Prevalence and Intensity of Urinary Schistosomiasis Among Selected People in Tulus Area, South Darfur State, Sudan


 Objective: Urinary schistosomiasis is a major public health issue in Sudan. The disease is endemic in many rural communities across the country. This is a cross-sectional study conducted to determine the prevalence and intensity of urinary schistosomiasis among selected induvial in the city of Tulus, South Darfur state, Sudan. One hundred terminal urine samples were collected and examined for Schistosoma haematobium eggs using standard filtration technique.Results: A total of 100 individual were enrolled in the study with a mean (± SD) age of 17.7 ± 0.73 years. Out of them, 62 (62%) were found to be infected with Schistosoma haematobium. The statistical analysis showed significant association with gender (P = 0.043) with higher prevalence 70.9% (39/55) in female than males 51.1% (23/45). Majority of the S. haematobium infections were classified as intense infection (82%, 51/62) with egg count ≥ 50 eggs/10 ml urine, while gross haematuria was observed in 10% of urine samples. Further studies, including large sample size will be essential to assess the burden of the disease in the study area.


Introduction
Urinary schistosomiasis is a chronic water-dependent parasitic disease caused by the trematode Schistosoma haematobium (S. haematobium) (1). It is the one of most devastating prevalent neglected tropical parasitic diseases (NTDs) due to the high morbidity and mortality rate among susceptible population in developing countries particularly in Africa (2). The poor sanitation and inadequate hygiene (WASH) as well as the lack of access to clean water are major contributors to the burden of the disease (3).
In endemic tropical and subtropical countries, the disease remains as a major public health problem. The high prevalence of schistosomiasis placed it as second most important parasitic disease with public health problem after malaria (4). In the 74 endemic countries, an estimated of 250 million people are infected while approximately 700 million people are at risk of getting the infection (4). In Africa and Middle East S. haematobium is widespread with more than 110 million infected people [6]. In addition, S. haematobium is the cause of nearly two-thirds of schistosomiasis cases resulted in long-term and severe complications (5).
Deposition of the S. haematobium eggs in tissues can cause progressive damage particularly in the bladder, ureters and kidney. The potential consequences of the infection includes haematuria (blood in urine), dysuria (painful urination), nutritional de ciencies and lesions of the urinary bladder (4).
Furthermore, increasing evidence supports that the infection can lead to infertility, cancer, kidney failure and increased susceptibility to HIV. While children might experience anaemia and physical weakness which consequently reduce their learning ability (6) Despite the intensive efforts to control the disease, it is still persists. Many reports stated that urinary schistosomiasis is endemic in Sudan. It was rst reported in the country in 1904. Since then, various epidemiological studies indicated the presence of the disease in all regions of the country (7,8).
A recent nationwide survey carried out in all the states estimated that the overall prevalence of S. haematobium was 5.2%. The same survey pointed East and South Darfur States as most severe endemic areas (9). However, there are limited data on the burden of the disease in these areas. This could be attributed to the civil war in the region as the prevention and control during con ict are often neglected.
Although, in the 1970s, schistosomiasis was reported to be endemic in the western area of Darfur [9], there have been few detailed surveys and published data in this region, particularly during the years overwhelmed by the civil war. Therefore, this study was conducted to provide preliminary information in regard to S. haematobium prevalence in a limited study population recruited form the city of Tulus, South Darfur state which can help in improving schistosomiasis control in the area.

Study design and Study site
This is cross-sectional study carried out during May 2018 to estimate the prevalence of S. haematobium in Tulus area. South Darfur State, Sudan.

Study participants and Sample collection
A total of 100 participants with different ages from both sex (45% males and 55% females) were enrolled in this Study. After informed consent was obtained, about 10 ml of urine samples were collected from each subject.

Laboratory investigation
The urine samples were rst observed whether show occult or gross hematuria, and then examined for the presence of S. haematobium eggs by membrane ltration technique as described previously [10]. In brief: all urine samples of su cient quantity were shaken, subsequently, 10 ml of each sample were pressed through a polycarbonate lter with a pore size of 20 µm (Sterlitech, Kent, WA, USA) using a standard 10 ml plastic syringe, the membrane was then put on a microscope slide, covered with a piece of hydrophilic cellophane soaked in glycerol solution, and examined under the microscope by trained laboratory technicians using some drops of Lugol's iodine to stain S. haematobium eggs after cellophane coverage. The presence and number of S. haematobium eggs was recorded. After microscopy, the slides were stored for second reading for quality control.
The number of S. haematobium eggs per lter was quanti ed; the intensity of the infection was classi ed as light (1-49 eggs/10 ml of urine) or heavy (≥ 50 eggs/10 ml of Urine), as de ned by the World Health Organization [19].

Statistical analysis
The collected data were stored, double checked and analyzed using Statistical package for social science (SPSS) version 22.0 (Inc. Chicago, I.USA). Chi Square test was used for ordinal variables to nd the signi cant differences between several categories and determination of the prevalence (as %), with Pvalues of, 0.05 being considered indicative of a statistically signi cant difference.

Results
A total of 100 individuals (45 males and 55 females) were enrolled from the city of Tulus. The respondents were from the age group of 3-42 years with a mean (SD) age of 17.7 (0.73) years. The overall prevalence of S. haematobium among respondents was 62% (62/100). The prevalence was 51.1% (23/45) and 70.9% (39/55) for the male and female respectively. However the prevalence of the disease was high in the females than males and there was a signi cance difference in the prevalence rate (P = .043), and they were not signi cantly more likely to have intense infections with this parasite.
Majority of the S. haematobium infections were classi ed as intense infection (82%, 51/62) with egg count ≥ 50 eggs/10 ml urine. In addition, gross haematuria was observed in 10% of urine samples. A positive correlation between the haematuria and intensity of eggs was revealed (P. value = .000) (  Table 1 Correlation between the haematuria and egg count

Discussion
In Sudan, schistosomiasis remains a life-threatening public health problem with an estimation of more than eight million people at risk of infection. Thus, Sudanese government prioritised collecting data on the burden of NTDs, particularly schistosomiasis. In response; many epidemiological studies were conducted in central and east Sudan (10,11), with relatively few, if any, such studies being conducted in Darfur area.
Therefore, this study was conducted to estimate the prevalence and intensity of S. haematobium infection in selected populations from the city of Tulus, South Darofur State. The study revealed that the percentage of infected people with S. haematobium infection based on urine ltration method was 62% (62/100). The high observed prevalence of urinary schistosomiasis (62%) was relatively in agreement with the study conducted by Deribe et al. (2011) in the same state whose reported a rate of 56% of infection among the respondents (12). Similarly, remarkably high prevalence (80.6%) was also reported in Gereida Camp, South Darfur (13).
The high prevalence could be attributed to the high exposure and dependence of the people in the area on open water sources for drinking and household purposes (12,14). The adaptation of intermediate host (Bulinus truncates) to pools and slow-owing waters in South Darfur area re ect consideration of these water bodies to be potential transmission sites for the disease (15). In addition, the fact that these small ponds in entire area are used for shing, bathing, and swimming increase the risk of getting the infection.
In contrast, the present study showed very much higher prevalence of S. haematobium compared to that obtained from nationwide survey (5.2%), even though, South Darfur States was the second most endemic area with a prevalence of 13.91% in that survey (9). Moreover, many other nding across the country reported lower ndings when the S. haematobium diagnostic stages were screened particularly among children (11,16,17).  (8,18,19).
Worldwide, similar observation of high Egg positive rate was also made in Senegal (57.6%) (1), while in many other country the rates were slightly lower such as those reported from Nigeria (48%), Gabon (45%), Malawi (10.4%) (4,6,20). This variation could be due to study period, target population, environmental condition, sample size variations and the method of laboratory diagnosis.
With regard to the intensity of the infection, majority of the S. haematobium infections (82%, 51/62) were of intense infection (≥ 50 eggs/10 ml urine). This nding agrees with previous reports (1,4) where the intensity was classi ed as high. However, light infection intensity was also reported (21). The variation between areas could be explained by the frequency of people contact with contaminated water bodies, burden of the adult worms hosted as well as the differences in environmental setting and culture. As a consequence of the high prevalence with heavy S. haematobium infection haematuria was observed in the current study, and there was a positive correlation between the haematuria and intensity of eggs (P. value = .000), this result is in line with result of Ismail et al.,2014 (22) [16]. Indeed the observed hematuria could be attributed to the heavy egg intensity reported among the study participants In conclusion: the very high prevalence of S. haematobium infection observed in the study area, indicate that the city of Tulus is endemic for urinary schistosomiasis, with a high intensity of infection. Therefore, integrated control program and prevention measures need to be implemented in the study area.
MA and AHS: conceived and designed the study and writing the Manuscript, GAA and KH: analyzed the data. All authors read and approved the nal manuscript.