Schistosomiasis is a chronic parasitic disease caused by blood flukes [1] [2]. These blood flukes (or trematode worms) are prime examples of complex multicellular pathogens that flourish in human hosts despite the presence of immune responses mounted against them [3]. Adult schistosomes possess a range of adaptations which enable them to partially overcome human host's defenses and possibly live and reproduce for many years in the host who becomes relatively resistant to new infections [4]. These worms have complex and indirect life cycles involving intermediate (snail) hosts and definitive hosts.

Majorly, populations of tropical and subtropical countries, especially children who indulge in water-based activities in unsafe or cercarial-infested water bodies are affected [2] [5] [6] [7] [8]. The three main species of Schistosoma that cause diseases in man are: Schistosoma mansoni, Schistosoma haematobium (S. haematobium) and Schistosoma japonicum [9] [10]. Other distributions of Schistosoma intercalatum in Central Africa and Schistosoma mekongi in Cambodia and Lao People's Democratic Republic can also cause human infections [2] [11]. Among all the species of Schistosoma, S. haematobium is the only cause of urinary schistosomiasis; all others cause intestinal schistosomiasis [6] [10].

Urinary schistosomiasis is diagnosed by microscopic detection of S. haematobium eggs in urine as a gold standard [6] [12]. Humans become infected by penetration (or dermo-invasion) of intact skin by active cercariae which are attracted to the warmth of body and skin lipids [13].

Schistosoma haematobium has been regarded as a 'neglected schistosome' [14] [15][16] despite its implication in HIV/AIDS co-infection and a burden of bladder cancer development. Though most of the infected individuals in endemic areas of Nigeria suffer from light infections, the disease adversely impacts on the economic and general health conditions of the affected communities [7] [17]. Consequently, the workforce is affected due to weakness and lethargy, and the academic performances of school children are affected [7] [18] [19].

Study area
The study was conducted in some selected and consented primary schools in Jaba Local Government Area (LGA) of Kaduna State, Nigeria. The area is located in the Northern hemisphere on Latitude 9° 19' 47"N to Latitude 9° 36' 35"N, and in the East on Longitude 7° 56' 24"E to Longitude 8° 12' 36"E. The area is occupied by the Ham People, a people notable for the rich Nok culture that possesses the Nok Terracotta carbon-dated to about 2000–2500 years ago. 'Kwain' (or Kwoi which means 'Community of the United') serves as the political capital of the LGA. It has many villages that include Bitaro, Nok, Kwoi, Zshiek (Kurmin Musa), Dung (also called Jaban Kogo), Chori, Fai, Ketere, Sambang Gida, Sambang Daji, Dura, Ankun, Gora, Kurmi Danagana, Tunga and many other Ham settlements in the Southern parts of Kaduna State [20]. The people of the area are predominantly farmers; they cultivate large quantities of gingers, Digitaria exilis, (popularly called 'acha' or 'hungry rice'), cocoyam, guinea corn, millet and maize among many others.

Awareness talks and enrollment of volunteers
Awareness talks on schistosomiasis, its danger, transmission, control and prevention were delivered in pre-selected/consented primary schools in Jaba LGA. The pupils were informed of the need to volunteer to be part of this study by willingly submitting their urine and blood samples for laboratory diagnoses. Those pupils that volunteered to be part of the study were 505 in number; they were given consent forms to present to their parents/guardians for full permission to enroll them. Confidentiality was applied on all data collected from them and result of laboratory tests was issued to each participated pupil. Those that had infection(s) were immediately referred to the hospital for medical attention.

Urine and blood samples collection
The pupils who consented to participate in the study were briefed and guided on how to collect 10 ml of their urine into provided sterile (wide-mouth) sampling bottles with screw caps between 10 am and 1 pm [21] . Then 2 ml of venous blood were collected into 5 ml EDTA K-3 bottle using new sterile syringe and needle for each volunteered pupil that had submitted a urine sample. The urine samples were screened away from sunlight by enclosing them in dark polythene bags. Both sample types from each pupil were simultaneously labeled and placed into separate ice containers. The samples were taken for analysis at the Bacteriology/Parasitology Laboratory in the Department of Microbiology, Faculty of Science, Ahmadu Bello University Zaria, Nigeria.

Structured questionnaires administration
Those pupils who submitted urine and blood samples were administered structured questionnaires. The questionnaires captured some sociodemographic and risk factors associated with urinary schistosomiasis. Assistance by respective class teachers and head teachers were sought for interpretation from English language into easily understood dialect of the study area.

Method for determination of packed cell volume (PCV)
The blood samples were brought out of the cold container and allowed to reach the room temperature upon arrival at the laboratory. The PCV of each pupil was determined by the microhematocrit centrifuge technique (HCT). Two plain capillary tubes were filled with a blood sample to three-fourth their heights and sealed carefully by means of Bunsen flame to the (2 mm) red demarcation on each tube. The tubes were spun in the microhematocrit centrifuge at relative centrifugation force (RCF) of 12,000–15,000 xg for 5 minutes, after which the PCV were read by correctly adjusting the red-packed-cells columns on the Hematocrit Reader and an average of the two values recorded [21]. Anemic PCV was <34%, normal PCV was between ≥34 and ≤45%, high PCV was ≥46% [22].

Detection and quantification of Schistosoma hematobium eggs in urine
Each urine sample was gently shaken to stir up any sediment in the sampling bottle and transferred into a labeled centrifuged tube. Normal saline was used to rinse the bottle where sediments still remained. Centrifugation was performed at a speed of 3000 rpm for 3–5 minutes and the supernatant was carefully decanted [21]. The sediments obtained in the centrifuge tube was tapped on the bench and mixed by gentle shaking. A Pasteur pipette was used to transfer all the sediments into a clean, grease-free glass slide. A drop of Lugol's iodine solution was added and a cover slip was placed over the wet mount and positioned under the light microscope. The entire wet mount was screened for egg(s) of Schistosoma haematobium using 10x and 40x objectives, while count of eggs/10 ml of urine was taken [21]. Where the sediments from a sample could not be contained in a single wet mount, multiple wet mounts were made from such a sample and the egg counts pooled together.

Statistical analysis
Data collected of socio-demographic and risk factors of urinary schistosomiasis together with laboratory findings were subjected to chi-square (χ²) and likelihood ratio (LR) analyses with the IBM SPSS Statistics Version 21 at p=0.05. Final results were presented in charts and tables.

Out of 505 urine samples of pupils examined, Schistosoma haematobium ova were detected in 62 of the samples with a prevalence of 12.3 % (Figure 1). The eggs of this parasite were yellow-brown, oval in shape with terminal spines; some of the eggs were shorter but majority were slender (Figure 2).

The level of intensity of urinary schistosomiasis was determined by obtaining counts of eggs/10 ml of urine sample and their simple average calculated as shown in (Table 1). The highest mean intensity was found among pupils in Primary 6, followed by those in Primary 4 and Primary 2 respectively. The female pupils in all the classes had higher intensity than the corresponding male pupils. The highest mean intensity in the females was 9.74 eggs/10 ml urine which occurred among the female pupils in Primary 6; whereas that of the males was 2.91 eggs/10 ml urine and it occurred among the male pupils in Primary 4. There was no statistical significance (χ² = 6.850; df = 5; p = 0.232) in the class distribution of the disease, but higher occurrence was obtained in the senior class category (Primary Class 4–6) and lower in the junior class category (Primary Class 1–3).

Gender was a statistically significant factor in the occurrence of urinary schistosomiasis (χ² = 4.926; df = 1; p = 0.026) as indicated in Table 2. There was a remarkable higher occurrence of the infection among the female pupils (15.5%) than in the male pupils (9.1%). Hence, female pupils were about twice more infected with urinary schistosomiasis than the male pupils.

This study found that in an independent t-test pupils within the age of 10.96±2.15 years had statistically significant occurrence of urinary schistosomiasis compared to pupils of 9.70–2.17 years (t = 4.251, df =503, p = 0.000). The occurrence of urinary schistosomiasis increased in a 'wave-like' fashion with rise in the pupils' age. Though the highest occurrence of 62.1% was found among the older pupils of 15 years of age, no occurrence was recorded in pupils within 4-6 years age bracket (Figure 3).

The mean of counts of eggs/10ml urine adopted a 'wave-like' pattern of increase. No egg was detected in urine samples of pupils within 4–6 years age bracket. The mean of counts peaked at age 15 years (Figure 4), which was similar to the age prevalence pattern in Figure 3. However, the Spearman's correlation (r_s) and Pearson product-moment correlation (r) run to determine the relationship between age of pupils and Schistosoma haematobium egg count/10ml of urine (i.e., intensity) in Jaba LGA showed weak, positive correlations, which were statistically significant (r_s = 0.172, P =0.000; r = 0.131, P = 0.003).

The prevalence of urinary schistosomiasis according to sampling locations in Jaba LGA showed high statistical significance (χ² = 38.599; df = 9; p = 0.000). The highest occurrence was found among pupils from Bitaro (23.2%) followed by Ankun (22.2%) and Kwoi (20.3%), whereas no occurrences were recorded among pupils from Nok (0.0%) and Sambang (0.0%) as given in Table 3.

The mean intensity of Schistosoma haematobium eggs in urine samples of pupils from the 10 different sampling locations were analysed by means of ANOVA. Although no statistical significance was obtained (since F = 1.419; df = 9; p = 0.177), the highest means of counts of eggs/10 ml of urine were 6.77 and 4.88 among pupils from the Central Area and Bitaro respectively (Table 3).

The level of urinary schistosomiasis among pupils versus sampling locations showed statistical significance (χ² = 50.094, df = 18, p = 0.000). This was categorized as 'light' and 'heavy' infections, with egg counts of <50 eggs/10 ml and ≥50 eggs/10 ml urine respectively. Light infections occurred most among the pupils from Bitaro (44.2%), followed by those from Kwoi (21.2%) and Ankun (9.6%). Heavy infections were most found among pupils from the Central Area (40.0%), followed by those from Bitaro (30.0%). Light infection was absent among pupils from Nok and Sambang. Also, heavy infection was not found in pupils from Chori, Dura, Gora, Nok and Sambang (Table 4).

Table 5 gives the age-related distribution of level of urinary schistosomiasis among the pupils in Jaba LGA (with χ² = 44.715 df = 22; p = 0.003). Both heavy and light infections occurred mostly in pupils of age 15 years. There was no heavy infection among pupils in age 4, 5, 6, 8, 11 and 14 years. Also, only pupils in age 4, 5 and 6 did not have light infections.

The prevalence of anemia among pupils in Jaba LGA was found to be 8.1%, while 37.6% of the pupils had normal PCV. The remaining study population (54.3%) had abnormally high PCV (Figure 5).

There was a statistically significant association between urinary schistosomiasis and anemia among the pupils (χ² = 11.870; df = 2; p = 0.003). Though anemia was recorded both among those with urinary schistosomiasis and uninfected pupils, a higher occurrence of the anemia (17.7%) was observed in pupils infected with urinary schistosomiasis than those who were not infected (6.8%). The cause of the anemia in the later may be due to other diseases as indicated in Table 6.

Heavy infections with urinary schistosomiasis among the pupils, with a statistical significance (χ² = 12.807; df = 4; p = 0.012) led to higher occurrence of anemia of 20.0% than light infections which caused 17.2% of anemia as indicated in Table 7.

The relationship between the level of urinary schistosomiasis and the gender of the pupils in Jaba LGA was insignificant (χ² = 5.166; df = 2; p = 0.076), but female pupils had higher proportions of light and heavy infections than the male pupils (Table 8).

The level of the urinary schistosomiasis did not influence the onset of (visible) hematuria among the pupils in this study (χ² = 3.105; df = 2; p = 0.212). All the pupils with heavy infections did not present with hematuria. Generally, 4.5% of the pupils presented with hematuria but no eggs of Schistosoma haematobium were recovered; the hematuria may be due to parasitic or other non-parasitic origins. However, 9.6% of the pupils with light infections presented with hematuria (Table 9).

In Table 10, five risk factors of urinary schistosomiasis among school pupils were considered in this study. There was a statistically important association between urinary schistosomiasis and 'Fadama' farming (χ² = 14.300; df = 1; p = 0.000). The pupils that made up the study population were unaware of urinary schistosomiasis. Pupils that wash their clothes in rivers/streams had more infections (14.7%) than those who wash their clothes at home (10.8%).

Appearances of some of the rivers in Jaba LGA of Kaduna State in Nigeria are shown in Plate II. Most of the rivers are surrounded by immediate wet fields locally referred as 'Fadama' for rice, cocoyam and sugarcane farming. The rivers are used for swimming, fishing, irrigation and washing by pupils and the members of the communities. The photograph was taken in the late evening when activities were not on-going.

The level of formal education of the pupils' parents had no statistical link with acquisition of urinary schistosomiasis by their children/wards (p > 0.05). However, lowest detection of Schistosoma haematobium eggs was observed in pupils whose parents did not acquire any formal education. Occurrence of the infection among the pupils increased as fathers' level of formal education increased (Table 11).

From data obtained via administered structured questionnaires on signs and symptoms of urinary schistosomiasis, only painful micturition (χ² = 5.135; df = 1; p = 0.023) and cloudy brown/red-colored urine (χ² = 20.604; df = 4; p = 0.000) had statistical relevance with the disease as shown in Table 12. Even though pupils with fever had more infection with Schistosoma haematobium (22.2%) than those without fever, it was insignificant together with the presence of abdominal pain and frequent urination.

In this study, the presence of urinary schistosomiasis was established by the detection of terminal spine eggs in urine samples of the pupils. Cheesbrough [21] had stated that diagnosis of schistosomiasis is by detection of eggs in urine or stool, which remains the gold standard.

The prevalence of 12.3% for urinary schistosomiasis among the pupils was much lower than many other findings which had claimed an endemicity of schistosomiasis in Nigeria. The prevalence in this study was lower than 31.3% reported in Abuja-Nigeria [22]. Other prevalence reports include 79.4% among children of Ezza-North LGA of Ebonyi, Nigeria [20], 41.5% in Benue-Nigeria [23], 78.4% in Lagos-Nigeria [24], 34.1% in Enugu-Nigeria [25], 48.7% in Borno-Nigeria [26], and 19.5% in Kaduna-Nigeria [27]. Compared to these high-prevalence areas, Jaba LGA had a lower burden of urinary schistosomiasis. This could be due to the fact that the area has relatively fewer fast-flowing streams and rivers that may not provide adequate breeding zone for cercariae and snails (especially Bulinus spp and Physopsis spp). Also many of the streams/rivers in the LGA are used for bathing and washing of clothes by many members of the communities. Detergents and soaps have adverse effects on cercariae/snails; hence these agents help in shortening the lifecycle and propagation of cercariae [28].

Also, this study uncovered a lesser prevalence of urinary schistosomiasis as compared to 15.2% prevalence reported in Mali by [29]. A prevalence of 20.7% was found in a retrospective study in Kumasi [30] and 30.7% had also been reported in Ghana [31]. A considerably higher prevalence of 35.9% was found in Ethiopia [32], and a prevalence of 42% among primary school children in South Africa [33]. Although a relatively low prevalence was obtained in this study, it is still higher than reported 4.5% prevalence in Abini and the absence of the infection in Ukwelo-Obudu communities of Cross River-Nigeria [34], and reported 6.3% prevalence among children of Ngbo-West LGA in Ebonyi-Nigeria [20], and 8.3% in Kano-Nigeria [35].

The statistically significant higher prevalence (of 15.5%) of urinary schistosomiasis amongst the females than in the males (9.1%) in this study is among a few reports of higher occurrence of schistosomiasis amongst the females. This finding supports the work of Oluwasogo and Fagbemi [24], in which females (60.9%) were more infected than males (39.2%). But this observed phenomenon opposes many findings which had suggested higher risks on the males [19] [22] [25][27][36]. Most of those studies that had implicated the male gender with higher risk of Schistosoma infections had been conducted in locations where the females were restricted from swimming activity. In Jaba LGA, both the females and the males had no traditional/religious restrictions from participating in swimming activity. In addition, there was an unequal exposure risks between the genders; females participated more in rice farming and other 'Fadama' activities. Individuals with heavy infections are most prone to chronic complications [37]. By extension, the females are not only at a higher risk of developing complications like female genital schistosomiasis (FGS), but they stand the risks of decreased fertility, abortions, vaginal discharge, contact bleeding and increased risk of HIV infection in concomitant urinary schistosomiasis [38].

Many reports on the prevalence of schistosomiasis had focused on age-group prevalence. This type of disease-reporting has not explained the occurrences in each age. Furthermore, conclusions made on an age-group may not adequately define a particular age characteristics. Hence, in this study the prevalence of urinary schistosomiasis for each age was calculated, which gave a 'wave-like' pattern of elevation with increase in ages of the pupils. The absence of the infection in pupils within ages 4, 5 and 6 years (unlike the older pupils) could be due to the fact they are too young to engage in constant water-based activities like swimming, wadding or 'Fadama' farming. Older pupils can engage freely and/or indiscriminately in water activities [36].

Aside the obviously high prevalence of urinary schistosomiasis in the females, this study revealed a higher percentage of heavy infections among the females (70.0%) than among the males (30.0%). The highest mean intensity of 9.74 eggs/10 ml urine among the females occurred among pupils in Primary 6; however, in the males it was 2.91 eggs/10 ml urine found among pupils in Primary 2. In an overall, the females had higher mean intensity (of 4.18 eggs/10 ml urine) than males (1.22 eggs/10 ml urine). An inclusion of behavioral difference between the genders could be used to explain reasons for the higher intensity/level of urinary schistosomiasis among the female pupils. Schistosomes are attracted to skin lipids [13] and since females (including those that are pupils) often apply high-scented perfumes, body creams and oils, they stand a higher chance of been repeatedly infected during water-contact activities. Though Bigwan et al. [36] had linked a higher prevalence of schistosomiasis in males to some socio-cultural practices such as bathing, washing, swimming, irrigation-farming and fishing in rivers/ponds, the reverse was the case in this study. Repeated infection episodes enhance the development of heavy infection/high intensity.

A proportion of pupils in each Primary class in Jaba LGA had urinary schistosomiasis; however, there were increases in both prevalence and intensity of the infection from junior classes (Primary 1–3) to senior classes (Primary 4–6). Though there was no statistical significance in those relationships, the observed increases could have been due to more water-contact activities among the older pupils. It shows further that urinary schistosomiasis is unrelated to the class of a pupil as a risk factor.

The highest occurrence of urinary schistosomiasis among pupils in Bitaro, Ankun and Kwoi could be due to more availability of rivers/streams and the dense water-contact activities among the pupils compared to other locations. Pupils in Sambang and Nok recorded an absence of the infection with fewer rivers/streams and reduced water-contact activities among the pupils; members of these two communities depend largely on borehole and well water. High water-contact activities, promotes a higher risk of contracting the infection. However, the highest mean count of S. haematobium eggs (of 6.77/10 ml urine) was found in the Central Area and not in the location of higher occurrence of the infection. Hence, high prevalence of the infection did not coincide with high intensity of infection because repeated exposure is required to enhance the development of a heavy infection or high intensity.

The overall occurrence of 2.0% heavy infections, 10.3% light infections and egg count ranging between 0–204 eggs/10 ml urine among the pupils in Jaba LGA was far less than the range of 21–1138 eggs/10 ml urine and 62.7% heavy infections reported by Ossai et al. [26]. This further indicated that pupils in Jaba LGA had relatively low level of urinary schistosomiasis. Nevertheless, the infected population continues to pose risk to other uninfected pupils and members of the community. This will also gradually increase the cost of personal and public health maintenance.

The 8.1% prevalence of anemia among the pupils could have resulted from multiple sources: dietary deficiency of iron, leukemia, heavy loss of blood and/or parasitic diseases. It has been noted that hematological indices of apparently healthy individuals can be affected by certain factors like age, gender, cultural background, nature of body build, social activities, nutrition, altitude and other environmental factors [39]. One of such hematological parameters considered in this study was PCV and classified as 'anemic', 'high' or 'normal' [21]. With statistical relevance, urinary schistosomiasis caused and/or enhanced the development of anemia among the pupils. Pupils who become recurrently infected may develop anemia, malnutrition and even learning difficulties [40]. The anemia can be related to the cumulative loss of blood in terminal hematuria associated with the disease [28] as well as the continuous feeding on glucose and blood products by schistosomes [37]; making urinary schistosomiasis a chronic symptomatic disease [41].

Though schistosomiasis has been reckoned as of one of the world's most prevalent public health problems [36] and Nigeria stands as one of Africa's most endemic countries [27] [42], with several control/intervention programmes the prevalence of urinary schistosomiasis seemed not to be decreasing. This is partly due to improper implementation of the control measures, unawareness and increased water-contact activities among members of rural communities. In this study, pupils who wash their clothes in rivers/streams had higher occurrence of the infection than those who wash at home.

The pupils who did not participate in swimming activities were more infected (15.2%) than those who were swimmers (accounting for 10.7%), but it was not statistically significant. Some other studies [27] [35] had positively associated schistosomiasis with water-contact activities (like swimming) in river/stream. The population in this study might have acquired most the infections through other water-based activities such as washing or wading in rivers/streams or irrigation farming, indicating that the disease has multiple means of transmission via skin or body contact with cercariae-infested water.

Pupils' parents' level of formal education did not show any statistical relationship with urinary schistosomiasis in them. However, the lowest prevalence was observed among pupils whose parents did not have any formal education. Perhaps, the tight working schedules of educated parents and late return from work gave their children/wards opportunities to indulge in unsafe water-contact activities. Pupils whose mothers attained tertiary education had lower infection. However, the prevalence of the infection increased steadily among the pupils as their fathers' level of formal education increases. This finding did not agree with the work of Houmsou et al. [23] who reported that children whose parents did not attain any formal education as well as those with primary education recorded the highest prevalence of urinary schistosomiasis.

Some symptoms could be useful in the diagnosis of urinary schistosomiasis. Red/brown-colored urine (a sign of hematuria) and painful micturition witnessed by some of the subjects in study statistically indicated their associations with the disease. The association of hematuria with urinary schistosomiasis had been emphasized by many researchers [35] [43] and described as a classic or main sign/symptom of the disease [2] [44]. Pains suffered during urination by infected pupils are direct effects of tissue inflammation, destruction of internal vesical or ureterovesical sphincter mechanism or minor granulomata due to immunological reactions to both schistosomes and their eggs [37] [45] [46][47].

The completely zero-level of awareness of schistosomiasis among pupils in Jaba LGA is indicative of negligence of the disease in Nigeria, a characteristic that defines it as a 'neglected tropical disease (NTD)' in the condition of poverty [2]. Hence, unawareness was a constant, and remains a strong risk factor in the continuous spread of the infection. This opposes the considerable awareness of 74.5% by pupils in rural communities of Kano State, Nigeria [37] where a lower prevalence of 8.3% was obtained as against the 12.3% prevalence obtained in this study with complete unawareness of the infection and its risks. The pupils in Jaba LGA are at continued risk of getting infected because of unawareness and continuous engagement in activities in cercariae-infested-water bodies. But it is anticipated that the organized awareness talks on schistosomiasis in pre-selected schools for this study will help in reducing the risks of exposure on enlightened pupils.

Jaba LGA is considerably an area of mild burden of urinary schistosomiasis, accounting for prevalence of 12.3%. Female pupils from the LGA had higher prevalence and intensity of the disease. Hence, they are faced with heightened risks of developing some complications like female genital schistosomiasis (FGS) and irreversible infertility. Prevalence and intensity of urinary schistosomiasis had 'wave-like' patterns of increase with rise in the ages of pupils. Anemia can result due to urinary schistosomiasis, a condition which can be severe with high worm burden. One of the basic factors promoting the continuous spread of schistosomiasis is lack of awareness of the disease, as more children stand at risk in most communities in Jaba LGA. 'Fadama' farming, painful micturition and red/brown-colored urine were statistically associated with urinary schistosomiasis among the study population. In view of the impacts of urinary schistosomiasis on health/development of African children, concerted efforts by government, school authorities, parents and researchers should be intensified in the control and prevention of the infection; treatment of infected/risk groups and early reporting of research/case findings should be encouraged.

We express our appreciation to all the pupils, parents and the management of every primary school that voluntarily partook in this study. We equally thank Mr. Joseph Shedow and Mrs. Doris Hassan Dala for their contributions to the success of this study in Jaba LGA, Kaduna State, Nigeria.

1. Osada Y, Kanazawa T. Schistosome: Its benefit and harm in patients suffering from concomitant diseases. J Biomed Biotechnol 2011;2011:264173.   [CrossRef]   [Pubmed]    
2. World Health Organisation. Schistosomiasis. Fact Sheet. 2016. [Available at: http://www.who.int/mediacentre/factsheets/fs115/en/]    
3. Pearce EJ, MacDonald AS. The immunobiology of schistosomiasis. Nat Rev Immunol 2002 Jul;2(7):499–511.   [CrossRef]   [Pubmed]    
4. Cox FEG. Modern Parasitology: A Text Book of Parasitology, 2ed. Germany: Backwell Science Limited; 2004.    
5. Noble ER, Glem AN. Biology of Animal Parasites, 5ed. Philadelphia, USA: Lea and Febiger; 1982. P. 157–8.    
6. Ibironke O, Koukounari A, Asaolu S, Moustaki I, Shiff C. Validation of a new test for Schistosoma haematobium based on detection of Dra1 DNA fragments in urine: Evaluation through latent class analysis. PLoS Negl Trop Dis 2012 Jan;6(1):e1464.   [CrossRef]   [Pubmed]    
7. Kanwai S, Ndams IS, Kogi E, Gyem ZG, Hena JS. Urinary schistosomiasis infection in Dumbin Dustse, Igabi Local Government Area, Kaduna State, Nigeria. Science World Journal 2011;6(3):1–3.    
8. Elele K, Ewurum N. Current Status of Urinary Schistosomiasis in Four Communities (Obedum, Anyu, Amerikpoko, and Odau) In Abual/Odual, Rivers State, South-South, Nigeria. Reiko International Journal of Science and Technology 2013;4(2).    
9. Rollinson DA, Southgate VR. The genus Schistosoma: A taxonomic appraisal. In: Rollinson D, Simpson AJ eds. The Biology of Schistosome: from Genes to Latrines. London: Academic Press: 1987. p. 1–49.    
10. Jamjoom MB. Molecular identification of some Schistosoma mansoni isolates in Saudi Arabia. World Journal of Medical Sciences 2006;1(2):102–7.    
11. Clerinx J, Soentjens P. Epidemiology, pathogenesis, and clinical manifestations of schistosomiasis. 2015. [Available at: http://www.uptodate.com/contents/epidemiology-pathogenesis-and-clinical-manifestations-of-schistosomiasis]    
12. Barsoum RS. Urinary schistosomiasis: Review. J Adv Res 2013 Sep;4(5):453–9.   [CrossRef]   [Pubmed]    
13. Sakanari JA, Mckerrow JH. Medical Parasitology. In: Brooks GF, Carroll KC, Butel JS, Morse SA, Mietzner TA eds. Jawertz, Melnick and Adelberg's Medical Microbiology. 25ed. US: McGraw Hill Companies Inc.; 2010. p. 665–701.    
14. Rollinson D. A wake up call for urinary schistosomiasis: Reconciling research effort with public health importance. Parasitology 2009 Oct;136(12):1593–610.   [CrossRef]   [Pubmed]    
15. Rinaldi G, Okatcha TI, Popratiloff A, et al. Genetic manipulation of Schistosoma haematobium, the neglected schistosome. PLoS Negl Trop Dis 2011 Oct;5(10):e1348.   [CrossRef]   [Pubmed]    
16. Brindley PJ, Hotez PJ. Break Out: Urogenital schistosomiasis and Schistosoma haematobium infection in the post-genomic era. PLoS Negl Trop Dis 2013;7(3):e1961.   [CrossRef]   [Pubmed]    
17. Chidozie EU, Duniyan SY. Urinary schistosomiasis epidemiological survey of urinary schistosomiasis among children in selected schools: A preliminary study in Minna, Nigeria. African Journal of Biotechnology 2008;7(16):2773–6.    
18. World Health Organisation. Report of the WHO informal consultation on Schistosomiasis Control. Genera, 2-4 December, 1998. Geneva: WHO/CDS/CPC/SIP/99.2. 1999. [Available at: http://apps.who.int/iris/bitstream/10665/65978/1/WHO_CDS_CPC_SIP_99.2.pdf]    
19. Uneke C, Ugwuoke-Adibuah S, Nwakpu K, Ngwu B. An Assessment of Schistosoma haematobium infection and urinary tract bacterial infection among school children in rural eastern Nigeria. The Internet Journal of Laboratory Medicine 2009;4(1):1–6.    
20. http://nokculture.com/    
21. Cheesbrough M. District Laboratory Practice in Tropical Countries, Part I, 2ed. Cambridge, UK: Cambridge University Press; 2009.    
22. Ifeanyi CIC, Matur BM, Ikeneche NF. Urinary schistosomiasis and concomitant bacteriuria in the Federal Capital Territory Abuja Nigeria. New York Science Journal 2009;2(2):1–8.    
23. Houmsou RS, Amuta EU Sar TT. Profile of an epidemiological study of urinary schistosomiasis in two local government areas of Benue State, Nigeria. International Journal of Medicine and Biomedical Research 2012;1(1):39–48.    
24. Oluwasogo OA, Fagbemi OB. Prevalence and risk factors of Schistosoma haematobium infections among primary school children in Igbokuta Village, Ikorodu North Local Government, Lagos State. IOSR Journal of Nursing and Health Science 2013;2(6):62–8.    
25. Ossai OP, Dankoli R, Nwodo C, et al. Bacteriuria and urinary schistosomiasis in primary school children in rural communities in Enugu State, Nigeria, 2012. Pan Afr Med J 2014 Jul 21;18 Suppl 1:15.   [CrossRef]   [Pubmed]    
26. Balla HJ, Babaganal Baba S, Ibrahim H. Incidence of urinary schistosomiasis among out-of-school pupils and "Almajiris" in Dikwa, North Eastern Nigeria. Global Journal of Medical Research 2015;15(2):9–13.    
27. Omenesa HO, Bishop HG. Raji HM. Prevalence of Urinary Schistosomiasis among Pupils Attending Primary Schools in Bomo Village, Zaria-Nigeria. International Journal of Research in Engineering and Science 2015;3(5):14–9.    
28. Grimes JE, Croll D, Harrison WE, Utzinger J, Freeman MC, Templeton MR. The relationship between water, sanitation and schistosomiasis: A systematic review and meta-analysis. PLoS Negl Trop Dis 2014 Dec 4;8(12):e3296.   [CrossRef]   [Pubmed]    
29. Dabo A, Badawi HM, Bary B, Doumbo OK. Urinary schistosomiasis among preschool-aged children in Sahelian rural communities in Mali. arasit Vectors 2011 Feb 21;4:21.   [CrossRef]   [Pubmed]    
30. Tay SCK, Amankwa R, Gbedema SY. Prevalence of Schistosoma haematobium infection in Ghana: A retrospective case study in Kumasi. International Journal of Parasitology Research 2011;3(2):48–52.    
31. Tetteh-Quarcoo PB, Attah SK, Donkor ES, et al. Urinary schistosomiasis in children-Still a concern in part of the Ghanaian capital city. Open Journal of Medical Microbiology 2013;3:151–8.    
32. Geleta S, Alemu A, Getie S, Mekonnen Z, 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. Parasit Vectors 2015 Apr 10;8:215.   [CrossRef]   [Pubmed]    
33. Samie A, Nchachi DJ, Obi CL, Igumbor EO. Prevalence and temporal distribution of Schistosoma haematobium infections in the Vhembe district, Limpopo Province, South Africa. African Journal of Biotechnology 2010;9(42):7157–64.   [CrossRef]    
34. Ingang-Etoh PC, Essien UC, Amama SA, Useh MF. Prevalence of urinary schistosomiasis among school children in Ukwelo-Obudu and Abini communities in Cross River State, Nigeria. Port Harcourt Medical Journal 2009;3(3).   [CrossRef]    
35. Dawaki S, Al-Mekhlafi HM, Ithoi I, et al. The Menace of Schistosomiasis in Nigeria: Knowledge, Attitude, and Practices Regarding Schistosomiasis among Rural Communities in Kano State. PLoS One. 2015 Nov 25;10(11):e0143667.   [CrossRef]   [Pubmed]    
36. Bigwan EI, Kunihya, RZ, John TJ. Epidemiological survey of urinary schistosomiasis among primary school children in Michika, Adamawa State, North-Eastern Nigeria. International Journal of Current Research and Review 2013;5(5):111–6.    
37. Leder K, Weller PF. Epidemiology, pathogenesis and clinical features of schistosomiasis 2011. [Available at: http://cursoenarm.net/UPTODATE/contents/mobipreview.htm?37/42/38560?source=see_link]    
38. Kjetland EF, Leutscher PD, Ndhlovu PD. A review of female genital schistosomiasis. Trends Parasitol 2012 Feb;28(2):58–65.   [CrossRef]   [Pubmed]    
39. El-Hazmi MA, Warsy AS. Normal reference values for hematological parameters, red cell indices, HB A2 and HB F from early childhood through adolescence in Saudis. Ann Saudi Med 2001 May-Jul;21(3-4):165–9.   [Pubmed]    
40. Centers for Disease Control and Prevention (CDC). Parasite-Schistosomiasis. 2012. [Available at: http://www.cdc.gov/parasites/schistosomiasis/biology.html]    
41. King CH. It's time to dispel the myth of "asymptomatic" schistosomiasis. PLoS Negl Trop Dis 2015 Feb 19;9(2):e0003504.   [CrossRef]   [Pubmed]    
42. Chitsulo L, Engels D, Montresor A, Savioli L. The global status of schistosomiasis and its control. Acta Trop 2000 Oct 23;77(1):41–51.   [CrossRef]   [Pubmed]    
43. Morenikeji O, Quazim J, Omoregie C, et al. A cross-sectional study on urogenital schistosomiasis in children; haematuria and proteinuria as diagnostic indicators in an endemic rural area of Nigeria. Afr Health Sci 2014 Jun;14(2):390–6.   [CrossRef]   [Pubmed]    
44. Van der Werf MJ, de Vlas SJ. Diagnosis of urinary schistosomiasis: A novel approach to compare bladder pathology measured by ultrasound and three methods for hematuria detection. American Journal of Tropical Medicine and Hygiene 2004;7(1):98–106.    
45. Elbaz T, Esmat G. Hepatic and intestinal schistosomiasis: Review. J Adv Res 2013 Sep;4(5):445–52.   [CrossRef]   [Pubmed]    
46. Botelho MC, Figueiredo J, Alves H. Bladder cancer and urinary Schistosomiasis in Angola. J Nephrol Res 2015 Jun;1(1):22–4.   [CrossRef]   [Pubmed]    
47. Botelho MC, Machado JC, Brindley PJ, Correia da Costa JM. Targeting molecular signaling pathways of Schistosoma haemotobium infection in bladder cancer. Virulence 2011 Jul-Aug;2(4):267–79.   [CrossRef]   [Pubmed]