Introduction

It is estimated that more than one billion of the world's population is chronically infected with soil-transmitted helminths, and 200 million are infected with schistosomiasis [1]. The high prevalence of these infections is closely correlated with poverty, poor environmental hygiene, and impoverished health services [1],[2]. Parasitic helminths are known causes of morbidities such as nutritional deficiency [3], impaired physical development and learning ability [4], and socioeconomic deprivations in populations living in the tropics where poor hygiene conditions provide an optimal environment for their development and transmission [5]–[7]. In many parts of the developing world, children are reported to have an intestinal helminth infection prevalence rate ranging between 50% and 80% [8],[9]. Although several studies indicate that intestinal helminth infections are highly prevalent among schoolchildren in Ogun State, Nigeria [10]–[13], there is no reported statewide prevalence for intestinal helminths except for ascariasis [13]. Also there are no available data about the demography and hygiene conditions of the state's schools to help guide the development of school health programmes, which are a requirement for sustainable control of soil-transmitted helminths in schoolchildren [14].

At present there is no National School–based parasite or soil-transmitted helminth control programme in Nigeria. In the past, there have been sporadic and uncoordinated deworming programmes untaken by government officials without any baseline information or data. The present study has three aims: first, to evaluate demographic features and intestinal helminth infections among schoolchildren; second, to investigate hygiene conditions in schools; and third, to identify factors that are essential in the development of sustainable school health programmes.

Materials and Methods

Results

Demography

A total of 257 schoolchildren attending the three schools were analyzed for demographic characteristic (Figure 1). The age distribution was not proportional in the study area, as the number of children was decreasing as their age's increases with progress in school. Of the 257 students total, 146 (56.8%) were boys and 111 (43.2%) were girls. The sex ratio by class level was proportional until primary level 3, after which the number of females gradually decreased in the urban government school, while in the rural government and the urban private schools, schoolchildren were proportionally distributed between sexes even in the higher class levels (Figure 1).

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Figure 1. Demographic Characteristics of Schoolchildren in Government-Owned Urban and Rural Schools and an Urban Private School, Ikenne Local Government Area, Ogun State, Nigeria.

The pair of bars on the right show age frequency data grouped by sex for an urban privately owned school. *The pair of bars on the left and in the center show data from an urban and a rural government school, respectively.

https://doi.org/10.1371/journal.pntd.0000146.g001

Hygiene conditions of schools

The hygiene condition of the three schools differed in several ways. Available water supply, presence of garbage around school compounds, conditions of latrines, and presence of soap in classrooms were different in the three schools (Table 1). These conditions were poorer in government-owned schools than in the private school. The water supply was inadequate in both government-owned schools; tap water was not constant, mostly twice a week and at times once a week in urban and rural government schools, respectively. Pupils brought bottle of water to school from their homes. In the private school, the water supply was regular, from a borehole. Pupils drank water using personal cups from the containers in their classes.

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Table 1. Description of Hygiene Condition Indicators in the Three Schools.

https://doi.org/10.1371/journal.pntd.0000146.t001

The toilet facilities in government-owned schools were in poor condition. The government-owned schools are equipped with pit latrines constructed through contracts. In each government-owned school, there were four pit latrines: two for boys, one for girls, and one for the teachers. The pit latrines for the schoolchildren were so dirty that the pupils preferred to defecate in vegetation surrounding the school compounds; and there were no basin and soap for handwashing after using the toilet. In the private school, the toilet facility was a water closet system, cleaned by a cleaner employed by the school, and water was provided at regular intervals for flushing the toilets.

There were many garbage piles around the school compounds in the government-owned schools, and schoolchildren were seen playing and digging around the garbage. The garbage piles included mainly waste paper, food wrappings, industrial water sachets (50 cl polyethylene bags containing water), dry leaves, and other matter produced regularly both in classrooms and outside the classroom. Garbage cans were also absent in these schools. The private school was an exception (although some waste paper was found in the classrooms), and there was garbage can inside the school premises.

Food vendors were present in the three schools; in rural and urban government schools vendors served pupils in their classrooms, while in private schools most pupils brought their own food to school from home. Inspection of food vendors was not done in the three schools. Foods items served by vendors in the urban were snacks such as meat pies, donuts, and groundnuts (peanuts). In all schools vendors served local dishes such as rice, beans, stew, and roasted meat known as “suya.”

Helminth infections

A total of 257 stool containers were distributed, and 232 (90.3%) were returned; 25 (9.7%) of the schoolchildren refused to submit a stool sample and therefore did not participate in the infection study. Compliance was 85.1% in the rural government school (A.U.D. Primary School, Irolu), 88.2% in the urban private school (El-Shaddai Nursery and Primary School, Ilisan), and 96.8% in the urban government school (Salvation Army Primary School, Iperu). Compliance was higher among lower-grade-level schoolchildren but decreased among higher-grade-level children in the the study area. In total, 232 schoolchildren were examined for intestinal helminth infection, and 116 (50.0%) were found to be infected with one or more helminths. The prevalence of helminth infections varied significantly (χ² = 18.85, df = 2, p<0.0005) among schoolchildren in the three schools. Prevalence rates were 63.5% in the rural government school, 54.9% in the urban government school, and 28.4% in the urban private school. Multiple infections were higher in the rural government school than in the urban government school, and no multiple infections were found in the private school. Ascaris lumbicoides was the most common infecting species in the three schools, while the prevalence of Trichuris trichiura was higher among schoolchildren in both rural and urban government schools than in the urban private school. The prevalence of Taenia species was higher in the rural school than in the urban government and private schools. Hookworm infection was low among schoolchildren in the urban and rural government schools, and there were none found in the private school (Table 2).

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Table 2. The Prevalence of Intestinal Helminth Infections in Government-Owned (Urban and Rural) and Privately Owned (Urban) Schools.

https://doi.org/10.1371/journal.pntd.0000146.t002

The prevalence of infection was further analyzed according to the age and sex of schoolchildren (Table 3). There were no significant differences in prevalence of infection between age groups of schoolchildren in the study schools. There were also no significant differences in infection between male and female schoolchildren in rural government and urban private school, but significantly more males were infected than females in the urban government school (p = 0.037) (Table 3).

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Table 3. The Prevalence of Intestinal Helminth Infections by Age Group and Sex of Schoolchildren in the Government-Owned (Urban and Rural) and Private (Urban) Schools.

https://doi.org/10.1371/journal.pntd.0000146.t003

Discussion

This survey investigated demography, helminthiasis, and sanitary conditions in three primary schools of different ownership and social settings in Ikenne LGA of Ogun State, Nigeria. The study shows clearly that the burden of parasitic infections in schoolchildren and poor sanitary conditions of the urban and rural schools owned by the government constitute a public health priority. It strongly supports the need for school health programmes aimed at reducing the prevalence of helminth infections in schoolchildren and improving the sanitation conditions in and around the schools. The demographic data, however, indicated that the proportion of schoolchildren benefiting from a school health programme would decline with increasing grade-level and that female children would be increasingly disadvantaged in government-owned schools.

The demographic data indicate that the number of schoolchildren gradually decrease with increasing age in government-owned urban and rural schools. This pattern may be due to a high rate of dropouts occasioned by lack of funds and/or parents sending their children to learn handwork/craftwork rather than to complete primary education. Another point revealed by the demographic data is that fewer female than male children attend government-owned urban and rural schools. Several socioeconomic and behavioural reasons may be involved in the female dropout rate [14], but it is probably due to three main reasons in this locality. First, parents considered it a waste of resources to invest in education of girls, and/or that educating a girl is a waste of resources as they will eventually be married out of the family. Second, some parents might believe that female children should stop attending school at puberty in order to avoid unwanted pregnancies. Third, in many parts of Africa, including Nigeria, female children are withdrawn from schools to be engaged as domestic house helpers or child labourers, especially in polygamous families. However, parents sending their wards to the private school give female children equal educational opportunity up to high-grade education. Higher socioeconomic and educational status of the parents may explain the attitude that female children should have opportunities to gain skills and capabilities equal to those available to male children. These demographic features are also similar among schoolchildren surveyed in Chad, Mali, Ghana, and Tanzania in Africa [16],[17], and in Turkey [18]. It is hoped that federal legislation making primary education free and compulsory in Nigeria will increase the level of enrolment of girls.

It is suggested that school health programmes will also offer the potential to attract children to school, to receive treatment and other benefits. These programmes may be in the form of school health clubs, deworming programmes, and teaching of basic hygiene education subjects. Such programmes must be participatory in both design and implementation, and involve government health departments, school boards, teachers, and the pupils themselves. The programme should also incorporate a process to reward best-performing schools in hygiene standards and to encourage competition among schools.

It is well known that, due to the falling standard of teaching in government schools, many parents/guardians prefer to send their wards to private schools, even at a very high, burdensome cost to them. Government resources to run and manage public schools over the years have been hampered through corruption and mismanagement of funds. Therefore, there are limited resources to improve the quality of education in government primary schools. However, parents still send their ward to public schools, because it is free.

This study indicates that prevalence of intestinal helminth infection was higher in government-owned urban and rural schools than in the urban private school. This result was expected, because the poor socioeconomic status, poor hygienic habits, and lack of sanitation in these settings all support helminth infection, as suggested by previous studies [19],[20]. In the government schools, water supplies were insufficient (deliveries one or twice in a week), and the toilet facilities—which were dilapidated latrines—were unsanitary. There was no soap for handwashing after using the latrine. Because of the condition of the latrines, most schoolchildren defecated around the school compounds and did not clean their hands afterward because of the lack of both water and education about good hygiene.

Garbage piles were accumulated around government-owned schools, and schoolchildren were seen digging and playing on them. Thus, the children may have been exposed to an additional risk for the transmission of infection in the rural and urban school, which may explain the higher prevalence of intestinal worm infections. Regularly emptied garbage cans are needed in public schools.

Food vendors are characteristic of many public schools in developing countries, as they provide snacks and lunches to pupils. However, their sources of food and mode of preparations have always been a source of concern to school authorities, who often try to ban them from their premises. However, in the absence of alternative sources of food for the children, it is suggested that school feeding programmes that utilize reliable food sources be encouraged. Schoolchildren in the urban private school also suffered a notable infection rate (28.4%), although this is substantially lower than in the government urban school at 54.9% and rural school at 63.5%; Table 2), although their school was more sanitary and the parents were in better socioeconomic conditions.

This study reconfirms that the three most common intestinal helminths are A. lumbricoides, T. trichiura, and hookworm as documented previously [6]. These three species are cosmopolitan; Ascaris spp. and Trichuris spp. are transmitted by the faecal-oral route, while hookworms active penetrate exposed skin. Presence of ascariasis and trichiuriasis indicates that food and water are contaminated with infective eggs of these parasites by any of a number of routes, or that hand-to-mouth transmission may occur. Food and drinking-water handling equipment may be contaminated if there are no safe and secured human waste disposal methods or handwashing facilities—as is the case in government-owned schools where pupils defecate around school compounds and are unable to wash their hands because there is no soap and only infrequent water. The hookworm infections observed may have been acquired by children who do not wear protective shoes, which is very common among schoolchildren in government-owned schools. Students in these schools usually remove their shoes when they are playing within and outside school premises, because they may have a single pair of shoes for a whole session and need to make them last. Taeniasis could have been acquired from consumption of raw or improperly cooked meat (beef and pork) in the form of a locally roasted delicacy called “suya.” This improperly cooked meat is usually provided by food vendors on exposed trays.

Because of the known devastating effects of these parasite infections on the physical and mental conditions of children, it is suggested that a control programme against these infection commence as soon as possible. Such a programme should adopt the use of combined interventions. One such intervention is periodic deworming of children, at least once every year, using information based on infection rate, intensity [1], and reinfection studies, particularly for ascariasis [21]. Another is the provision and use of basic amenities and health education on the dangers, modes of transmission, and prevention of these intestinal parasites. Yet another is to address the problem of poor water supply and poor sanitation conditions in government schools—this measure would help a deworming programme succeed. Finally, local health officials and school management should collaborate to initiate school health programmes for delivering anthelmitic drugs and health education activities to these schools.

The results of this study have provided baseline information for planning school-based health education programmes in the rural and urban government-owned schools studied. Additional funds will be needed to provide the same information for other schools in Ikenne LGA in particular, and Ogun State in general.

Acknowledgments

The authors wish to thanks the head teachers of the three schools for their cooperation during the period of the study and the schools' pupils for providing stool samples. We thank the Ogun State Universal Basic Education Board for permission to use their schools for the study. We equally thank the management of the El-Shaddai Private Nursery, Head teachers of A.U.D. Primary School, and Salvation Army Primary School for access to their pupils. Finally we are grateful to parents/guardians of children that participated in the study for their consent.