Stem Cell Oncology – Adella (Ed.) © 2018 Taylor & Francis Group, London, ISBN 978-0-8153-9272-9

Ascariasis incidence in children who received single and repeated educational lectures

M.A. Boediman, M. Lubis, O.R. Ramayani & P.D.H. Simbolon Department of Child Health, Medical School, Faculty of Medicine, Universitas Sumatera Utara, Medan, North Sumatera, Indonesia

ABSTRACT: The World Health Organization (WHO) have recommended albendazole 400 mg for the eradication ascariasis. Despite effective treatment options, reinfection following treatment alone is inevitable. A case-control study was conducted to investigate the difference in incidence of ascariasis in children who received education on sanitation and personal hygiene once with recurrent in Singkuang village, South Tapanuli, North Sumatera from April to October 2016. The subjects were elementary school children selected using a cluster sampling technique. Statistical analysis was performed by Chi-square and Fisher’s exact test. One hundred and seventy elementary school children were divided into two groups, with 85 subjects in the control group. The incidence of ascariasis was found to be 24% in the control group and 3% in the case group. Children who received recurrent education tended to be 8.4 times more likely not to succumb to ascariasis. There were significant differences in the incidence in both groups (p = 0.001).

Keywords: ascariasis, children, educational lecture, parasitic worm

1 INTRODUCTION

The incidence of soil-transmitted helminths (STH) in developing countries remains high. The main cause of intestinal parasitic infections is Ascaris lumbricoides (Clarke et al., 2017; Yap et al., 2016). The groups most vulnerable to this infection are school-age children, with an intensity peaking in the 5–14 year-age group (Yap et al., 2016). Among STH, ascariasis is the most common worm infection, with an estimated worldwide incidence of 25% (0.8 to 1.22 billion people) (Bethony et al., 2006). The World Health Organization’s (WHO) policy for control of ascariasis centres on three groups, preschool-aged children (pre-SAC), school-aged children (SAC) and women of child bearing age, on the basis that heavy infection in these groups will have a detrimental impact on anaemia, child growth and development. The current WHO guidelines focus on school- aged children, both for monitoring infection and as a target for treatment, although treatment of pre-SAC and women of childbearing age is also recommended where sustainable delivery mechanisms exist, especially in areas of intense transmission. The guidelines recom- mend treating SAC annually where any STH prevalence falls between 20% and 50% and twice a year where it exceeds 50% (Anderson et al., 2015). At present, the control strategy for STH infection promoted by the WHO is based solely on the eradication of periodic worms or deworming in high-risk communities (Clarke et al., 2017). By treating the highest risk group, environmental contamination is reduced and consequently, infection in the wider community decreases. School-based deworming programmes have been shown to contribute towards achieving several of the Millennium Development Goals (MDG). Despite effective treatment options for STH infections, reinfection following treatment alone is inevitable (Jia et al., 2012). One strategy that has been identified to reduce reinfection following deworming treatment is health education, focussing on teaching hygienic and

201

IISCOC17_Book.indbSCOC17_Book.indb 201201 33/21/2018/21/2018 2:04:232:04:23 PMPM sanitary behaviours. The simplest and cheapest strategy is handwashing. Previous studies have assessed the effectiveness of handwashing in reducing the prevalence of ascariasis (Mah- mud et al., 2015). Regular education in schools can be a way of conveying the right method of handwashing to a child. A school-based health hygiene education intervention was effective in increasing STH knowledge and in reducing ascariasis (Gyorkos et al., 2013). Educa- tion on health, especially prevention of ascariasis disease, for both parents and children is an important factor in breaking the chain of transmission as well as the incidence rate of ascariasis disease (Schmidlin et al., 2013; Corneiro et al., 2002).

2 METHOD

This study took place in Singkuang village, Mandailing Natal, North Sumatera from April 2016 until October 2016. The subjects were elementary school children selected using a cluster sampling technique. The exclusion criteria were students who refused to take worm medi- cines and incomplete follow the execution. All children who fulfilled the inclusion criteria were enrolled in the study. Primary school data collection in Singkuang village, the selection of elementary school will be conducted randomly. Elementary schools that were selected were randomised for one or three-time extension interventions. Basic baseline data on parents’ and children’s knowledge of helminth infection and its prevention were collected based on the available questionnaires. Examination of faeces by the parasitology officer of the Faculty of Medicine, the University of North Sumatra was conducted using the Kato Katz method. All participants who suffered and did not suffer from a worm infection were given the anthelmintic medication, albendazole 400 mg, in a single dose. The participants were randomly grouped into case and control groups. Single education was performed in the control group and repeated three times in the case group. We tested the validity of the education lecture instrument by using Pearson’s correlation test and obtained a result for Cronbach’s alpha coefficient of 0.86. Repeat examination of faeces was conducted three months after and assessed the incidence rate of ascariasis in both new and reinfected children. Data were analysed using the Statistical Package for Social Sciences (SPSS) for Windows, version 19 (2010), with a 95% confidence interval and a p value <0.05 was considered as significant. Randomisation was used Microsoft Excel Randomisation. The analysis was performed using a Chi-square and Fisher’s exact test. Ethical approval was granted by the Research Ethics Committee, Medical Faculty, University of North Sumatera.

3 RESULTS

One hundred and seventy elementary school children from Singkuang village, Mandailing Natal, North Sumatra, were enrolled and divided into two groups, with 85 subjects in the control group. The study population characteristics showed that the mean age of children in the control group was 10.1 (SD 1.97) years and in the case group 8.8 (SD 2.04) years. Both groups were dominated by males. Based on the class, children in the control group were mostly in fifth class (23.5%), while in the case group they were mostly in first grade (28.2%). The number of siblings and the order in the family of children in each group was almost the same. Children in both groups mostly had short stature and normal nutritional status. Parents of children in both groups have incomes ranging from 500,000 to 1,000,000 Rupiah, with most occupations being either fishermen or farmers. More than 80% of children’s parent’s education is up to elementary school. From the total sample, 50 students suffered from ascariasis. This shows that the prevalence of ascariasis in this study was 29.4%. This study reported that after six months follow-up, we found 96.5% (82/85 samples) and 76.5% (65/85) samples in the uninfected state, the remaining was 3.5% and 23.5% samples in reinfection state, respectively for intervention and control group. The relative risk ratio for both groups was 8.410. The findings from the six months follow-up assessment showed 202

IISCOC17_Book.indbSCOC17_Book.indb 202202 33/21/2018/21/2018 2:04:232:04:23 PMPM Table 1. Educational relationship of sanitation and hygiene with the occurrence of ascariasis.

Ascariasis

Education No Yes RR 95% CI p*

Multiple 82 3 8.410 [2.394, 29.543] 0.001 Single 65 20

Table 2. Factors related to the success of education.

Variable Wald p* Constants 95% CI

Gender 1.215 0.270 3.914 [0.346, 44.311] Age 0.843 0.359 1.669 [0.559, 4.978] Class of school 0.023 0.880 0.791 [0.037, 16.728] Family order 3.203 0.074 0.390 [0.139, 1.094] Number of siblings 0.800 0.371 0.720 [0.351, 1.478] Parental education 2.165 0.141 16.695 [0.393, 709.63] Parental employment 3.986 0.046 184.404 [1.100, 30917.9] Parental income 2.576 0.109 0.013 [0.000, 26.111]

that there were differences in the incidence in both groups (p = 0.001). Children who received recurrent education tended to be 8.4 times more likely not to succumb to ascariasis (Table 1). This study also looked for factors related to the success of the education programme. The results of the logistic regression test on factors related to the success of education in this study showed that the parent’s occupation is the only factor affecting the success of education, where the success of education will increase 184 times in children of parents with civil service employees compared with children of parents with other jobs (Table 2).

4 DISCUSSION

In Indonesia, the prevalence of ascariasis remains high, especially in children aged one to ten years. Research conducted by Rahmad in Sibolga, North Sumatra, showed a prevalence of ascariasis of 55.8% and in Karo of 18.3% (Rahmad, 2008). Meanwhile, research by Ginting (2009) in Samosir reported a higher figure of 55.8%. Another study in the area of North Sumatra, Deli Serdang by Rahma reported a prevalence of 84.4% (Rahma, 2011). The present research was conducted in the North Sumatera province, Mandailing Natal Regency. This region consists of coastal and tropical lowlands. The results showed a prevalence of ascariasis of 29.4%. This figure is lower than the prevalence in the Sibolga and Deli Serdang areas which are both coastal and lowland areas. This may be due to a lack of STH infection screening conducted in the study area. Ascaris infection is more common in children aged 6–12 years (Mahmud et al., 2015). This is because children still have a lack of knowledge or consciousness about personal hygiene and health. The presence of Intestinal Parasitic Infections (IPIs) have a statistically significant association with the educational status of the household heads, the absence of washing facilities, home cleanness conditions and type of toilet used (p < 0.05) (Abbosie & Seid, 2014). The economic and educational level of parents also affects the incidence of ascariasis in children (Nematian et al., 2004). Parents with low economic levels tend to use health facilities more often associated with prevention of health or ascariasis. Low-educated parents will have less knowledge, including in the health field. One of the things they often ignore is personal hygiene and the environment. Also, poorly educated parents will find it difficult to provide good health education to their children, including the prevention of worms. 203

ISCOC17_Book.indb 203 3/21/2018 2:04:23 PM STHs are easily treated with one of four drugs: albendazole and mebendazole, and to a lesser extent, levamisole and pyrantel pamoate (Anderson et al., 2015). In line with the WHO strategy for controlling STH infections in endemic countries, a national school- based deworming programme currently provides annual delivery of albendazole to school children (Kepha, 2017). However, reinfection commonly occurs due to the inability of the human host to mount protective immunity to reinfection by intestinal helminths (Jia et al., 2012). The impacts on both prevalence and intensity of infection were significantly higher among children receiving four-monthly treatments of albendazole compared to those who received a single annual treatment (Kepha, 2017). But if treatment combined with inadequate hygiene and sanitation. Ziegelbauer et al. (2012) to restrict or eliminate re-exposure in environments continuously contaminated with the egg or larval free-living transmission stages of these parasitic worms (Gabrie et al., 2014; Seid et al., 2015; Walker et al., 2011). The major strengths of this study include the large sample size, the randomised design, the high response and follow-up rates, appropriate statistical adjustment for clustering by schools, the matched-paired design and potential confounders. One limitation of this study is related to the open-label design. Although difficult to assess, it may be possible that students’ knowledge of their exposure status (i.e. whether they received the intervention or not) may have biased their self-reported responses to the behaviour questions, leading to potential measurement error. Another limitation is that we only had one follow-up period (i.e. four months) and we cannot conclude if knowledge of STH transmission and the protective effects on the intensity of Ascaris lumbricoides infection can be maintained over longer time periods.

5 CONCLUSION

There is a significant difference in the incidence of ascariasis between children receiving education on sanitation and recurrent hygiene with those who only receive a once off educational lecture.

REFERENCES

Abbosie, A. & Seid, M. (2014). Assessment of the prevalence of intestinal parasitosis and associated risk factors among primary school children in Chencha town, Southern Ethiopia. BMC Public Health, 14, 166–174. Anderson, R.M., Turner, H.C., Truscott, J.E., Hollingsworth, T.D. & Brooker, S.J. (2015). Should the goal for the treatment of soil transmitted helminth (STH) infections be changed from morbidity control in children to community-wide transmission elimination? PLOS Neglected Tropical Diseases, 9(8), 1–8. Bethony, J., Brooker, S., Albonico, M., Geiger, S.M., Loukas, A. & Diemert, D. (2006). Soil-transmitted helminth infections: Ascariasis, trichuriasis, and hookworm. The Lancet, 367, 1521–1532. Clarke, N.E., Clements, A.C.A., Doi, S.A., Wang, D. & Campbell, S.J. (2017). Differential effect of mass deworming and targeted deworming for soil-transmitted helminth control in children: A systematic review and meta-analysis. The Lancet, 389 (10066), 287–297. Corneiro, F.F., Cifuentes, E., Tellez-Rojo, M.M. & Romieu, I. (2002). The risk of Ascaris lumbricoides infection in children as an environmental health indicator to guide preventive activities in Caparaó and Alto Caparaó, Brazil. Bulletin of the WHO, 80, 40–46. Gabrie, J.A., Rueda, M.M., Canales, M., Gyorkos, T.W. & Sancezh, A.L. (2014). School hygiene and deworming are key protective factors for reduced transmission of soil-transmitted helminths among schoolchildren in Honduras. Parasites & Vectors, 7, 354. Ginting A. (2009). Faktor-Faktor yang berhubungan dengan kejadian kecacingan pada Anak Sekolah Dasar di Desa tertinggal Kecamatan Pangururan Kabupaten Samosir Tahun 2008. Medan: Universitas Sumatera Utara. Gyorkos, T.W., Maheu-Giroux, M., Blouin, B. & Casapia, M. (2013). Impact of health education on soil-transmitted helminth infections in schoolchildren of the Peruvian Amazon: A cluster-randomized controlled trial. PLOS Neglected Tropical Diseases, 7, e2397.

204

IISCOC17_Book.indbSCOC17_Book.indb 204204 33/21/2018/21/2018 2:04:232:04:23 PMPM Jia, T.W., Melville, S., Utzinger, J., King, C.H. & Zhou, X.N. (2012). Soil-transmitted helminth reinfection after drug treatment: A systematic review and meta-analysis. PLOS Neglected Tropical Diseases, 6, e1621. Khepa, S., Mwandawiro, C.S., Anderson, R.M., Pullan, R.L. & Nuwaha, F. (2017). Impact of single annual treatment and four-monthly treatment of hookworm and Ascaris lumbricoides, and factors associated with residual infection among Kenyan school children. Infectious Diseases of Poverty, 6, 30. Mahmud, M.A., Spigt, M., Bezabih, A.M., Pavon, I.L., Dinant, G. & Velasco, R.B. (2015). Efficacy of handwashing with soap and nail clipping on intestinal parasitic infections in school-aged children: A factorial cluster randomized controlled trial. PLOS Medicine, 10, 1–16. Nematian, J., Nematian, E., Gholamrezanezhad, A. & Asgari, A. (2004). Prevalence of intestinal parasitic infections and their relation with socio-economic factors and hygienic habits in Tehran primary school students. Acta Tropica, 92, 179–186. Rahma, M.W. (2011). Hubungan antara higiene dengan infeksi cacing Soil Transmitted Helminths pada siswa-siswi SD Negeri No. 101837 Suka Makmur, Kecamatan Sibolangit, Kabupaten Deli Serdang Tahun 2011. Medan: Universitas Sumatera Utara. Rahmad, Z.R. (2008). Hubungan higiene perorangan siswa dengan infeksi kecacingan anak SD Negeri di Kecamatan Sibolga Kota Sibolga. Medan: Universitas Sumatera Utara. Schmidlin, T., Hurlimann, E., Silue, K.D., Yapi, R.B., Houngbedji, C. & Kouadio, B.A. (2013). Effects of hygiene and defecation behavior on helminths and intestinal protozoa infections in Taabo, Cote d’Ivoire. PLOS One, 8, e65722. Seid, M., Dejeniae, T. & Tomass, Z. (2015). Prevalence of intestinal helminths and associated risk factors in rural school-children in Were-Abaye Sub District, Tigray Region, Northern Ethiopia. Acta Parasitologica Globalis, 6, 29–35. Walker, M., Hall, A. & Basanez, M. (2011). Individual predisposition, household clustering and risk factors for human infection with Ascaris lumbricoides: New epidemiological insights. PLOS Neglected Tropical Diseases, 5, e1047–1057. Yap, P., Utzinget, J., Hattendorf, J. & Steinmann, P. (2016). Influence of nutrition on infection and reinfection with soil-transmitted helminthes: A systematic review. Parasites & Vectors, 229(7), 1–14. Ziegelbauer, K., Speich, B., Mausezahl, D., Bos, R., Keiser, J. & Utzinger, J. (2012). Effect of sanitation on soil transmitted helminth infection: Systematic review and meta-analysis. PLOS Medicine, 9, e1001162.

205

IISCOC17_Book.indbSCOC17_Book.indb 205205 33/21/2018/21/2018 2:04:232:04:23 PMPM