Schistosomiasis and Associated Risk Factors Among School-Aged Children in Northern Nigeria

Background: The Jigawa State Ministry of Health in Northern Nigeria undertook a pilot intervention without a follow-up to control schistosomiasis through preventive chemotherapy by ensuring that each child swallows praziquantel from 2009 to 2013 in five primary schools in Dutse metropolis. Previously, the overall prevalence for urinary and intestinal schistosomiasis determined using Sedimentation and Kato Katz methods was 22.9%. Methods: A cross sectional study involving 150 randomly selected pupils, aged 6 15 years old was conducted using sedimentation and Kato-Katz methods to determine the prevalence of urinary and intestinal schistosomiasis respectively in three schools in July, 2018. Information on demographic and associated risk factors was collected using a structured questionnaire and the data generated was analyzed using SPSS statistics version 18.0. Results: The overall prevalence was 10% with S. haematobium 8%, S. mansoni 2.67% and co-infection 0.67%. Males had higher prevalence, 15.10% than females 1.75%. The 11 15 years age group had higher prevalence, 10.10% than 6 10 years, 9.68%. Nearly all the infections occurred among class 4-6 pupils with 12.10% and 2.94% in 1-3. Based on parental occupations, children of unskilled laborer had the highest prevalence of 16.67% followed by children of civil servants 12.50%, and children of butchers 0%. Kachi School had the highest prevalence of 14.00% while Sir Muhammadu Sunusi had the lowest 4.00%. Schistosomiasis prevalence was found only to be significantly associated with gender; higher among males than females (15.1% vs 1.75%, P = 0.011). Conclusion and Implications for Translation: Schistosomiasis is still endemic among school-aged children in Dutse metropolis, but with a drop in overall prevalence from 22.9% to 10.00%. Chemotherapy and health education should be sustained on both in and out of school-aged children in order to control the transmission.


Background of the Study
Schistosomiasis is the most prevalent neglected tropical disease (NTD) after malaria and intestinal helminthiases. 1 It is the third most devastating tropical disease in the world, being a major public health problem in many developing countries in Africa, South America and the Middle East. More than 207 million people are infected globally, 80% of these live in Africa and an estimated 700 million people are at risk of infection in 76 countries where the disease is considered endemic. 2 People in endemic areas were exposed to infested water mainly through their agricultural work, domestic chores and other recreational activities. Globally 200,000 deaths are attributed to schistosomiasis annually. 3 Nigeria is having the greatest number of cases of schistosomiasis worldwide, with about 24 million people at risk of infection and an overall prevalence of 9.5%. 4,5 The five species of schistosoma that causes the disease worldwide include S. haematobium, S .mansoni, S. japonicum, S. intercalatum and S. mekongi and S. haematobium, and S. japonicum account for greater percentage (95%) of all human cases of schistosomiasis found in the world. 6 In Nigeria, two species are pathogenic to man; S. haematobium and S. mansoni. The disease caused by S. haematobium is characterized by bloody urine, calcification of the bladder and kidney failure and bladder cancer in children. It is also the major cause of female genital Schistosomiasis (FGS). 7,8 On the other hand, intestinal schistosomiasis can result in abdominal pain, diarrhea, blood in the stool, liver enlargement is common in advanced cases, and is frequently associated with an accumulation of fluid in the peritoneal cavity and hypertension of the abdominal blood vessels. In such cases there may also be enlargement of the spleen. 9 Schistosomiasis prevalence data for Nigeria extracted from peer-reviewed journals and reports, geo-referenced and collated in a nationwide geographical information system database revealed that the disease is endemic in 35 of the country's 36 states, including the federal capital territory of Abuja. 10 Schistosomiasis prevalence and morbidity is highest among school children, adolescent and young adult. 11 Thus, the negative impact on school performance and the debilitation cause by untreated infection demoralized both social and economic development in endemic areas. 12 The global effort to eliminate schistosomiasis is enshrined in World Health Organization's (WHO) schistosomiasis plan with a vision of a "World Free of Schistosomiasis," with its end goal to eliminate the disease as a public health problem by 2025, and to interrupt transmission in many areas by the same time. 2 The control of schistosomiasis is based on large-scale treatment of at-risk population groups, access to safe water, improved sanitation, hygiene education, and snail control. 13 In response to this global effort Nigeria came up with national program to eliminate schistosomiasis together with other NTDs. According to the Nigerian master plan for NTDs 2015 -2020, all the 774 Local Government Areas (LGAs) in the country have been mapped; 603 are endemic for schistosomiasis and that provisional prevalence of the disease ranged between 0-84% nationwide. 14,15 Prior to the development of the master plan there was a national effort to control schistosomiasis mainly through chemotherapy that is the provision of an antihelminthic praziquantel and health education to school-aged children. For instance, in Jigawa State pilot control effort was carried out by the state Ministry of Health in five primary schools in Dutse metropolis from 2009 to 2013. 16 Based on WHO protocol for the control of schistosomiasis, all the children with exception of the sick in the five schools were given the antihelminthic drug once in a year to swallow under the supervision of their teachers and health officials from the ministry. The children were later observed for any side effects due to the administration of the antihelminthic. In addition, health education campaign was done on how the children could safeguard themselves from contracting the disease. Prior to the commencement of the control effort in these primary schools, the overall prevalence of schistosomiasis using the sedimentation and kato-katz methods was 22.9%. 17 However, there was no follow up on the progress made in such control efforts. The present work aims at conducting a post intervention study on the prevalence and risk factors of schistosomiasis using the same methods on school-aged children in three primary schools in Dutse metropolis in order to determine the status of schistosomiasis following the intervention.

Objectives
To determine the prevalence of urinary and intestinal schistosomiasis among school aged children (6-15 years) in Dutse Metropolis following preventive chemotherapy from 2009 to 2013. To determine the risk factors associated with prevalence of schistosomiasis among school aged children (6-15 years) in Dutse Metropolis following chemotherapy from 2009 to 2013. Our specific aim was to conduct a post-intervention study of the prevalence of schistosomiasis and its associated risk factors among school aged children in Dutse Metropolis, Dutse, Jigawa State, Northern Nigeria. We hypothesized that there is no significant difference in the prevalence of schistosomiasis among school aged children (6-15 years) between the pre and post intervention periods in Dutse Metropolis. The researchers hypothesize that there is no association between the prevalence of schistosomiasis and risk factors among school aged (6-15 years) in Dutse Metropolis.

Study Area
The study was carried out in Dutse metropolis, Dutse Local Government Area, Jigawa State, Nigeria. Dutse is a city located in Northern Nigeria and is the capital of Jigawa State. It is situated between latitude 11 42'8.46'N and longitude 9 20'2.46"E or 11.702351 and 9.334016 respectively. Dutse is currently the largest city in Jigawa State with an estimated population of 153,000. 18 The population of Dutse is predominantly the Hausa and Fulani tribes practicing agriculture as the main source of livelihood.

Study Design, Sample Size and Population
A cross sectional study involving 150 school pupils, aged 6 -15 years old, was conducted in Dutse metropolis in July 2018. The sample size was determined using the formula for schistosomiasis. 19 Where, N= Sample size, Z= the normal standard deviate (Z=1.96) P= the frequency of occurrence of schistosomes (P = 22.9%), Q= 1-p D= degree of precision (0.05%).
Out of the five schools targeted for pilot schistosomiasis control in Dutse metropolis by the Jigawa State Ministry of Health in 2009 and 2013, three primary schools were selected for the post intervention study namely; Galadanchi, Dr. Nuhu Muhammad Sunusi and Kachi Special primary schools. A total of 150 pupils were randomly selected from classes 1 -6.

Questionnaire Administration
A validated structured questionnaire was used to obtain demographic and socioeconomic information such as water contact activity, source of drinking water, personal and environmental hygiene practices and contact with a water body.

Parasitological Examination
Three hundred (300) samples comprising 150 urine and 150 stool samples were collected by assignment of numbers to every member of the randomly selected participants from the different classes. In an appropriately labeled plastic screw cap urine and stool containers, the children were asked to collect 10mls of the urine sample and 5g of fresh stool samples at mid-day. The pupils were also instructed on how to collect the urine sample advising to include the first and last drops, for these drops often contain the highest number of the eggs.
Both stool and urine samples were taken in an ice container to the Biology Laboratory, Department of Biological Sciences, Federal University Dutse, Jigawa State, Nigeria for immediate processing. The urine samples were processed using sedimentation technique as described in previous studies. 20,21 The supernatant was discarded using syringe and needle, and the sediment was transferred to a plain slide with cover slip and the sediment was examined initially at ×10 and then × 40 magnifications under the light microscope. Eggs were detected and identified by the shape and terminal spine characteristic of S. haematobium. The stool samples 106 www.ijtmrph.org were analyzed as outlined in prior studies 20,22 using Kato-katz kit. Malachite green was added to each of the processed slide and was examined under the microscope initially under ×10 and later ×40 for the presence of egg or ova of S. mansoni. The eggs were detected and identified by the shape and lateral spine characteristics of S. mansoni. Positive samples for both S. haematobium and S. mansoni were counted and recorded.

Data Analysis
The data generated was analyzed using SPSS version 18.0 (IBM corporation, NY, USA). The demographic characteristics and socioeconomic variables of the research participants were presented in form of frequencies and percentages. Chi square was used to test the association between demographic, socioeconomic and behavioral variables with infection. A linear regression analysis was used to identify the risk factors that significantly (P < 0.05) associated with schistosomiasis infection.

Ethical Approval
Ethical clearance was obtained from Jigawa State Ministry of Health via a letter with a reference number MOH/SEC/3.5/620/1 dated 21 st April, 2018. Correspondingly the Jigawa State Universal Basic Education Board (JGSUBEB) consented to the study based on the MOH ethical clearance. The purpose of the study was explained to the Headmaster of the schools and informed consent from the pupils, parent or guardian of the children was sought before the commencement of the work and was kept in confidentiality.

Demographic and Socioeconomic Characteristics of the Participants
The demographic and social characteristics of the participants are presented in Table 1. Majority of the participants were males 62% while 38% were females. Participation according to age groups showed that the 11 -15 years age group had the highest number 72% followed by 6 -10 years age group with 28%. The same trend is maintained with regard to participation based on class of the pupils, children in class 4 -6 were more in number than those in class 1-3. Many of the pupils' parents were of civil servants 48% while others were farmers 28%. Table 2 presents the details prevalence of infection among the participants. The overall prevalence of schistosomiasis was 10% with S. haematobium 8%, S. mansoni 2.67% and co-infection 0.67%. Males had an overwhelming prevalence of 15.10% over females with 1.75%. The 11 -15 years age group had higher prevalence of 10.10% than 6 -10 years age group had 9.68%. Kachi Primary School had the highest prevalence 14.00% followed by Galadanchi with 12.00% while Sir Muhammadu Sunusi had the lowest 4.00%. Almost all the infection occurred among pupils in classes 4 -6 with 12.10% and an infection among the class 1 -3 pupils. Children whose parental occupation was unskilled laborer had the highest prevalence of 16.67% followed by civil servants 12.50%, farming 4.76%, trading 6.25% and butcher 0.00%. the level of significance was retained at P = 0.033 indicating that males were at higher risk of becoming infected than their female counterparts. The level of significance was still retained in logistic regression analysis (P = 0.033), the odds of infection was more than nine times higher in males than in females (OR = 9.38; 95% CI =1.19, 73.76).

Discussion
This study recorded an overall post intervention prevalence of 10.00% for schistosomiasis among the pupils in three primary schools in Dutse metropolis, thus still indicating that the disease is endemic among school aged children in Dutse metropolis. However, the result revealed a considerable reduction in the disease prevalence from 22.9% before the intervention that was done from 2009 to 2013 to post intervention prevalence of 10%. The lower prevalence observed during the post intervention might be a reflection of the success of the intervention as well as increased availability of potable water sources in form piped borne water and bore hole as well as improved environmental sanitation provided by government at all levels (state, local and private). These efforts might have helped in reducing water contact activities of the pupils with contaminated water that expose them to infection with schistosomiasis. This is also supported by the fact that previous studies in Dutse metropolis have reported much higher prevalence of infection with schistosomiasis. For instance, an overall prevalence of 37.33% was reported among primary school aged children in Dutse. 23 Another study observed an overall prevalence of 39.2% among patients attending a secondary health facility in Dutse. 24 This study included adolescents that have been reported in many studies to be more susceptible to infection with the schistosomiasis when compared with either children or the aged persons.
The overall prevalence obtained in this study was also much lower than many other previous findings such as those from neighboring Kano State of 25% and 17.8%. 25,26 A prevalence of 63.73% was observed in poor communities of Sokoto town, Sokoto State, Nigeria. 27 In another study urinary  Table 3 shows the univariate analysis to determine the association between infection with schistosomiasis and demographic characteristics, socioeconomic status and behaviors of the research participants. Apart from gender, all the other variables (age, parents' occupation, water contact activities, water source usage and personal hygiene) were found to be not significantly associated with schistosomiasis infection among the school aged children in the three primary schools. Schistosomiasis prevalence was found to be significantly higher among males than females (14.1% vs 1.7%, P = 0.011). When gender was considered for logistic regression analysis in Table 3, www.ijtmrph.org schistosomiasis from Riverine areas of Ondo State, Nigeria a prevalence of 48.4% was reported. 27 The difference between our finding and that of these studies could be attributed to the fact that no interventions were undertaken in the other populations where such studies were carried out.

Risk Factors of Schistosomiasis among the Study Population
In addition, these studies were done in poor or rural communities that lack portable drinking water which exposed the population to higher risk of contracting schistosomiasis. However, the result in this study was higher than an overall prevalence of 1.55% reported in Bauchi State, Nigeria. 13 According to the researchers, the lower prevalence ought to be the nature of subjects involve in the study whom were mostly students and civil servants that lived in urban areas with improved water supply.
The prevalence of infection with S. haematobium was higher than that with S. mansoni in this study. This is consistent with findings from previous studies such as reports by. 13,23,25,27 The explanation for this is that the vectors responsible for the transmission of S. haematobium, the Bulinus species have higher relative abundance than Biomphalaria species that transmit S. mansoni in local water bodies in Northern Nigeria. 28 This argument is further reinforced by the results of many previous studies on the ecology of freshwater snails especially in dams which have reported that Bulinus species have higher relative abundance when compared with Biomphalaria species. 6 This also agrees with global report that intestinal schistosomiasis is less prevalent than urinary schistosomiasis in tropical Africa.
Males had higher prevalence than females in terms of infection with both urinary and intestinal schistosomiasis. This finding is consistent with many previous studies. 13,23,25,26,29 The higher prevalence rate among males might be associated with cultural practices of the inhabitants where the disease is endemic in tropical Africa and Nigeria in particular where it is mainly the males that are engaged extensively in activities such as swimming, fishing and farming that results in higher risk infection with schistosomiasis. However, finding from some studies have reported a slightly higher prevalence of the disease in female than male. 17,30 This might be because in settings where these studies were conducted both male and female are almost equally engaged in activities that predisposes them to infection.
Children within age group of 11-15 years had the highest prevalence of urinary and intestinal schistosomiasis. This outcome is consistent with the many studies. 23,25,26,29,13 The higher prevalence recorded among this age group was probably linked to the outdoor activities that they were more actively engaged in than the younger children, the 6-10-years age group especially swimming in contaminated water that exposes them more to infection with schistosomiasis. The finding was also in agreement with previous reports. 25,27 This is also supported by the fact that children in classes 4 -6 which generally belong to older age group had higher prevalence than those in lower classes. Based on school location, Kachi had the highest prevalence followed by Galadanchi while Dr. Muhammadu Nuhu Sunusi had the lowest. The possible explanation for this could be Kachi and Galadanchi are located in the suburb of Dutse metropolis that enjoyed less improved water supply and have the presence of environmental factors such as standing water bodies that expose children to infection with schistosomiasis.

Limitations
The major constrain was that the post intervention study was done about three years after the index intervention. Therefore, the reported reduction in prevalence may not be solely attributed to the index intervention, it could also be associated with government programs especially improved water supply and environmental sanitation. In addition, among the risk factors considered only gender was controlled. There should be a more extensive study of schistosomiasis among both school and out of school children covering the entire state so that a comprehensive data on mapping is generated that could be used in planning and executing a more integrated schistosomiasis control program in the state.

Key Messages
• Prior to index intervention, the overall prevalence of urinary and intestinal schistosomiasis determined using sedimentation and kato-katz methods respectively among school-aged children was 22.9%. • The index intervention was mainly through preventive chemotherapy following WHO protocols by administering of praziquantel to each child once in a year from 2009 to 2013. • A post intervention study in 2018 revealed that the disease is still endemic with an overall prevalence of 10%, thus indicating a reduction which could be attributed to index intervention and other factors such as improved clean water supply, environmental sanitation and personal hygiene in the study area.