. mansoni infection intensity was present in the age groups 31–40 and >50 years [18].

Intestinal parasitic infections constitute a major health burden in many developing countries. People of all ages can be affected by intestinal parasitic infections, with an increased risk for school children [1,27]. Apart from causing morbidity and mortality, infections with intestinal parasites have considerable impact on normal development, well-being, and the cognitive and educational performance of school-aged children [1]. According to previous studies conducted in Sudan, the prevalence of intestinal helminths was 2.7% in Khartoum State [28], while infection rates of H. nana were 32.6% in Khartoum State [15]. In the present study, the overall prevalence of intestinal helminthiasis was 7.7%, which was higher than the report of pre-school-aged children in Khartoum State [15]. And we found 5 different species of intestinal helminths including S. mansoni, which was the similar number of helminth’s species reported by Babiker et al. [28]. We found that the highest prevalence among intestinal parasitic infections was H. nana infections (6.6%). H. nana commonly infects both humans and rodents and can have an epidemiologically significant impact in family units, because it is the only tapeworm that can be directly transmitted between humans and auto-reinfection is possible [15,29]. Our reported H. nana infection rate was higher than for food handlers (1.6%) [28] and much lower among pre-school-aged children (32.6%) [15] in Sudan. These variations may be due to differences in climatic conditions, water sources, health and environmental sanitation, previous control interventions, socioeconomic status of the population subjects, and differences in host susceptibility to parasitic infections [15,29]. Abdel Hamnid et al. [15] reported that H. nana infections were more prevalent among men than women, with no significant differences between age groups, which was also observed in this study. Interestingly, there were no significant differences in the prevalence of intestinal helminthiasis between Al Hidaib and Khour Ajwal villages, even though schistosomiasis prevalence was significantly higher in Al Hidaib than in Khou Ajwal. Thus, major intestinal helminths detected in this study, H. nana, are more affected by the general environmental sanitation than access to clean water supplies.

The limitation of this study is based on the single egg screening process, which is less reliable in estimating prevalence of schistosomiasis and intestinal parasitic infections. The examination of 2 or more specimens at different time points for every individual would likely have resulted in higher prevalence for schistosomiasis and intestinal helminthiasis as well as a larger number of detected intestinal parasite species. In addition, we applied Kato Cellophane method to examine the stool samples, thus there were some limitation to detect the intestinal protozoa.

Our data provide up-to-date information regarding the infection status of Schistosoma species and intestinal helminths among village residents living in the rural river basin area in Sudan’s White Nile State. From this study, the overall prevalence of schistosomiasis and intestinal helminthiasis was found to be 36.3% and 7.7%, respectively. Urinary schistosomiasis was found highly prevalent among pre-school and school-aged children, and intestinal helminths are also prevalent among the village residents. Therefore, integrated intervention including health education, environmental hygiene, and clean water supplies and treatment should be taken into account to reduce the prevalence of schistosomiasis and intestinal parasitic infections.