Prevalence of Schistosoma haematobium infection among students at Al-Agali Islamic complex in Al-Kalakela area, Khartoum State-Sudan

INTRODUCTION

Schistosomiasis (Bilharziasis as “the infection was first described by the German physician Theodor Bilharz”) is a water borne parasitic disease caused by Schistosoma, the digenic trematode found in the blood vessels of man and livestock.¹ Schistosomiasis is a parasitic disease caused by blood vessel-dwelling flukes of the genus Schistosoma. There are several species in the genus but primarily S. haematobium (causes urinary

Schistosomiasis), S. mansoni, and S. japonicum (both cause intestinal schistosomiasis) infect humans.^2,3

Schistosomiasis considered as a neglected tropical disease by the World Health Organization (WHO), schistosomiasis affects more than 250 million people worldwide with an estimated global burden of 1.4 million disability-adjusted life years (DALYs) in 2017.⁴ Schistosomiasis is one of the occupational associated infection that can be transmitted to a susceptible host or through recreation that involves contact with water infested with the free living cercariae that penetrate the skin and develops to maturity in the human⁵. Schistosomiasis is a worldwide public health problem within tropical and sub-tropical areas. An estimated 779 million people are at risk of contracting the infection. It is most prevalent among school-going children⁶. The main group at risk is school children, while other specific occupational groups (fishermen, irrigation workers, farmers), women and other groups using infested water for domestic purposes are also considered to be at risk.³

S. haematobium is an etiologic agent of urinary schistosomiasis and it is most prevalent in Africa⁷. In sub-Saharan Africa, S. haematobium infection is estimated to cause 70, 32, 18 and 10 million cases of haematuria, dysuria, bladder-wall pathology and major hydronephrosis, respectively.⁷ Urinary schistosomiasis leads to a variety of clinical manifestations as haematuria, The presence of blood cells in urine. Other associated features are dysuria and suprapubic pain.⁸

The prevalence of Schistosomiasis in Africa: many countries are affected by disease, so the prevalence different from countries. In Nigeria the urinary schistosomiasis varies from 13.8% among secondary school students at Ondo State, 58.7% among children school in Kwara State to78% among primary school pupils -Lagos State.^8-10

The prevalence of schistosomiasis in the children in the River Volta basin in South Eastern Ghana ranges from 2-21%.¹¹ In Malawi: the prevalence of S. haematobium among preschool children 13% ¹². In Tanzania: the prevalence of S. haematobium among children aged 5 to 17 years 5.7%.¹³ In Cote d’Ivoire: the prevalence of S. haematobium among schoolchildren 14%⁴. In Ethiopia: The prevalence of S. haematobium infection among children in Hassoba, Buri and Hanledebe villages in the Middle Awash Valley was 37%, 25%, and 23.5%, respectively.¹⁴ In Burkina Faso the prevalence among school-age children 8.76%.¹⁵ In Senegal the prevalence of S. haematobium among school children 57.6%.¹⁶ Several endemic countries in Africa launched national programmes for the control of schistosomiasis.¹⁵ These programmes are largely based on preventive chemo-therapy with praziquantel and are targeted at school-age children and adults at risk.¹⁵

In Sudan, the risk for schistosomiasis is widespread, especially in the major irrigation systems in the Gezira area between the Blue and White Nile Rivers. High prevalence of S. mansoni infection in some areas in the West Equatorial region and both S. mansoni and S. haematoabium are endemic in the Upper Nile region, in Sudan about 5 million people are infected by schistosomiasis.¹⁷ Schistosomiasis is widespread and constitutes a critical public health problem in Sudan mainly among children school age as compared to other age groups. Number of factors have been deemed responsible because of higher rates between the specified age groups. Thus, for instance, include the increased water activities such as fishing or swimming. Besides, improper hygiene arrangements provide better opportunities for the spread of infection.¹⁸ The prevalence of Schistosomiasis in Sudan different from area to other, the different studies showed the prevalence was 40% among schoolchildren in White Nile State.¹⁷ 46.5% among student in White Nile River Basin². 45.6% among children at Al-Rahad City – North Kordofan State¹⁸. 24.1% among school children in Al-Lamab Bahar Abiad Area, Khartoum State.³ This study, therefore, aimed to study the prevalence and associated risk factors of S. haematobium infection among students at Al-Agali Islamic Complex in Al-Kalakela area, Khartoum State - Sudan.

METHODS

Study design

A cross sectional descriptive study which was conducted among students at Al-Agali Islamic Complex in Al-Kalakla area in Khartoum State, Sudan.

Study population and sampling

The study population were students at Al-Agali Islamic Complex. The total number of students was 110. We use the total coverage of students attending during the study period, 102 students were participated. While 8 students were absent during period of data collection.

Data collection

Data were collected from participants (Students) used the following tools:

Questionnaire

Pre tested structured questionnaire was used to collect socio-demographic characteristics such as (Sex, age group, marital status, monthly income, educational level, and family history of obesity), possible risk factor such as

Collection of urine samples

Urine samples were collected from participants between 10:00 a.m. and 1:00 p.m. corresponding to the period of maximum egg output in urine. A clean dry 30 ml plastic screw capped container was used. The container was labelled with corresponding number so the results would not be exchanged. The urine collected was immediately taken to the laboratory to analysis.

Parasitological examination

Collected urine samples were immediately transported to the laboratory of epidemiology at Faculty of Public and Environmental Health - University of Khartoum (about 20 km from the study area). Using sedimentation method. The procedures for the urine examination are as follows: 10 ml of each urine sample was taken, centrifuged at 3000 rpm for 5 minutes. The supernatant was discharged and sediment transferred onto clean grease free glass, covered with a cover glass. Then entire sediment was examined microscopically using 40X objective to identify Schistosoma haematobium ova which is characterized by the presence of terminal spine and recorded as eggs/10ml of urine.

Data analysis

Data were analysed used SPSS (Statistical Package for Social Science) version 20. Chi-square test was used to determine the significance differences between variables. The Odds ratio (OR) was applied with 95% confidence intervals. Differences to be significant at level of p.value less than 0.05. Study was conducted after approval from the department of epidemiology at Faculty of Public and Environmental Health, University of Khartoum. Verbal consent was taken from the head of the Complex and then informed consent was obtained from the parents of students.

RESULTS

Prevalence of S. haematobium among participants

Out of 102 samples of urine examined 13 were found infected (positive) with S. haematobium (urinary schistosomiasis) which gives a prevalence of 12.7%, while 87.3% (89/102) were negative (Figure 1).

Socio-demographic characteristics of study participants

According to the age group 54.9% of participants in age group11-15 years, 30.4% in age group 16-20 years, while 14.7% (15 out of 102) in age group 5-10 years. Regarding to their parents’ education status, 55.9% of participants, their mothers were illiterate, 35.3% primary/basic education, while 8.8% (9/102) secondary education. Regarding to their fathers’ education 46.1% were illiterate, 39.2% primary/basic education while 14.7% have secondary education. Regarding to their family monthly income most of their participants’ families were low income (66.7%), 26.4% of families’ middle income while 6.9% (7/102) with high income. Regarding to the participants’ family size, 41.2% of families have less than six members, 19.6% their members 6 person, while 39.2% of participants have big families (>6 persons) (Table 1).

Socio-demographic characteristics associated with S. haematobium positivity

According to association between socio-demographic variables (Age group, parents’ education, monthly family income and family size) and S. haematobium positivity, the results showed there is no statistically significant (p>0.05) (Table 2).

*P<0.05 considered significant at CI 95%.

*P-value < 0.05 considered significant at CI 95%.

Association between some risk factors and S. haematobium positivity among participants

Table 3 Demonstrate the relationship between some risk factors such as; Hearing by Schistosoma, mode of transmission, source of water supply, swimming in rivers, working in agriculture, past history of schistosoma and pre-schistosoma treatment S. haematobium positivity. The results showed that, the prevalence more among those don’t knew the mode of transmission, there was statistical association between don’t knew of mode of transmission history and S. haematobium positivity OR 0.09 (95% CI 0.011- 0.75, p=0.025). The findings show the participants whose swimming in rivers are eight times more likely to have S. haematobium compared to those not swimming in rivers OR 8.09 (95% CI 1.69-38.73, p=0.008). The results show respondents whose working in agriculture are four-and forty-three times more likely to have S. haematobium compared to those have not working in agriculture OR 4.43 (95% CI 1.26- 15.56, p=0.020). The results show there was statistically significant between past medical history of schistosoma and S. haematobium positivity OR 4.87(95% CI 1.44- 16.45, p=0.010). Also, the result show there was strong statistical association between the pre-schistosoma treatment and S. haematobium positivity OR10.29 (2.14-49.39, p=0.0003). The results show there is no statistical association between hearing about schistosoma, source of water supply and S. haematobium positivity (p=0.307 and 1.385 respectively).

DISCUSSION

This study was designed to determine the prevalence of S. haematobium and to identify the possible risk factors associated with infection among student in Al-Agali Islamic Complex, Southern part of Khartoum – Sudan. Schistosomiasis is the most prevalent parasitic disease in Sudan, both urogenital and intestinal forms of schistosomiasis are common throughout the country with geographically varying degrees of prevalence.² The findings showed, the prevalence of S. haematobium among students was 12.7%. This result similar with that found among children school in Um-Asher Area, Khartoum, Sudan 12.9%.²⁴ Our finding was lower than that found in different areas in Sudan; 24.1% among school children in Al-Lamab Bahar Abiad Area, Khartoum State, 40% among schoolchildren in White Nile State, 45.6% among children at Al-Rahad City-North Kordofan State¹⁸ and 46.5% among student in White Nile River Basin.^2,3,17,18 Our finding was higher than that found in Tanzania 5.7%.¹³ Also, our result similar with that found in Malawi 13%.¹² Our finding was lower than finding in some different countries in Africa; In Nigeria 58.7%, in Cote d’Ivoire 14%, in Senegal 57.6%^, in Ethiopia 23.5%-37%.^4,9,14,16

The results showed the prevalence of S. hameatobium higher among age greater ten years; 54.9% in age group 11-15 years, 30.4% in age group 16-20 years while 14.7% in age group 5-10 years. This agreement with that found in Sudan, the highest frequency of positive cases was found among the age group of 12 to 15 years (64.4%).¹⁷ Also similar with that reported in Yemen, the children aged >10 years were more prone to be infected with S. haematobium than younger children.¹⁹ This study revealed that there was no statistical association between socio-demographic characteristics (age group, parents’ education, monthly family income and family size) and S. haematobium positivity (p>0.05). in particular, our finding disagrees with that reported in Sudan an association between the levels of parental education and S. haematobium infection.²⁰ In Cote d’Ivoire a significant relationship between illiteracy of the parents/guardians and Schistosoma infection was reported⁴. In Yemen a significant association between the high prevalence of schistosomiasis and the age of children, fathers’ educational level, household monthly income¹⁹. Our results similar with that reported in Malawi; socioeconomic status of the household was not an independent factor associated with infection in Children.²²

The findings of the present study showed there was statistical association between don’t knew of mode of transmission history and S. haematobium positivity OR 0.09(95% CI 0.011- 0.75, p=0.025).

The association between schistosomiasis and water contact is well documented. The findings showed the participants whose swimming in rivers are eight times more likely to have S. haematobium compared to those not swimming in rivers OR 8.09 (95% CI 1.69-38.73, p=0.008). our study similar with findings have been reported in previous studies in different countries; in Nigeria reported the closeness of the schools to the host stream and the frequent exposure to the stream contributed to high prevalence of urinary schistosomiasis among the students.⁸ In Cote d’Ivoire study revealed that swimming and fishing in freshwater by schoolchildren was strongly associated with infection with S. haematobium.⁴

The study showed respondents whose working in agriculture were at four-and forty-three folds’ higher risk of getting S. haematobium OR 4.43 (95% CI 1.26- 15.56, p=0.020). this agreement with that found in Nigeria noted that pupils whose parents were farmers had the highest infection rate and relatively followed by those whose parents were civil servants and traders²¹. Also, this result agreed with study from Ethiopia; reported occupation of father was significantly associated with urinary schistosomiasis where children with farmer as father’s occupation were two times more likely to be infected than children with non-farmer as father’s occupation²³. The study showed there was statistically significant between previous infection of schistosomiasis and S. haematobium positivity OR 4.87 (95% CI 1.44- 16.45, p=0.010). Which is similar to that found in Sudan a history of urinary schistosomiasis treatment was strongly associated with

S. haematobium infection in South Kordofan State.²⁰ Our finding agreement with study from Nigeria, showed that participants who had a history of schistosomiasis were 2.87 times more likely to be infected compared with individuals that did not have history of schistosomiasis.²⁵

CONCLUSION

The present study shows that S. haematobium is still prevalent among students in Khartoum State, Sudan; 12.7% of the participants were found to be positive for S. haematobium. Screening of family members and treating the infected individuals should be adopted by the public health authorities to control this infection. School and community-based health education regarding mode of transmission and possible risk factors are recommended to reduce the transmission and morbidity of schistosomiasis.

Limitations of the study

This study had numbers of limitations. The cross‑sectional design may not allow for the temporal relationship for the potential risk factors and outcomes, other factors were not assessed such as (Ethnicity, time spend in swimming and information and source of information about) and small of sample size that my influence on study.

Funding: No funding sources

Conflict of interest: None declared

Ethical approval: The study was approved by the Institutional Ethics Committee

REFERENCES

1. 1. Singh K, Muddasiru D and Singh J. Current status of schistosomiasis in Sokoto, Nigeria. Parasite Epidemiology and Control. 2016;239-44.
2. 2. Ismail AHAH, Hong S, Babiker BTA, Hassan AMR, Sulaiman ZAM, Jeong H, et al. Prevalence, risk factors, and clinical manifestations of schistosomiasis among school children in the White Nile River basin, Sudan. Parasites and Vectors. 2014;7:478.
3. 3. Osman RO, Eisa NS, Nasr AA, Ali OOS, Siddig EE and Mohamed NS. Prevalence of Schistosoma haematobium among School Children in Al-Lamab Bahar Abiad Area, Khartoum State, Sudan 2017: A Cross Sectional Study. EC Microbiology 2018;14.8:454-9.
4. 4. Angora EK, Boissier J, Menan H, Rey O, Tuo K, Toure AO, et al. Prevalence and Risk Factors for Schistosomiasis among Schoolchildren in two Settings of Cote d’Ivoire. Trop. Med. Infect. Dis. 2019;4:110.
5. 5. Otuneme OG, Obebe OO, Sajobi TT, Akinleye WA and Faloye TG. Prevalence of Schistosomiasis in a neglected community, South western Nigeria at two points in time, spaced three years apart. African Health Sciences. 2019;19(1):1338-45.
6. 6. Kabuyaya M, Chimbari MJ and Mukaratirwa S. Infection status and risk factors associated with urinary schistosomiasis among school-going children in the Ndumo area of uMkhanyakude District in KwaZulu-Natal, South Africa two years post-treatment. Int J Infectious Diseases. 2018;71:100-6.
7. 7. Geleta S, Alemu A, Getie A, Mekonnen Z and Erko B. Prevalence of urinary schistosomiasis and associated risk factors among Abobo Primary School children in Gambella Regional State, southwestern Ethiopia: a cross sectional study. Parasites and Vectors. 2015;8:215.
8. 8. Akinneye JO, Fasidi MM, Afolabi OJ and Adesina FP. Prevalence of Urinary Schistosomiasis among Secondary School Students in Ifedore Local Government, Ondo State, Nigeria. Int J Trop Dis. 2018;1:004.
9. 9. Bolaji OS, Elkanah FA, Ojo JA, Ojurongbe O, Adeyeba OA. Prevalence and Intensity of Schistosoma haematobium among school children in Ajase-Ipo, Kwara State, Nigeria. Asian J Biomed and P’ceutical Sci. 2015;5(43):06-11.
10. 10. Oluwasogo OA and Fagbemi OB. Prevalence and risk factors of Schistosoma haematobium infections among primary school children in Igbokuta Village, Ikorodu North Local Government, Lagos State. IOSR J Nursing and Health Sci. 2013;2(6):62-8.
11. 11. Nkegbe E. Prevalence of Schistosomiasis among School Children in the Lower River Volta Basin in Ghana. Gomal J Med Sci. 2010; 8(1):54-6.
12. 12. Moyo VB, Changadeya W, Chiotha S and Sikawa D. Urinary schistosomiasis among preschool children in Malengachanzi, Nkhotakota District, Malawi: Prevalence and risk factors. Malawi Med J. 2016;28(1):10-4.
13. 13. Kavana NJ. Prevalence of Schistosomiasis Infection among Young Children Aged 5 to 17 Years in Kilosa District, Tanzania: A 3Year Retrospective Review. J Trop Dis. 2018;6:255.
14. 14. Degarege A, Mekonnen Z, Levecke B, Legesse M, Negash Y, Vercruysse J, et al. Prevalence of Schistosoma haematobium Infection among School-Age Children in Afar Area, Northeastern Ethiopia. PLoS ONE 2015;10(8):e0133142.
15. 15. Ouedraogo H, Drabo F, Zongo D, Bagayan M, Bamba I, Pima T, et al. Schistosomiasis in school-age children in Burkina Faso after a decade of preventive chemotherapy. Bull World Health Organ. 2016;94:3745.
16. 16. Senghor B, Diallo A, Sylla SN, Doucouré S, Ndiath MO, Gaayeb L, et al. Prevalence and intensity of urinary schistosomiasis among school children in the district of Niakhar, region of Fatick, Senegal. Parasites and Vectors 2014;7:5.
17. 17. Elsiddig, HA, Khider E, NourSM, Makhawi AM and Mogadam EBM. Prevalence of urinary schistosomiasis among schoolchildren in White Nile State, Sudan. African Edu Res J. 2019;7(1):29-32.
18. 18. Salim AMM. Prevalence of Schistosoma Haematobium in Sudan Dry Lan (A case Study at Al-Rahad City, North Kordofan State. Int J Inno and Res in Educ Sci. 2018;5(2):2349-521.
19. 19. Sady H, Al-Mekhlafi HM, Mahdy MAK, Lim YAL,Lim YAL, Surin J and Mahmud R. Prevalence and Associated Factors of Schistosomiasis among Children in Yemen: Implications for an Effective Control Programme. PLoS Negl Trop Dis. 2013;7(8):e2377.
20. 20. Abou-Zeid AH, Abkar TA and Mohamed RO. Schistosomiasis infection among primary school students in a war zone, Southern Kordofan State, Sudan: a cross-sectional study. BMC Public Health. 2013;13:643.
21. 21. Naphtali RS, Yaro MB and Arubi M. Prevalence of Schistosoma haematobium among Primary School Children in Girei Local Government Area, Adamawa State, Nigeria. IOSR J Nursing and Health Sci. 2017;6(1):48-50.
22. 22. Kapito-Tembo AP, Mwapasa V, Meshnick SR, Samanyika Y, Banda D, Bowie C and Radkel S. Prevalence Distribution and Risk Factors for Schistosoma hematobium Infection among School Children in Blantyre, Malawi. PLoS Negl Trop Dis. 2009;3(1):e361.
23. 23. Geleta S, Alemu A, Getie S, Mekonnen Z and Erko B. Prevalence of urinary schistosomiasis and associated risk factors among Abobo Primary School children in Gambella Regional State, southwestern Ethiopia: a cross sectional study. Parasites and Vectors. 2015;8:215.
24. 24. Hajissa K, Muhajir AMA, Eshag HA, Alfadel A, Nahied E, Dahab R, et al. Prevalence of schistosomiasis and associated risk factors among school children in Um-Asher Area, Khartoum, Sudan. BMC Res Notes. 2018;11:779.
25. 25. Dawaki S, Al-Mekhlafi HM, Ithoi I, Ibrahim J, Abdulsalam AM, Ahmed A, et al. Prevalence and risk factors of schistosomiasis among Hausa communities in Kano State, Nigeria. Rev Inst Med Trop Sao Paulo. 2016;58:54.