Impact of School-Based Health Education Intervention on the Incidence of Soil-transmitted Helminths in Pupils of Rural Schools, Kogi East, North Central Nigeria.

Background: The negative impact of soil-transmitted helminths (STHs) in Nigeria is enormous posing serious public health issues. This study was undertaken to investigate the impact of health education intervention on re-infection of STHs in pupils of rural schools of Kogi East, North Central Nigeria. Methods: A cross-sectional survey was carried out in 45 schools to determine the prevalence of STHs in the 9 local government areas of Kogi East. Stool samples were collected and examined for STHs. A total of 10 schools with the highest prevalence were selected for the follow-up study, 5 schools were dewormed and given health education (DHE) intervention while the other 5 schools were dewormed only (DO). Reassessment of schools for re-infection was carried out for a period of 12 months. Data obtained were analyzed using descriptive statistics. Student t-test was used to make comparison between interventions in the incidence of infections. Analysis was carried out at p<0.05. Results: Re-infection with STHs was observed from the 7 th month of both interventions. In the 36 th week (9 th month), incidence observed in schools given DHE schools (4.79%, 8 pupils) were higher than in DO schools (3.19%, 5 pupils), no signicant difference (t = -0.840, p = 0.426) between the interventions. Also, at the 48 th week (12 th month), no signicant difference (t = -0.346, p = 0.738) between the DHE schools (7.19%, 12 pupils) and DO schools (6.37%, 10 pupils). Hookworms had the highest incidence in DHE (6.6%, 11 pupils) and DO (6.4%, 10 pupils) schools among the STHs. A. lumbricoides incidence was low and was observed in a school given DHE (0.6%, 1 pupil). S. stercoralis was not observed throughout. At 48 th (12 th month), an incidence of 6.37% was observed compared to 32.03% prevalence at baseline in the DO schools and an incidence of 7.11% and prevalence of 36.09% in the DHE schools. Signicant difference (p<0.05) exist between baseline and intervention. Conclusion: Non-dewormed individuals at the community levels may have contributed to the poor performance of health education. Community-based deworming should be encouraged alongside improvement in the water, sanitation and hygiene infrastructures at both school and home.


Introduction
Soil-transmitted helminths (STHs) are among the foremost causes of global health problems especially in underprivileged and deprived populations where implementation and control are challenging to maintain. Soil-transmitted helminthiasis are caused by parasitic nematodes transmitted through contact with parasites eggs (Ascaris lumbricoides and Trichuris trichiura) or larvae (hookworms) and are responsible for more than 40% of worldwide morbidity from all tropical infections [1,2,3]. An estimated 2 billion people are infected worldwide with 819, 439 and 439 million people infected with A. lumbricoides, T. trichiura and hookworms respectively [3,4].
Soil-transmitted helminthiasis is the most widespread Neglected Tropical Diseases (NTDs) in Nigeria [2]. Children in rural areas lacking clean water and sanitation infrastructures are the most affected [5]. Infection with these parasites leads to hampered cognitive and physical development, and nutritional effects [6,7,8]. Infections with A. lumbricoides can cause abdominal pain, lactose intolerance and decreased absorption of vitamin A and other nutrients. Severe infection with whipworm leads to in ammation at the site of attachment in the intestines and result in colitis and rectal prolapse. Infections with hookworms may lead to intestinal blood loss that results in iron-de ciency anaemia [7,9].
Preventive chemotherapy is recommended by WHO as means of controlling STH infections which involves consistent administration of drugs to population at-risk. The WHO recommends annual deworming of pre-school aged children and school-aged children in areas where the prevalence of STH is between 20% and 50% and semi-annual if above 50% are infected [10]. Despite this repetitive treatment, infection prevalence and intensity have rapidly bounce back. This lack of sustainability lessens the effectiveness of MDA.
In Nigeria, the main strategy for control of soil-transmitted helminth (STH) infections is the periodic mass drug administration (MDA) of antihelminthics to the population at risk [2]. MDA alone as an intervention does not prevent re-infection of STHs [11,12]. Therefore, there is need for a complementary measures to prevent re-infection, such as health education and improved sanitation. This will help augment the control approach and hence the effectiveness of MDA for optimal productivity and sustainability [12]. This integrative approach will help reduce the number of treatment rounds, lessen the disease burden and create a long-standing sustainable control.
Health education is a vital, low-cost and simple component of most interventions for prevention and control of many NTDs. Since NTD transmission is enabled by human activities and behaviour, education on sanitation, personal and cooking hygiene can prevent re-infection within the school and community.
Increasing their knowledge on self-care, skills, resources and support to practise self-care every day can prevent the development of disabilities and further reduce the disease progression [13].

Inclusion and exclusion criteria
Children attending schools in rural communities of Kogi East with ages from 5 to 14 years were included in this study. Preschool-aged children (<5 years) and children older than 14 years attending rural schools in Kogi East were excluded from this study.

School mobilization and sensitization
Advocacy visits were paid to the Honourable Commissioner for Health and this was preceded by letters from the KSMoH and also the SUBEB to the Education Secretaries of the Local Government Education Authorities (LGEAs).

Study design
The study was carried out between January 2018 and December, 2019. District-wide mapping for STH infections was conducted in all the nine (9) LGAs of Kogi East (Ankpa, Bassa, Dekina, Ibaji, Idah, Igalamela/Odolu, Ofu, Olamaboro and Omala LGAs) in a coordinated manner using WHO National protocol framework [16] and was in line with the Federal Ministry of Health (FMoH) protocol on integrated epidemiological mapping and baseline survey for STHs [2]. Randomised selection of schools was done followed by a randomised systematic selection of children in the schools to be surveyed. Enrolled school age children were targeted from the surveyed schools ( Figure 2).

Sample size
During the baseline survey, a total of 100 pupils were sampled in each LGA according to the WHO national protocol framework [16]. This study sampled 36 pupils per school, that is, 36 pupils in ve schools (180 samples) per LGA, which gave a sample size of 1620. However, with the minimum sample size of 100 pupils per LGA, the minimum sample size of 900 was reached.

Statement of consent of participants
Written consents were obtained from the guardians/parents of study participants, informing them of their rights and granting permission for their children to participate in the study.

Selection of participating schools and children
In all the LGAs, ve (5) schools were randomly selected from different communities in the rural areas of the LGAs, that is, a total of 45 schools were sampled. A sampling frame developed was used for selection of pupils in each selected school. A total of 36 pupils of both sexes, males and females were selected on pro-rata basis from 5 -16 years old (class one to class six) from each school sampled.

Sample collection and parasitological examination
Stool samples were collected from selected schoolchildren using sterile specimen bottles. Each child in the study was given a sterile specimen bottle to take home after which instruction on how sample collection was explained to them. A single faecal sample was collected from each child and preserved using 10% formalin. Stool samples were taken to the Department of Animal and Environmental Biology, Kogi State University, Anyigba for parasitological examination using formal ether sedimentation technique [17].
In a suitable container, 1 g of stool sample was mixed thoroughly with 10ml of saline solution to form an emulsion which was then ltered through ne mesh gauze into a conical centrifuge tube. Suspension was centrifuged at Relative Centrifuge Force (RCF) of 600 g (about 2000 rpm) for about 10 minutes yielding about 0.5 ml of sediment. After supernatant was discarded, the sediment was washed with 10 ml of saline solution, and then recentrifuged. This was done repeatedly until supernatant became clear. After the last wash, supernatant was discarded and 10 ml of 10% formalin was added, mixed, and then the mixture was allowed to stand for 5 minutes to effect xation. About 2 ml of ethyl acetate was added; tube was stoppered and vigorously mixed. The mixture was centrifuged at 450 g RCF (about 1500 rpm) for 10 minutes which gave four results; a top layer of ethyl acetate, plug of debris, layer of formalin, and sediment.
Plug of debris from the side of the tube were removed using the applicator stick, and the top three layers were carefully discarded. With a pipette, the remaining sediment was mixed with the small amount of uid and a drop each was transferred to a drop of saline and iodine on a glass side, covered with coverslip and examined microscopically for the presence of parasitic forms.

Selection of endemic schools for intervention studies
The results obtained from the survey served as the baseline assessment. A total of 10 schools were selected from the baseline study, the criteria for selection was based on highest infection rate. Five schools each were paired with another ve schools with the closest proximity. The ve (5) schools with the highest infection rate served as the intervention group while the other ve (5) schools served as the control group. An open-label pair-matched cluster-randomized controlled trial study design was used ( Figure 3).

Randomization and masking
The unit of randomization was the school. To ensure a balanced proportion of children in each group and comparison between intervention and control schools with regard to expected baseline STH prevalence, schools were matched according to geographical zone. Within each pair, one school was randomly allocated to deworming and health education (intervention school) and the other to deworming alone (control school) ( Figure 3).

Deworming of endemic schools for follow-up studies
Following baseline assessment, all children in the 10 selected schools were given a 400 mg chewable albendazole tablet (Manufactured and Donated by GlaxoSmithKline to World Health Organization). The tablets used for this study were obtained from NTDs Unit, Kogi State Ministry of Health, Lokoja, Nigeria and each child was monitored to ensure that the tablet is chewed and swallowed. E cacy of the albendazole treatment was assessed in a random sampling of 60 pupils each from 3 schools dewormed to check for the presence of at least one of the STH species [18].

Health education intervention
The health education intervention was administered during every visit at each intervention school and it consist of two components.
First, pupils were taught on STH acquisition, transmission and prevention. Urban School Health Kit by WHO [19] was adopted during this component. During this intervention, pupils were taught on ways to improve their personal hygiene and understand the importance of preventing STH infection.
Secondly, a half-day workshop was organized for teachers with the goal of promoting an integrated health curriculum. These workshops was held following deworming.
Posters highlighting key health messages were distributed and displayed in strategic locations around the school. The key messages for prevention used in this study are; washing hands before eating, washing hands with soap after playing with soil, washing hands with soap after using the toilet, wearing slippers or shoes when going outside, avoiding open (indiscriminate) defecation, washing vegetables and fruits before consumption, drinking clean (boiled) water, covering food from ies and cutting nails periodically.

Follow-up studies
The follow-up assessments commenced one month after deworming and was carried out monthly until re-infection of STHs was observed ( Figure 4). The stool specimens collected on every visit were transported to the laboratory where they were examined within 48 hours. Similar procedure used in parasitological examination of samples as stated above was used.

Statistical Analyses
Data were entered using Microsoft Excel version 2013. Descriptive statistics were used to compute prevalence and incidence. The student t-test was used to determine the level of signi cant between the intervention group and the control group. All analyses were performed using Statistical Package for Social Sciences (SPSS) software (Version 22.0 for Windows; SPSS Inc., Chicago, IL, USA).

Results
A total of 2331 pupils were dewormed in 10 schools across Kogi East ( Table 2). Five of the dewormed schools were subjected to health education. The effect of both interventions were assessed over a 12 months period. No parasitic infection was observed upto to the 24th week (6th month) of stool examination.
Infection with soil-transmitted helminths was observed from the 7th month after the administration of both interventions i.e. deworming only (DO) and deworming and health education (DHE).
Comparison of incidence in DO schools to DHE schools revealed no signi cant difference (p > 0.05) ( Table 3). Although, higher incidence of infection were observed in DHE schools than DO schools. In the 36th week (9th month), incidence observed in schools given DHE schools (4.79%, 8 pupils) was higher than in DO schools (3.19%, 5 pupils), no signi cant difference (t = -0.840, p = 0.426) exist between the interventions. Also, at the 48th week (12th month), no signi cant difference (t = -0.346, p = 0.738) was also observed in the incidence between the DHE schools (7.19%, 12 pupils) and DO schools (6.37%, 10 pupils).
The incidence of individual parasites at the 48th week (12th month) revealed no signi cant difference (p > 0.05) in the parasite species found. Hookworms had the highest re-infection rate with incidence of 6.6% (11 pupils) and 6.4% (10 pupils) in DHE and DO schools respectively. A. lumbricoides re-infection was low and was observed only in a school given DHE with incidence of 0.6% (1 pupil). S. stercoralis was not observed throughout the follow-up study over the one year period ( Table 4).
Comparison of incidence of infection between DHE and DO schools at 12th, 24th, 36th and 48th weeks revealed no signi cant difference (p > 0.05). Although, the incidence was higher in the DHE schools than DO schools ( Table 5).
Comparison of baseline prevalence and incidence at 48th week (12th month) of follow-up revealed signi cant variation (p ≤ 0.05) in both intervention. In DO schools, an incidence of 6.37% was observed compared to 32.03% prevalence at baseline while in DHE, an incidence of 7.11% was observed which was signi cant from baseline prevalence of 36.09% (Table 6).

Discussion
The present study assessed the effect of health education on pupils of rural primary schools in Kogi East, North Central Nigeria. The study revealed that health education has no signi cant effect on the re-infection of soil-transmitted helminths in the region. Chemotherapy proves effective than health education.
The observation of this study is a complete deviation from series of studies previously on the effect of health education on STHs [18,20,21] but similar to the observation of a study in Ethiopia [22] where a prevalence of 25.8% was observed at baseline and incidence of 23.8% at endline. The prevalence of intestinal parasitic infections was not signi cantly decreased at the endline compared with the baseline [PR = 0.92, 95% CI = (0.62, 1.38)]. They [22] also reported that that water, sanitation and hygiene (WASH) education was signi cantly associated with households' sanitation performance. They stated that health education increases the awareness on good WASH practices and encourages behavioural change but that it needs to be carried out at the household level rather than at school level for better performance. The health education intervention in India [20] and Mali [21] were effective been a community-based total sanitation approaches while in this study, school-based approach was used. A study in Malaysia [23] and low and middle-income countries [24] stated that communitybased health education intervention is one of the effective WASH promotion approaches to empower rural communities. A study in Peruvian Amazon [18] recommended that school-based periodic deworming programs are likely to perform better when enhanced with a sustained health hygiene education in an integrated manner.
Health education increases awareness about the potential health implications, the implementation barriers at household level are important factors that needs proper consideration as this will in uence subsequently affects the reinfection of these parasites. Several household barrier factors such as nancial status, parent education level, culture, willingness to adhere to instructions etc. should be put under consideration [25,26,27].
Hookworms was the main parasites that was observed to have higher incidence compared to A. lumbricoides and S. stercoralis. Previous studies have found that health education has only a minimal, insigni cant effect on hookworm infections [18,28]. These studies reported that children in underprivileged communities are faced with several barriers which affects the positive change provided by the health education. Such factors includes lack of nancial resources to purchase a pair of shoes [29,30]. Oral interview revealed that some of the pupils had only one pair of shoes which was used when going to school and were prevented by their parents from using such shoes at home or when moving around in the village. Thereby predisposing them to infections with hookworms.
The signi cant reduction in incidence during follow-up observed in this study might be due to chemotherapy administered prior to follow-up study. Series of studies have reported the effectiveness of chemotherapy in control STHs infection especially when done annually. A study in Gurage Zone, Ethiopia [31] reported that chemotherapy results in substantial reduction in overall prevalence and infection intensity of STHs. The residual infections with STHs in this study is a re ection of the maintenance of transmission among the untreated populations in the community which are constantly in contact with the dewormed children. Some studies in Kenya reported low infection of STHs among all age groups given school-based deworming [32,33,34].

Conclusions
Health education had no signi cant effect on the re-infection of soil-transmitted helminths in the Kogi East, North Central Nigeria. Inclusion of health education alongside with both school-based deworming proved not effective than school-based deworming alone. The use of community-based deworming alongside improvement in the water, sanitation and hygiene infrastructures both at schools and home will help provide a better opportunity to put the knowledge acquired through health education programmes to use. Rather than acquire health education without basic amenities to put such education to use.

Consent for publication
Not applicable.

Availability of data and material
The data sets in this study are available from the corresponding author on reasonable request.

Competing interests
The authors declare that they have no competing interests.