Soil-transmitted helminthic infections and schistosomiasis are among the widely spread chronic infections in the world. Globally, two billion individuals are infected with helminths, out of the majorities living in resource-poor settings (Noyer and Brandt, 1999; WHO, 2002). World Health Organization (WHO) estimated that 1.45 billion people are infected with Ascaris lumbricoides, 1.3 billion with hookworms and 1.05 billion with Trichuris trichiura (WHO, 2002). Schistosomiasis is endemic in 76 countries and also it is one of the public health concerns in developing countries. Approximately 90% of the estimated 207 million cases of human schistosomiasis living in sub-Saharan Africa (Hotez and Kamath, 2009), with Schistosoma haematobium the most widespread of the causative parasites (Steinmann et al., 2006). Within sub-Saharan Africa, Nigeria is the country with the most cases of human schistosomiasis, about 29 million in 2008 (Hotez and Kamath, 2009).

The occurrence of helminthic infections is associated with socio-economic, environmental and other factors like ignorance of simple health promoting factors and overcrowding, limited access to clean water, tropical climate and low altitude (WHO, 2002). School-aged children are one of the groups at high risk for intestinal parasitic infections. Factors like poor development of hygienic habits, immune system and over-crowding contributes for infection (Jarabo et al., 1995). School-aged children are the most severely affected by polyparasitism with intestinal parasites and Schistosoma haematobium and continue to bear the greatest health burdens due to the infections (Drake and Bundy, 2001). The adverse effects of intestinal parasites among children are diverse and alarming. Intestinal parasitic infections have detrimental effects on the survival, appetite, growth and physical fitness, school attendance and cognitive performance of school age children (Nokes and Bundy, 1993; Stephenson et al., 1993; de Silva et al., 1997; Hadidjaja et al., 1998).

In Nigeria, intestinal parasitic infections and urinary schistosomiasis continue to constitute a major public health and developmental challenge especially among school-aged children. Several reports illustrated that ascariasis is the most prevalent intestinal parasitic infection in different communities usually occurring together with trichuriasis. Intervention against soil-transmitted helminths (STH) and Schistosoma infections are based on regular anti-helminthic treatment, improved water supply, sanitation and health education (World Bank, 2003; Albonico et al., 2006). Polyparasitism of STH and Schistosoma infections have been reported from various epidemiological settings in Africa (Tchuem Tchuenté et al., 2003; Mazigo et al., 2010; Alemu et al., 2011).

Recent studies on intestinal helminthiases and schistosomiasis from Nigeria include those of Agbolade et al. (2007), Ugbomoiko and Ofoezie (2007) and Uneke et al. (2008), however, current prevalence of STH and schistosomiasis was not well addressed in different parts of Nigeria including our present study area. Therefore, the aim of this study was to determine the prevalence and intensity of soil-transmitted helminths and S. haematobium infection among school children in Saki town, Oyo State Southwest Nigeria. It is hoped that the findings of the investigation will contribute to effective disease control planning and implementation in the area of study and others in Nigeria and other tropical countries with similar heavy burdens of infectious disease.

Statistical analysis

Differences in the prevalence of each parasite infection among subgroups were determined using chi-squared values from the contingency tables. Variations in mean egg counts between dichotomous variables were assessed with the student-test and One-way analyses of variance (One way-ANOVA) for explanatory variables with more than two levels. All analyses were performed using SPSS for windows version 17.

Overall infection patterns

The composition of the study population by school and sex is summarized in Table 1. In total, 956 (62.2%) children harboured at least one parasitic infection. Four species of intestinal helminths, namely, A. lumbricoides, hookworm, T. trichiura and S. haematobium were recovered from the children investigated. The overall prevalence of A. lumbricoides, hookworm, T. trichiura and S. haematobium were 39.6, 18.3, 12.9 and 32.7%, respectively with corresponding intensities of 2417.9±186.2, 192.9±19.3, 137.4±17.8 eggs per gram of faeces and 24.5±1.9 eggs per 10 ml (Table 2).

Children from LA Primary School, Ape-Abe recorded the highest prevalence of intestinal helminth infection (70.4%) which was significantly higher than the prevalence of other schools (c²=17.942 df=4, p=0.001). The lowest prevalence of helminth infection (55.0%) was recorded among the children attending LA Primary School, Taba. There was no significant difference in the overall prevalence of infection between the genders (prevalence in males=61.3%; females=63.0%).

Infection patterns relative to gender and schools

Children attending LA Primary School, Isia had the highest prevalence of ascariasis (48.0%) while the lowest prevalence of 33.2% was recorded among children attending LA Primary School, Agolabi (Table 3). There was a significant difference in prevalence and intensity of Ascaris infection between males and females among the children attending primary school at Apa-Abe and Isia (P < 0.05). Also, differences in the prevalence reached significant levels for hookworm in both sexes among children attending LA Primary School, Agolabi. The prevalences and intensities of other infections were comparable within each school (Table 3).

The pattern of schistosome infection was such that the prevalence and intensity were higher in males than in females (although the differences were not statistically significant) among children attending schools at Isia, Sango and Taba, while reverse was the case for children attending schools at Apa-Abe and Agolabi (Table 3).

Age and gender patterns of infection

The age and gender distribution of intestinal helminth infections in the schools investigated are presented in Table 4. Prevalence values of the four observed parasites, that is, A. lumbricoides (23.3 to 48.8%), hookworm (12.6 to 24.0%), T. trichiura (5.7 to 16.7%) and S. haematobium (22.6 to 39.3%), were more of age than gender dependent. While gender-dependent distribution of infections was comparable and followed no clear cut patterns in all age groups except those in 9 to 10 years old and 13 to 14 years for T. trichiura and hookworm, respectively, and age dependent patterns were pronounced. For both Ascaris and hookworm infections, the prevalence increased from the youngest age-group to a peak in the 7 to 8 years old for Ascaris and 13 to 14y ears for hookworm. While for T. trichiura and S. haematobium, the lowest prevalence of infection was recorded in the oldest age group (15 to 16 years old). There was no definite pattern of intensity of infection. A significant gender-dependent intensity pattern was recorded for hookworm and T. trichiura infections among 13 to 14 years old and 15 to 16 years old, respectively (P < 0.05).

Multiple infection patterns

More than half (62.2%) of children were infected with at least one of the four parasites, while 35.5% had single infection, 54.3% had double infections, 17.7% had triple infections and 3.1% had four parasites. From the infected children, 57.0, 87.2, 28.5 and 4.9% harboured single, double, triple and four parasites, respectively. The most common double infection was the Ascaris and S. haematobium combination which accounted for 28.9%. This was followed by Ascaris/hookworm (16.3%) and Ascaris/T. trichiura (12.3%). The least occurring combination for hookworm and T. trichiura accounted for 7.9%. Of 272 (28.5%) observed triple infections, Ascaris, hookworm and S. haematobium combination accounted for 10.6%. Each of the combination of T. trichiura, hookworm and S. haematobium; and Ascaris, T. trichiura and hookworm accounted for 4.7%. The only four parasite species infection of Ascaris, hookworm, T. trichiura and S. haematobium combination accounted for 4.9%.  The  prevalence  of  dual  infections  did  not  differ significantly by gender (p>0.05). Male children had the highest prevalence of triple infections (29.6%) compared to 27.4% of the females.

The findings from the current study confirm that Saki town in Southwest Nigeria is highly endemic for urinary schistosomiasis and soil-transmitted helminthiasis (STH). Although intestinal helminth parasites particularly STH and schistosomes infections are neglected diseases that occur predominantly in rural areas, the deplorable social and environmental conditions as well as inadequate basic amenities in the urban poor communities and the so-called peri-urban areas of developing countries including Nigeria are ideal for the persistence of these parasites (Drake and Bundy, 2001; WHO, 2002).

From the study, about two out of every three school children in the town were infected with one or more parasitic infections (ascariasis, hookworm, trichuriasis and schistosomiasis). In terms of prevalence and intensity, ascariasis appears the most important public health problem in the area of study. Its overall prevalence (39.6%) is more than double the national average (18%) (Crompton et al., 1989). However, while the patterns of infection of hookworm, trichuriasis and schistosomiasis suggest a lesser public health importance, in reality they have a serious public health implication for the community. For instance, an overall prevalence of 32.7% for S. haematobium infection is more than 2.5 times for the national average (13.1%) (Ofoezie, 2002).

A cross-sectional survey conducted on STH among pre-school and school-aged children in Ile-Ife, Osun State, Nigeria (Sowemimo and Asaolu, 2011) reported that the overall prevalence of infection was 34.4% which is lower than the prevalence of 51.2% recorded in this study. Other study conducted on intestinal helminthic infections in school-aged children in Ilie in Olorunda Local Government Area of Osun State, Southwest Nigeria (Adefioye et al., 2011) reported overall prevalence of 52.0% for STH infection which is comparable to 51.2% recorded in this study. A. lumbricoides was reported to be the most prevalent parasite (36.2%) followed by hookworms (10.5%). This is similar to the result obtained in this study where Ascaris (39.6%) was the most frequently encountered parasite. The differences in prevalence among the different communities might be associated with environmental sanitation, water supply and socioeconomic status of households, although this needs to be verified in more extensive follow up studies. Other factors related to macro- and micro-environment, time of study, method of examination, etc., do also contribute to the differences in the prevalence and distribution of these intestinal helminths. No significant difference was obtained in infection rates between the genders of schoolchildren under consideration. This denotes a similar exposure risk to infection by these helminths and it is in agreement with previous study from Ethiopia (Alemu et al., 2011).

The high prevalence of STH and S. haematobium infections recorded among school children of the study area raises a serious concern. It signifies the fact that children are the highest risk groups in the community and serve as sources of infection and transmission. These parasites are well known to be associated with lowered work capacity and productivity both in children and adults and increased susceptibility to other infections. Helminths also impair the mental and physical development of children (Jardiam-Batelho et al., 2008). Again majority of wormy children are not only infected with one species of worm, but they also tend to harbour the heaviest burdens and almost two-thirds of children were infected with one or more helminths.

In this study, STH and S. haematobium were co-endemic in the study area. Previous studies have clearly documented the relationship between intestinal helminth infections, polyparasitism and cognitive functions, growth and malnutrition among school children (Partnership for Child Development, 2002; Jardian-Batelhoet al., 2008). Children with multiple parasitic infections especially those with heavy infections intensity tend to experience more severe cognitive outcomes and other health problems such as malnutrition than children with only one helminth infection (Sakti et al., 1999; Jardian-Batelho et al., 2008). Studies conducted throughout Africa and China indicate that most parasitic infections do not occur singly, but as co-infections (Raso et al., 2004; Ugbomoiko and Ofoezie, 2007; Steinmann et al., 2008). Hence, co-infections of soil-transmitted helminths and S. haeamtobium could partly be attributed to the co-endemicity of these intestinal helminths in the study area and poor sanitations.

In this study, the most common double infection was the combination of Ascaris and S. haematobium with a prevalence of 28.9%. This is in contrast with the observation of Agbolade et al. (2007) who reported the combination of Ascaris and hookworm to be the most common double infection. Agbolade et al. (2007) also reported that the most common triple infections were the combination of Ascaris, hookworms and Trichuris. This is in contrast with the findings in this study where the combination of S. haematobium, Ascaris and hookworm were the most common triple infection. This finding indicates that S. haematobium is more endemic than T. trichiura in the area of study.

In conclusion, the prevalences of STH and S. haematobium were quite high and they account for major health problem in the study area. There is the need for a control measures such as deworming programmes coupled with provision of improved water supplies and sanitation to be put in place in order to bring about reduction in the prevalence level of both diseases. There is also an urgent need for concerted efforts towards ensuring adequate control of intestinal helminthiasis and schistosomiasis in Saki town, Oyo State by the authority concerned and the community at large. 

The authors appreciate the school children, their teachers and parents/guardians for their cooperation during the study. They are also grateful to Miss Grace Owoeye for typing the manuscript.

The author declared he has no conflict of interest.