SOIL- TRANSMITTED NEMATODE INFECTIONS IN SCHOOL CHILDREN IN A PERI-URBAN AREA, NORTH CENTRAL NIGERIA

Parasitic infections caused by Soil Transmitted Nematodes (STN) are a common occurrence in developing countries with unfavourable environmental conditions that favour the development of eggs and larvae of STN. This was a cross sectional study carried out from January to April, 2018 to determine the prevalence and intensity of STN infections in six randomly selected primary schools in the Ilorin South Local Government Area, Kwara State, Nigeria. Stool specimens were collected from 508 pupils (259 males; 249 females), which were prepared and examined using the Kato-Katz technique. Of 508 stool specimens examined, 206 (40.6%) were infected with at least one of the STN. Eggs of Ascaris lumbricoides, Trichuris trichiura, Enterobius vermicularis and hookworms were identified with prevalences of 37.9%, 4.9%, 2.4% and 30.1% respectively. In all six schools examined, 115 males (44.4%) and 91 females(36.5%) were found to be infected (P<0.01). Pupils in the age group 5-7 years were found to be the most infected (52.2%), while the least occurred in the age group 14-16 years (28.2%). Of the 206 (40.6%) infected pupils; light, moderate and heavy infections were noted in 12.2%,20.7% and 7.5% respectively. The egg-count of Ascaris lumbricoides, Trichuris trichiura, hookworms and Enterobius vermicularis were 277.8±168.4, 160±118.1, 199.7±131.4 and 33.6±13.1 eggs per gram of faeces respectively. The intensity of STN infections was higher among males (231.3±159.8) than among females (230.8±154.8). Pupils in the age group 11-13 had the highest intensity of infection (267.0±158.1). Prevalence of single and double infections was 75.3% and 24.7% respectively. STN infections are prevalent in the study area which calls for regular deworming, health education and provision of basic sanitary and social amenities to reduce the disease burden.


Introduction
Soil-transmitted nematode (STN) infections are a serious public health and medical problem especially in tropical and subtropical countries (Pullan et al., 2014;WHO, 2017) and is the second largest leading cause of mortality in children above six years in Africa.STN infections may account for up to 12% of the total disease burden among children in resource-poor-countries (WHO, 2009).The World Health Organization estimates that over 270 million preschool children and over 600 million school-age children are living in areas where these parasites are intensively transmitted (WHO, 2012). In sub Saharan Africa, more than one quarter has one or more intestinal nematode infections occurring simultaneously (Montressor et al., 2002). Studies have shown that infection with soil transmitted nematodes affect mostly children of school going age with significant effects on morbidity and mortality resulting in more than 10,000-135,000 deaths annually (Lustigman et al., 2012). Symptoms associated with STN infections in school age children include anaemia, growth retardation, cognitive impairment, malnutrition, dysentery, fever, dehydration and vomiting amongst other severe symptoms that may also occur. In Nigeria, STN infections mainly Ascaris lumbricoides, Trichuris trichiura, and hookworms are a major health concern especially in rural and urban slums (Amali et al., 2013;Amaechi et al., 2014;Ohiolei et al., 2017). Here too, it is common that individuals are infected with more than one nematode species .Therefore a continuous assessment of the prevalence status of these infections is required to assist in reducing the disease burden. The present study investigated the status of soil transmitted nematode infections among primary school children in an urban slum, north central Nigeria, where the disease is endemic with a view to implementing control initiatives to manage these nematode infections.

Study Area and population
The study was conducted in three districts (Akanbi, Balogun Fulani, Okaka/Oke-Ogun) in the Ilorin South Local Government Area of Kwara State. The headquarters (Fufu) is 30Km from Ilorin the State Capital. The dominant ethnic group is Yoruba with other minority groups such as the Hausas, Fulanis, Nupes, Barubas and Igbos.The vegetation is guinea savannah, comprising of tall grasses with scattered trees, dominated by Shea butter trees (Vitellaria paradoxa) and Locust bean trees (Parkia biglobosa). The environment is seasonal with dry and wet seasons and an intervening harmattan from December to January. The annual rainfall ranges from 1000 and 1500mm while the mean temperature is between 20 ○ C and 37 ○ C.The major occupations in the study area include subsistence agriculture, livestock farming, petty trading, craft making and government jobs. Their main food crops include; yam, cassava, guinea corn, maize and rice. The area is provided with basic amenities such as health centers, pharmacies, hospitals, and schools while electricity, bore-holes and pipe-borne water is also available. Most of the inhabitants still make use of pit latrines and bushes for defecation. The hygiene conditions of the area are unfavourable.

Sample collection and laboratory procedures
Random sampling technique was used in the study. Six primary schools were randomly selected among the three selected districts by balloting. The Fisher formula was used to determine the desired sample size. n = Z 2 1 -α/2 P (1-P) (Daniel,1995)  The minimum sample size (n) was calculated to be 384 .Given this the inclusion of 508 children for the study satisfied the minimum requirement.
A registration list of pupils (aged 5-16years) from the selected schools was obtained and using a simple random sampling method, pupils were selected from each school and class. When a selected pupil was absent, a student before or after this student was selected as a replacement. Before the collection of the stool specimen, the research including the benefits was explained to the teachers and school children. Collection of specimens was thoroughly explained in local dialect after which they were given a clean, dry, leak-free wide-mouthed universal bottle with a screw cap, a clean sheet of paper, a spatula. A consent form was also distributed. Stool specimens were collected the following morning between 0900-2200hrs and preserved in 10% formalin and immediately transported to the laboratory of the Department of Medical Microbiology, University of Ilorin immediately for processing and examination. Each stool specimen was examined macroscopically for colour, consistency (whether formed, semi-formed or watery) and constituents (presence or absence of blood or mucus). The Kato-Katz technique was used to prepare stool specimens for microscopy for qualitative and quantitative diagnosis of STNs (based on eggs or larvae).

Ethical consideration
The protocol used in this study was approved by the Ethical Review Committee of the University of Ilorin, Nigeria (UERC/ASN/2017/1088), Ministry of Education and Human Capital Development and Local Government Education Board (E/MISC/170/1/128). Prior to the study, informed consent of parents and guardians of the school children was obtained after a detailed explanation of the study protocol. Following the ethical review regulation, patients who were found to be positive for the tested infections were given treatment.

Data analysis
Data obtained from parasitological analyses were analyzed using SPSS (Statistical Package for Social Sciences, version 20.0 California, USA) to interpret the levels of soil-transmitted nematode infections among school children in Ilorin South Local Government Area of Kwara State. The Chi square test was used to discern differences when the values (P<0.05) were considered to be statistically significant.

Overall prevalence of soil-transmitted nematode infections
A total of 508 school children, 259 boys and 249 girls in six randomly selected primary schools in Ilorin South Local Government Areas of Kwara State were examined. In all, characteristic eggs of four nematodes (A. lumbricoides, T. trichuria, Hookworms and E. vermicularis) were identified. Of the 508 pupils examined 206 (40.6%) were infected with at least one of the four STNs (Table 1).

Prevalence of Soil Transmitted Nematode Infections by Gender
Of the 259 boys and 249 girls examined, 115 boys (44.4%) and 91 girls (36.5%) were infected with STNs. However, the boys were significantly more infected than the girls (p<0.01). The prevalence of STN infections by gender reveals that the STNs were more prevalent among the boys than girls except in the case for T. trichiura and E. vermicularis infections.

Prevalence of Soil Transmitted Nematode Infections by Age
The age range of pupils examined was 5-16 years. Pupils in the age group 5-7 years (52.2%) were the most infected while the least infected were those in the age-group 14-16 years 28.2% (Table 2). There was a significant difference among the age groups in relation to STN infections (p<0.01).

Prevalence of Soil Transmitted Nematodes by STN Species
The prevalence of Soil Double infections of A. lumbricoides and hookworms were seen in all the six schools with a prevalence of 20.8% while double infections of A. lumbricoides and T. trichiura were seen in four schools; United, Model, Centre-Igboro and Isale-Asa LGEA Primary Schools with prevalence of 3.9% (Table 3).

Overall Intensity of Soil Transmitted Nematode Infections among School Children
The intensity of STN infections among the school children shows that majority of the pupils were infected with light (12.2%) and moderate (20.7%) infections, while 7.5% of the pupils were infected with heavy infection of STNs (Table 5).   The intensity of infection was highest among age group 11-13 years (267.0±158.1),while the lowest intensity was recorded among age group 14-16 years (172.3±173.6),with a significant difference between the various age groups (p<0.05) ( Table 7).

Discussion
The results of this study revealed that STN infections are common among the pupils of the selected primary schools in Ilorin South LGA, Kwara State, Nigeria. Of 508 school children examined, 206 (40.6%) were infected with at least one of the STNs which is attributable to ignorance, poverty, poor environmental sanitation, poor personal hygiene practices and the lack of basic amenities.
The overall prevalence recorded in this study is similar to a study carried out in the Moro Local Government Areas of Kwara State (Babatunde et al., 2013) where an overall prevalence of 41.6% was reported.
However, Amaechi et al., (2013) reported a higher prevalence (75.7%) among school children in rural communities of Abia State, Nigeria. Several factors could have contributed to the variation in prevalence of soil transmitted nematode infections in different areas of the country. These include ecological factors such as relative humidity, temperature, rainfall, vegetation and other climatic factors, socio-cultural habits, religious practices and geographical locations (Anosike et al., 2006). Differences in the targeted age groups and populations, timing of examinations and diagnostic techniques could also be responsible for variations in the prevalence of STN. Males had higher infection rates (44.4%) than females (36.5%). This result was consistent with the findings of Babatunde et al.(2013) and Amaechi et al., (2013) in Kwara State and Abia State respectively. The significant difference between males and females in this study may be a result of the playful outdoor activities and adventurous nature of males in comparison to the females. This is in agreement with the report of Obiukwu et al., 2008.   The highest prevalence (52.2%) of STN infections occurred among the age-group of 5-7 years,which declined towards 11 to 16 years. As the children grow older, they become more selective in their choice of food and activities thereby reducing infection risks through proper health habits (Amaechi et al., 2013). The higher prevalence in the pupils of the ages 5-7 years might be due to the level of exposure to indiscriminate eating of foods, fruits and snacks purchased from vendors, vulnerability to infections, lower level of immunity and the lack of attention to personal hygiene (Asinobi et al., 2004). The higher prevalence recorded in this study among pupils under the age of 10 years is in agreement with the finding of Ekpeyong and Eyo (2008), Akingbade et al., (2013) and Amaechi et al., (2013). This implies that pupils in the first years of their life are likely to suffer from nutritional deficits, growth retardation, cognitive impairment, serious illness and occasionally death and even surgical emergencies such as intestinal obstruction (de Silva et al., 1997).

In this study, four characteristic eggs of STN;
A.lumbricoides, T. trichiura, hookworm species and E. vermicularis were identified from the stool specimens. This agrees with the study of Babatunde et al., (2013). The transmission of these STNs is related to congenial condition for transmission of the parasites such as high relative humidity, optimal temperatures and shade (Brooker and Michael, 2000). Equally, important factors that favour the transmission of the parasites as revealed through the present study are ignorance, poverty, lack of portable water, poor personal hygiene, environmental sanitation and the lack of basic amenities such as pipe-borne water and good health care facilities.
The prevalence of the infection of A. lumbricodes (37.9%) was the highest among all the STNs encountered which is in agreement with findings of others for areas within Nigeria (e.g Asaolu et al., 1992;Amaechi et al., 2013;Babatunde et al., 2013Ojurongbe et al., 2014.The relatively high prevalence of the infections of A. lumbriocodes indicates poor sanitation and unhygienic practices among the pupils (Crompton & Savioli, 1993) ignorance on the part of the parents and pupils, poverty, lack of basic amenities and good health facilities.
More than one infection (multiple infections) was also reported in the study as it was common for a pupil to be infected with two or more STNs (Amaechi et al., 2013;Salawu et al., 2014). In this study, double infections were recorded; A. lumbricoides and Hookworm (20.8%) and A. lumbricoides and T. trichiura (3.9%). These possibly indicate that the environmental conditions in the study are conducive to the development and successful transmission of the Ubiquitous triad of A. lumbricoides, T. trichiura and Hookworms (Suswam et al., 1992).
Pupils whose parents were selfemployed showed highest prevalence of 42.1%. Some studies associated parents' occupation with STN infections (Chukwuma et al., 2009;Nmorsi et al., 2009). It is expected that parents engaged in occupations which involves contact with soil (farmers and bricklayers) and sewage are either reservoirs or sources of nematodes, and they once infected, would have a higher chance of transmitting the parasites to their children.
The highest prevalence of STN infections was recorded among pupils whose parents are without formal education (78.6%). This finding is in agreement with the studies carried out by Halpenny et al. (2013) and Wang et al. (2012) who report that care-givers education levels were significantly associated with STNs infections among pre-school and school going children. It is commonly known that caregivers, particularly mothers, are often responsible for both food preparation and health education of children in the family and, they significantly influence the health of their children. If a child's mother is educated, she is more likely to know about the dangers of STNs and how to  Cheesebrough (1981) and Chiodini et al. (2001).Walking barefoot promotes the entry of infective filariform larvae of hookworm species, hence, increasing chances of infection . Health education programmes in schools could enhance awareness on the transmission modes and control mechanism of STNs. Intensity of infection is the main epidemiological index used to describe STN infections; this intensity is measured by the number of eggs per gram of faeces (WHO, 2002a). The distribution of these eggs/larvae showed that the majority of the pupils had moderate infections (20.7%) while few had light (12.2%) and heavy (7.5%) infections. Generally, only STN infections of moderate and heavy levels produce clinical manifestations (Chan et al., 1994). This finding agrees with those of Babatunde et al., (2013).
The highest intensity (egg-count) of infection was of A. lumbricoides (277.8±168.4 eggs/g). However, this could be attributed to the fact that female A. lumbricodes produces the highest number of eggs which are extremely resistant to harsh environmental conditions (Roberts et al., 2009). The intensity of STN infections in relation to gender was similar among males and females probably because both sexes have the same level of exposure to STN infections in the study area. The intensity of STN infections was lower among the ages 14-16 years compared to pupils under the age of 13 years which could be attributed to the fact that at mid adolescence, the pupils in this age-group are more conscious of their personal hygiene and are more likely to walk barefoot.

Conclusions
Soil-transmitted nematode infections are common in peri-urban communities of Nigeria considered in the present study with considerable morbidity and mortality being recorded especially amongst primary school children. We have established that in least developed and low income communities, the lack of parental education, walking bare foot and other common habits such as finger sucking and biting, geophagy and eating of unwashed fruits are possible risk factors that are significantly associated with STN infections among school children. Health education targeted at enlightening school children on personal hygiene, provision of basic, social amenities and large scale de-worming campaigns should be frequently carried out in schools as a means of managing these STN infections.