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Impact of health education on the prevalence of enterobiasis in Korean preschool students
Acta Tropica 122 (2012) 59–63
Contents lists available at SciVerse ScienceDirect
Acta Tropica journal homepage: www.elsevier.com/locate/actatropica
Impact of health education on the prevalence of enterobiasis in Korean preschool students In-Soon Kang a,1 , Dong-Hee Kim a,1 , Hye-Gyung An b , Hyun-Mi Son b , Min Kyoung Cho c , Mi-Kyung Park c , Shin Ae Kang c , Bo Young Kim c , Hak Sun Yu c,∗ a
Department of Nursing, College of Nursing, Pusan National University, Yangsan-si, Gyeongsangnam-do 626-870, Republic of Korea Department of Nursing, Youngsan University, Yangsan-si, Gyeongsangnam-do 626-790, Republic of Korea c Department of Parasitology, School of Medicine, Pusan National University, Yangsan-si, Gyeongsangnam-do 626-870, Republic of Korea b
a r t i c l e
i n f o
Article history: Received 9 September 2011 Received in revised form 26 November 2011 Accepted 29 November 2011 Available online 7 December 2011 Keywords: Enterobius vermicularis Cellotape anal swab Health education
a b s t r a c t Health education has been shown to be effective in slowing the spread of the disease, infectious disease in particular. To evaluate the impact of health education on the prevalence and pattern of new infection of enterobiasis, children from 6 kindergartens in Ulsan city, South Korea, were recruited after undergoing a screening for enterobiasis, and then divided into three groups, including group medication (GM), education (Edu), and control group. All children in GM group received medical treatment with 500 mg albendazole twice, with 15 days interval. In the Edu group, only children diagnosed positive for Enterobius vermicularis eggs received medical treatment with 500 mg albendazole twice, with 15 days interval and all parents in the group received brochures providing information about enterobiasis. In the control group, only children diagnosed positive for E. vermicularis eggs received medical treatment with 500 mg albendazole twice, with 15 days interval, and no information about enterobiasis was provided to parents. Two post-treatment examinations were performed at three and six months after treatment. The infection rate in the GM group was dramatically decreased at 3 months, and this rate was almost the same as at 6 months after treatment. Infection rate of children in the Edu group was shown to drop from 9.9% to 3.0% at 3 months, and to 2.7% at 6 months after treatment; however, the infection rate in the control group continued to be higher than in the other two groups at both 3 and 6 months, with smaller change at 3 months compared to the other two groups. In addition, both new infection and re-infection cases in the Edu group were fewer, compared to those in the control group. In conclusion, although GM is the best method for eradication of enterobiasis, providing health information about enterobiasis to parents could reduce the prevalence, as well as the rate of new infection or re-infection with E. vermicularis in their children. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Enterobius vermicularis (pinworm) has infected Homo sapiens since the time of our species origin in Africa, and pinworm infection is a common helminth infection occurring worldwide (Hopkins, 1992; Kliks, 1990). Although the infection rates were different according to geographic location, infections may occur in almost all countries at this time. In Thailand, about 21.6% primary school children were infected with this parasite, 8.2% were infected in Turkey and 10.7% in South Korea (Changsap et al., 2002; Degerli
∗ Corresponding author at: Department of Parasitology, School of Medicine, Pusan National University, Beomeo-ri, Mulgeum-eup, Yangsan-si, Gyeongsangnam-do 626-870, Republic of Korea. Tel.: +82 51 510 8022; fax: +82 51 980 0872. E-mail address: [email protected] (H.S. Yu). 1 These authors contributed equally to this study. 0001-706X/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.actatropica.2011.11.017
et al., 2009; Kim et al., 2010). Although the parasite is highly present in preschool children, practically nothing has been done in most of the countries to eliminate infections. One of the reasons was that the symptoms of enterobiasis are not fatal, and most of the people believe that pinworm infection could be easily eradicated by one time medical treatment, even though that is not enough to kill eggs and larva. During 1970–2000, the government and parasitologists of Korea have struggled to eradicate many human parasite infections; thus, intestinal parasite egg positive rates have been dramatically decreased (from 84.3% in 1971 to 2.4% in 1997) by their efforts (Ministry of Health and Welfare and Korea Association of Health, 2004). Nevertheless, a relatively high egg-positive rate of E. vermicularis, ranging from 7.8% to 18.5%, has been reported in Korean children during the last decade (Kang et al., 2006; Kim et al., 2010; Lee et al., 2000; Park et al., 2005; Song et al., 2003). Two major reasons for not eradicating enterobiasis in preschool children might be the
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increasing number of young children being cared for in kindergartens and either the lack information or mis-information of their care givers, including parents, about E. vermicularis infection (Kim et al., 2010; Song et al., 2003). Many studies have investigated the factors that affect enterobiasis rates in children. Inadequate sanitation, poor level of parental care, no experience of taking an antihelminthic medicine and poor knowledge regarding enterobiasis, including transmission, prevention and how to take antihelminthic treatment have been associated with high prevalence of enterobiasis (Kang et al., 2006; Muge et al., 2008; Song et al., 2003). Comparatively, little emphasis has been put on the impact of health educational intervention on the prevalence of enterobiasis, although increasing health awareness, knowledge about disease and prevention management have all successfully improved many different health outcomes. Nithikathkul et al. (2005) recently evaluated the effect of health educational programs on the prevalence of enterobiasis in school children in Thailand. Educational interventions promoting knowledge of enterobiasis have also proven cost-effective in decreasing re-infection rates in school children (Nithikathkul et al., 2005). To the best of our knowledge, no study has looked at the impact of educational intervention among preschool children. School aged children are old enough to begin taking responsibility for their own personal hygiene, whereas children younger than six years old are still less responsible than older children. Since parents are in charge for their child’s personal hygiene and premedication with antihelminthic drugs, the focus of this study was to give brochures on prevention, transmission and treatment of enterobiasis to parents and to examine the effect on the prevalence of enterobiasis among kindergarten children in Korea. 2. Material and methods 2.1. Subject recruitment and screening evaluation The study protocol was approved by the Ethical Review Committee of Pusan National University Hospital and informed consent was obtained from each participant before enrollment. For recruitment, the letter containing information about the nature, significance, and objectives of the study, copies of a questionnaire, a guide for swab examination and a consent form, were sent to directors of kindergartens registered in the Ulsan Association of Kindergartens. Investigators met with the directors who agreed to participate in this study and described the details of the study. The directors sent a consent form, a letter of information and a questionnaire to the parents of each child. Three thousand nine hundred and forty one children from thirty-six kindergartens underwent a screening for enterobiasis via the cellotape anal swab technique. Kindergartens that had at least 6% of positive egg rates were potentially eligible for this intervention study. On the basis of a combination of egg positive rates and geographic location, eight kindergartens were finally chosen for this intervention study.
2.3. Parent education and medication of children in the selective groups After finishing baseline evaluations, the kindergartens were assigned by a research assistant to GM, Edu, and control groups. Entire classrooms in each kindergarten were tested and a total of 436 children (233 boys and 203 girls) were examined at baseline. At the first post-treatment examination, 405 children were examined, and 380 children participated at the second post-treatment examination. Of 436 parents provided with the pre-treatment questionnaire, 263 parents responded to the follow-up questionnaire and 21 parents did not fully complete their questionnaires. The director of each kindergarten and participants were blinded to the exposure status of participants. Easy-to-understand pictorial brochures were used to convey five messages, including lifespan of E. vermicularis, examination for enterobiasis, symptoms and signs, infection and transmission, and treatment and prevention of enterobiasis. The director of each kindergarten sent these brochures to parents and double checked by phone calls. In the GM group, all children in the kindergarten received medical treatment with 500 mg albendazole twice, with 15 days interval. In the Edu group, only children diagnosed positive for E. vermicularis eggs received medical treatment with 500 mg albendazole twice, with 15 days interval, and all parents in the group received the brochures. In the control group, only children diagnosed positive for E. vermicularis eggs received medical treatment with 500 mg albendazole twice, with 15 days interval (i.e. the usual communitybased control method for enterobiasis in Korea) and no information material was sent to parents. After the study, all participating children were treated with 500 mg albendazole twice, with 15 days interval. 2.4. Study outcome The study outcomes in each study group were the E. vermicularis eggs positive rate and the re-infection rate at three months and six months after enrollment. E. vermicularis infection was evaluated with the cellotape anal swab technique, before and after treatment. The pre-treatment structured questionnaire was provided to the parents of each child, asking about demographics and socioeconomic status and general knowledge of enterobiasis. Knowledge regarding enterobiasis was assessed six months after enrollment using a follow-up questionnaire. 2.5. Statistical analysis Statistical analysis was performed using PASW software (SPSS, Chicago, IL, USA). Baseline characteristics of study participants were compared using proportions. The prevalence of egg positive rate of E. vermicularis at baseline and after treatment was compared using proportions. Comparison of knowledge regarding enterobiasis between baseline and after treatment was performed by the paired t-test.
2.2. Group design
3. Results
To evaluate the effect of education on the prevalence of enterobiasis, we selected 6 kindergartens and divided the children into three groups, including group medication (GM), education (Edu), and control group. E. vermicularis infection rate and the location of the kindergarten were taken into account to determine the grouping. Table 1 shows several characteristics of study participants. After grouping, we compared several characteristics, and most of them were similar in the three groups. The small difference observed between the groups was not statistically significant.
The infection rate in the GM group was dramatically decreased at 3 months from 17.8% to 0.7%, and this rate was almost the same at 6 months after treatment (Table 2). Although the rates in the Edu and control groups were also decreased at the same time points, they were higher than in the GM group. The infection rate in children in the Edu group was shown to decrease from 9.9% to 2.7% at six months after treatment. Both at 3 months and 6 months after treatment, children in the control group had the highest E. vermicularis infection rate, i.e. 7.7% at 3 months and 7.9% at 6 months
I.-S. Kang et al. / Acta Tropica 122 (2012) 59–63
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Table 1 Distribution of baseline characteristics of study participants (n = 436). Variable Gender Boys Girls Subtotal Age (years) ≤5 ≥6 Subtotal Child’s premedication with anthelmintics Yes No Subtotal Family’s premedication with anthelmintics Yes No Subtotal Housing Apartment Private residence Row house Subtotal Education of mother High school College and above Subtotal Occupation of mother Housewife Other professions Subtotal Education of father High school College and above Subtotal Occupation of father Officer Laborer Other professions Subtotal Family size ≤3 4 ≥5 Subtotal Number of siblings 1 ≥2 Subtotal Parent’s experience of education about enterobiasis Yes No Subtotal Parent’s knowledge of enterobiasis (M ± SD) Subtotal a
Group medication
Education
Control
X2 /ANOVA (p)
75 (49.3) 77 (50.7) 152
97 (56.4) 75 (43.6) 172
61 (54.5) 51 (45.5) 112
1.677 (.432)
71 (46.7) 81 (53.3) 152
100 (58.1) 72 (41.9) 172
65 (58.0) 47 (42.0) 112
5.172 (.075)
86 (56.6) 66 (43.4) 152
98 (57.3) 73 (42.7) 171
62 (55.4) 50 (44.6) 112
.105 (.949)
76 (50.0) 76 (50.0) 152
79 (46.2) 92 (53.8) 171
54 (48.2) 58 (51.8) 112
1.353 (.508)
126 (83.4) 12 (7.9) 13 (8.7) 151
143 (83.1) 13 (7.6) 16 (9.3) 172
92 (82.1) 15 (13.4) 5 (4.5) 112
5.135 (.274)
39 (25.8) 112 (74.2) 151
38 (22.1) 134 (77.9) 172
37 (33.3) 74 (66.7) 111
2.321 (.313)
87 (57.6) 64 (42.4) 151
81 (47.4) 90 (52.6) 171
50 (45.0) 61 (55.0) 111
5.047 (.080)
40 (26.5) 111 (73.5) 151
36 (20.9) 136 (79.1) 172
29 (25.9) 83 (74.1) 112
1.611 (.447)
61 (41.2) 48 (32.4) 39 (26.4) 148
78 (45.3) 64 (37.3) 30 (17.4) 172
49 (45.4) 46 (42.6) 13 (12.0) 108
9.251 (.055)
21 (13.9) 94 (62.3) 36 (23.8) 151
34 (19.8) 111 (64.5) 27 (15.7) 172
28 (25.0) 63 (56.3) 21 (18.7) 112
7.774 (.100)
17 (11.3) 134 (88.7) 151
25 (14.5) 147 (85.5) 172
24 (21.4) 88 (78.6) 112
5.258 (.072)
10 (6.7) 139 (93.3) 149 7.95 ± 1.54 152
19 (11.1) 152 (88.9) 171 7.83 ± 1.56 172
12 (11.1) 96 (88.9) 108 7.88 ± 1.41 112
.105 (.949)
.264a (.768)
Analysis of variance (ANOVA).
(Table 2). These results showed that parents’ education had some effect to prevent the spread of enterobiasis. Some children were suspected of new infection at three and six months after treatment; the number of new infections in the GM group was lower than in the Edu and control groups (Table 3). Although newly infected children were detected in the Edu group at
Table 2 Prevalence of E. vermicularis eggs positive rate before and after treatment. Group
Group medication Education Control Total
Number of positive/number examined (%) Baseline
3 months after
6 months after
27/152 (17.7%) 17/172 (9.9%) 15/112 (13.4%) 59/436 (13.5%)
1/136 (0.7%) 5/166 (3.0%) 8/104 (7.7%) 14/405 (3.4%)
1/130 (0.8%) 4/149 (2.7%) 8/101 (7.9%) 16/380 (4.2%)
each time point, the number was smaller than in the control group. Moreover, although children diagnosed positive for E. vermicularis eggs were treated with antihelminthic drugs after each diagnostic period, children re-infected with E. vermicularis were found in both Edu and control groups (Table 3). At six months from baseline, the parents’ knowledge about E. vermicularis infection has certainly increased in the Edu group. Moreover, during the 6 months after supplementary education, the percentage of families taking anthelmintic medication themselves increased in the Edu group to 58.1%, compared to 38.7% at baseline (Table 4). 4. Discussion To determine if the prevalence of E. vermicularis infection among children could be controlled by parent’s health education, we
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Table 3 Diagnosis of E. vermicularis infection before and after treatment (n = 436). Group
Diagnosis of E. vermicularis infection Baseline – 3 months after
No. cases/No. examined (%)
3 months after – 6 months after
No. cases/No. examined (%)
Group medication
Negative – Positivea
1/135 (0.7%)
Negative – Positivea Positive – Positiveb
1/129 (0.8%) 0/1 (0.0%)
Education
Negative – Positivea
5/166 (3.0%)
Negative – Positivea Positive – Positiveb
3/144 (2.1%) 1/5 (20.0%)
Control
Negative – Positivea
8/104 (7.7%)
Negative – Positivea Positive – Positiveb
6/93 (6.5%) 2/8 (25.0%)
a b
New infected case. Re-infection case.
Table 4 Parent’s knowledge about E. vermicularis infection and family’s medication (n = 242). Group
Group medication (n = 103)
Knowledge of E. vermicularis infection (M ± SD) 7.76 ± 1.86 Baseline 7.65 ± 1.93 6 months after Family’s medication with anthelmintics N (%) 53 (51.5%) Baseline 68 (66.0%) 6 months after *
Education (n = 62)
Control (n = 77)
7.80 ± 1.50 9.32 ± 1.73*
7.87 ± 1.25 7.63 ± 1.31
24 (38.7%) 36 (58.1%)
32 (41.6%) 14 (18.2%)
Analyzed by paired t-test (t = 5.762, p < .001).
compared enterobiasis infection rates between the parent education (Edu) group and the non-education (control) group, at three and six months after treatment. Most parasitologists have known that enterobiasis in children can easily be eradicated by adequate medical treatment and prevention. Since the mid 1970s, there have been many papers emphasizing ideal therapeutical strategies, especially group therapy and repeated medication for drug resistant larvae (Cho and Kang, 1975; Cho et al., 1976, 1985; Hong et al., 1980). However, most parents have known that antihelminthic medication could easily cure every helminthic infection, including E. vermicularis, by just one time treatment. Therefore, their children were probably taking medication only one time. Also, the parents pay less attention to factors associated with pinworm infection, because they believe that pinworm infection is not fatal and that the worm can be easily eliminated after taking antihelminthic medication only once (Kim et al., 2010). In addition, most directors and teachers in kindergartens have limited knowledge about E. vermincularis infection (personal communication). These factors could maintain steady E. vermicularis egg infection rates among preschool children during the last three decades. In this study, all children in the GM group were medicated with 500 mg albendazole twice, with 15 days interval at baseline. We found that the infection rate of E. vermicularis was dramatically decreased both three and six months after treatment (Table 2). These results revealed that taking anthelminthic medication against E. vermicularis infection is best if all children in the kindergarten receive the therapeutic dose at the same time. However, this is not easy, because consensus among staff of health government and social participants might be necessary, although this method has already been efficient for decreasing infection rates. At six months after treatment, we found recurrence of E. vermicularis infection in both education and control groups (Table 3). This phenomenon might be caused by untreated children diagnosed as negative at the previous examination, but still carrying the parasites. Only children diagnosed as infected were treated with medication in the education and control groups, as the usual community-based control method for enterobiasis in Korea. If children were infected with E. vermicularis eggs 14 days before the diagnosis time point, we could not detect the parasitic eggs, because
the total time from ingestion of the eggs to sexual maturity of the worm is 15–43 days (Roberts et al., 2009). Although the Edu group showed smaller changes than in the GM group, the infection rate in the Edu group was lower than in the control group (Table 2). In addition, new infection or reinfection rates in the Edu group were lower than in the control group (Table 3). In a previous study, the children of parents with little knowledge about enterobiasis had a higher risk of enterobiasis. In addition, although most of the parents knew that good personal hygiene helped to reduce the chances of E. vermicularis infection, they rarely knew about the correct methods for the treatment of E. vermicularis infection (Kim et al., 2010). In the present study, the parents’ knowledge about enterobiasis was significantly increased in the Edu group by sending the brochures to their homes. Moreover, 6 months after supplementary education, the percentage of families taking anthelmintic medication themselves increased in the Edu group with about 20%, compared to baseline (Table 4). In Thailand, a total of 777 children from 11 elementary schools were examined in order to determine the effects of supplying health education. The study showed a decrease in infections among children who received supplementary education (Nithikathkul et al., 2005). In this study, the knowledge about enterobiasis has improved after just one time education using brochures. Therefore, we believe that providing education focused on increasing the parents’ knowledge and practices is more effective than the existing community-based control method for enterobiasis in Korea. Interestingly, at both three and six months after treatment, the occurrence of new infection was found not only in the groups of education and control, but also in the GM group. One possible explanation is that one of the family numbers or siblings carried the E. vermicularis infection and could transmit it to the child. Another possibility is that some places or objects in the preschool might have been contaminated with E. vermicularis eggs. Pinworm eggs have been previously found in the dust from school rooms and school cafeterias, providing a source of infection (Roberts et al., 2009). Based on these results, although all investigated children are free from entorobiasis in the present, occurrence of new infection always will be possible, via new members of the community infected with E. vermicularis. Therefore, it may not be easy to achieve complete eradication of E. vermicularis among children in endemic places by one time parents’ education. Structured parent education programs need to be provided on a regular basis, at least once a year for newly enrolled parents. Furthermore, involvement of preschool directors and teachers into education is important, so that they could control environmental contamination with E. vermicularis eggs. In conclusion, although GM is the best method for eradication of enterobiasis, providing health information about enterobiasis to parents could reduce the prevalence, as well as the rate of new infection and/or re-infection with E. vermicularis in their children. Health educators should provide adequate information, including prevention and treatment of enterobiasis; such efforts will have a
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long-term impact on the prevalence of this infection among children. Conflict of interest None declared. Acknowledgment This work was supported by a 2-Year Research Grant of Pusan National University. References Changsap, B., Nithikathkul, C., Boontan, P., Wannapinyosheep, S., Vongvanich, N., Poister, C., 2002. Enterobiasis in primary schools in Bang Khun Thian District, Bangkok, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 33 (Suppl. 3), 72–75. Cho, S.Y., Kang, S.Y., 1975. Significance of scotch-tape anal swab technique in diagnosis of Enterobius vermicularis infection. Kisaengch’unghak Chapchi 13, 102–114. Cho, S.Y., Kang, S.Y., Kim, S.I., Song, C.Y., 1985. Effect of anthelmintics on the early stage of Enterobius vermicularis. Kisaengch’unghak Chapchi 23, 7–17. Cho, S.Y., Kang, S.Y., Ryang, Y.S., Seo, B.S., 1976. Relationships between the results of repeated anal swab examinations and worm burden of Enterobius vermicularis. Kisaengch’unghak Chapchi 14, 109–116. Degerli, S., Malatyali, E., Ozcelik, S., Celiksoz, A., 2009. Enterobiosis in Sivas Turkey from past to present, effects on primary school children and potential risk factors. Turkiye Parazitolojii Dergisi/Turkiye Parazitoloji Dernegi = Acta parasitologica Turcica/Turkish Society for Parasitology 33, 95–100.
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Hong, S.T., Cho, S.Y., Seo, B.S., Yun, C.K., 1980. Chemotherapeutic control of Enterobius vermicularis infection in orphanages. Kisaengch’unghak Chapchi 18, 37–44. Hopkins, D.R., 1992. Homing in on helminths. The American Journal of Tropical Medicine and Hygiene 46, 626–634. Kang, S., Jeon, H.K., Eom, K.S., Park, J.K., 2006. Egg positive rate of Enterobius vermicularis among preschool children in Cheongju, Chungcheongbuk-do, Korea. The Korean Journal of Parasitology 44, 247–249. Kim, D.H., Son, H.M., Kim, J.Y., Cho, M.K., Park, M.K., Kang, S.Y., Kim, B.Y., Yu, H.S., 2010. Parents’ knowledge about enterobiasis might be one of the most important risk factors for enterobiasis in children. The Korean Journal of Parasitology 48, 121–126. Kliks, M.M., 1990. Helminths as heirlooms and souvenirs: a review of new world paleoparasitology. Parasitology Today (Personal ed.) 6, 93–100. Lee, K.J., Lee, I.Y., Im, K., 2000. Enterobius vermicularis egg positive rate in a primary school in Chungchongnam-do (province) in Korea. The Korean Journal of Parasitology 38, 177–178. Muge, O.A., Baykan, Z., Artan, C., 2008. Enterobiasis among preschool children: a study from Kayseri, Turkey. Japanese Journal of Infectious Diseases 61, 482–483. Nithikathkul, C., Akarachantachote, N., Wannapinyosheep, S., Pumdonming, W., Brodsky, M., Sukthana, Y., 2005. Impact of health educational programmes on the prevalence of enterobiasis in schoolchildren in Thailand. Journal of Helminthology 79, 61–65. Park, J.H., Han, E.T., Kim, W.H., Shin, E.H., Guk, S.M., Kim, J.L., Chai, J.Y., 2005. A survey of Enterobius vermicularis infection among children on western and southern coastal islands of the Republic of Korea. The Korean Journal of Parasitology 43, 129–134. Roberts, L.S., Schmidt, G.D., Janovy, J., 2009. Foundations of Parasitology, 8th ed. McGraw-Hill Higher Education, Boston. Song, H.J., Cho, C.H., Kim, J.S., Choi, M.H., Hong, S.T., 2003. Prevalence and risk factors for enterobiasis among preschool children in a metropolitan city in Korea. Parasitology Research 91, 46–50.
Contents lists available at SciVerse ScienceDirect
Acta Tropica journal homepage: www.elsevier.com/locate/actatropica
Impact of health education on the prevalence of enterobiasis in Korean preschool students In-Soon Kang a,1 , Dong-Hee Kim a,1 , Hye-Gyung An b , Hyun-Mi Son b , Min Kyoung Cho c , Mi-Kyung Park c , Shin Ae Kang c , Bo Young Kim c , Hak Sun Yu c,∗ a
Department of Nursing, College of Nursing, Pusan National University, Yangsan-si, Gyeongsangnam-do 626-870, Republic of Korea Department of Nursing, Youngsan University, Yangsan-si, Gyeongsangnam-do 626-790, Republic of Korea c Department of Parasitology, School of Medicine, Pusan National University, Yangsan-si, Gyeongsangnam-do 626-870, Republic of Korea b
a r t i c l e
i n f o
Article history: Received 9 September 2011 Received in revised form 26 November 2011 Accepted 29 November 2011 Available online 7 December 2011 Keywords: Enterobius vermicularis Cellotape anal swab Health education
a b s t r a c t Health education has been shown to be effective in slowing the spread of the disease, infectious disease in particular. To evaluate the impact of health education on the prevalence and pattern of new infection of enterobiasis, children from 6 kindergartens in Ulsan city, South Korea, were recruited after undergoing a screening for enterobiasis, and then divided into three groups, including group medication (GM), education (Edu), and control group. All children in GM group received medical treatment with 500 mg albendazole twice, with 15 days interval. In the Edu group, only children diagnosed positive for Enterobius vermicularis eggs received medical treatment with 500 mg albendazole twice, with 15 days interval and all parents in the group received brochures providing information about enterobiasis. In the control group, only children diagnosed positive for E. vermicularis eggs received medical treatment with 500 mg albendazole twice, with 15 days interval, and no information about enterobiasis was provided to parents. Two post-treatment examinations were performed at three and six months after treatment. The infection rate in the GM group was dramatically decreased at 3 months, and this rate was almost the same as at 6 months after treatment. Infection rate of children in the Edu group was shown to drop from 9.9% to 3.0% at 3 months, and to 2.7% at 6 months after treatment; however, the infection rate in the control group continued to be higher than in the other two groups at both 3 and 6 months, with smaller change at 3 months compared to the other two groups. In addition, both new infection and re-infection cases in the Edu group were fewer, compared to those in the control group. In conclusion, although GM is the best method for eradication of enterobiasis, providing health information about enterobiasis to parents could reduce the prevalence, as well as the rate of new infection or re-infection with E. vermicularis in their children. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Enterobius vermicularis (pinworm) has infected Homo sapiens since the time of our species origin in Africa, and pinworm infection is a common helminth infection occurring worldwide (Hopkins, 1992; Kliks, 1990). Although the infection rates were different according to geographic location, infections may occur in almost all countries at this time. In Thailand, about 21.6% primary school children were infected with this parasite, 8.2% were infected in Turkey and 10.7% in South Korea (Changsap et al., 2002; Degerli
∗ Corresponding author at: Department of Parasitology, School of Medicine, Pusan National University, Beomeo-ri, Mulgeum-eup, Yangsan-si, Gyeongsangnam-do 626-870, Republic of Korea. Tel.: +82 51 510 8022; fax: +82 51 980 0872. E-mail address: [email protected] (H.S. Yu). 1 These authors contributed equally to this study. 0001-706X/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.actatropica.2011.11.017
et al., 2009; Kim et al., 2010). Although the parasite is highly present in preschool children, practically nothing has been done in most of the countries to eliminate infections. One of the reasons was that the symptoms of enterobiasis are not fatal, and most of the people believe that pinworm infection could be easily eradicated by one time medical treatment, even though that is not enough to kill eggs and larva. During 1970–2000, the government and parasitologists of Korea have struggled to eradicate many human parasite infections; thus, intestinal parasite egg positive rates have been dramatically decreased (from 84.3% in 1971 to 2.4% in 1997) by their efforts (Ministry of Health and Welfare and Korea Association of Health, 2004). Nevertheless, a relatively high egg-positive rate of E. vermicularis, ranging from 7.8% to 18.5%, has been reported in Korean children during the last decade (Kang et al., 2006; Kim et al., 2010; Lee et al., 2000; Park et al., 2005; Song et al., 2003). Two major reasons for not eradicating enterobiasis in preschool children might be the
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increasing number of young children being cared for in kindergartens and either the lack information or mis-information of their care givers, including parents, about E. vermicularis infection (Kim et al., 2010; Song et al., 2003). Many studies have investigated the factors that affect enterobiasis rates in children. Inadequate sanitation, poor level of parental care, no experience of taking an antihelminthic medicine and poor knowledge regarding enterobiasis, including transmission, prevention and how to take antihelminthic treatment have been associated with high prevalence of enterobiasis (Kang et al., 2006; Muge et al., 2008; Song et al., 2003). Comparatively, little emphasis has been put on the impact of health educational intervention on the prevalence of enterobiasis, although increasing health awareness, knowledge about disease and prevention management have all successfully improved many different health outcomes. Nithikathkul et al. (2005) recently evaluated the effect of health educational programs on the prevalence of enterobiasis in school children in Thailand. Educational interventions promoting knowledge of enterobiasis have also proven cost-effective in decreasing re-infection rates in school children (Nithikathkul et al., 2005). To the best of our knowledge, no study has looked at the impact of educational intervention among preschool children. School aged children are old enough to begin taking responsibility for their own personal hygiene, whereas children younger than six years old are still less responsible than older children. Since parents are in charge for their child’s personal hygiene and premedication with antihelminthic drugs, the focus of this study was to give brochures on prevention, transmission and treatment of enterobiasis to parents and to examine the effect on the prevalence of enterobiasis among kindergarten children in Korea. 2. Material and methods 2.1. Subject recruitment and screening evaluation The study protocol was approved by the Ethical Review Committee of Pusan National University Hospital and informed consent was obtained from each participant before enrollment. For recruitment, the letter containing information about the nature, significance, and objectives of the study, copies of a questionnaire, a guide for swab examination and a consent form, were sent to directors of kindergartens registered in the Ulsan Association of Kindergartens. Investigators met with the directors who agreed to participate in this study and described the details of the study. The directors sent a consent form, a letter of information and a questionnaire to the parents of each child. Three thousand nine hundred and forty one children from thirty-six kindergartens underwent a screening for enterobiasis via the cellotape anal swab technique. Kindergartens that had at least 6% of positive egg rates were potentially eligible for this intervention study. On the basis of a combination of egg positive rates and geographic location, eight kindergartens were finally chosen for this intervention study.
2.3. Parent education and medication of children in the selective groups After finishing baseline evaluations, the kindergartens were assigned by a research assistant to GM, Edu, and control groups. Entire classrooms in each kindergarten were tested and a total of 436 children (233 boys and 203 girls) were examined at baseline. At the first post-treatment examination, 405 children were examined, and 380 children participated at the second post-treatment examination. Of 436 parents provided with the pre-treatment questionnaire, 263 parents responded to the follow-up questionnaire and 21 parents did not fully complete their questionnaires. The director of each kindergarten and participants were blinded to the exposure status of participants. Easy-to-understand pictorial brochures were used to convey five messages, including lifespan of E. vermicularis, examination for enterobiasis, symptoms and signs, infection and transmission, and treatment and prevention of enterobiasis. The director of each kindergarten sent these brochures to parents and double checked by phone calls. In the GM group, all children in the kindergarten received medical treatment with 500 mg albendazole twice, with 15 days interval. In the Edu group, only children diagnosed positive for E. vermicularis eggs received medical treatment with 500 mg albendazole twice, with 15 days interval, and all parents in the group received the brochures. In the control group, only children diagnosed positive for E. vermicularis eggs received medical treatment with 500 mg albendazole twice, with 15 days interval (i.e. the usual communitybased control method for enterobiasis in Korea) and no information material was sent to parents. After the study, all participating children were treated with 500 mg albendazole twice, with 15 days interval. 2.4. Study outcome The study outcomes in each study group were the E. vermicularis eggs positive rate and the re-infection rate at three months and six months after enrollment. E. vermicularis infection was evaluated with the cellotape anal swab technique, before and after treatment. The pre-treatment structured questionnaire was provided to the parents of each child, asking about demographics and socioeconomic status and general knowledge of enterobiasis. Knowledge regarding enterobiasis was assessed six months after enrollment using a follow-up questionnaire. 2.5. Statistical analysis Statistical analysis was performed using PASW software (SPSS, Chicago, IL, USA). Baseline characteristics of study participants were compared using proportions. The prevalence of egg positive rate of E. vermicularis at baseline and after treatment was compared using proportions. Comparison of knowledge regarding enterobiasis between baseline and after treatment was performed by the paired t-test.
2.2. Group design
3. Results
To evaluate the effect of education on the prevalence of enterobiasis, we selected 6 kindergartens and divided the children into three groups, including group medication (GM), education (Edu), and control group. E. vermicularis infection rate and the location of the kindergarten were taken into account to determine the grouping. Table 1 shows several characteristics of study participants. After grouping, we compared several characteristics, and most of them were similar in the three groups. The small difference observed between the groups was not statistically significant.
The infection rate in the GM group was dramatically decreased at 3 months from 17.8% to 0.7%, and this rate was almost the same at 6 months after treatment (Table 2). Although the rates in the Edu and control groups were also decreased at the same time points, they were higher than in the GM group. The infection rate in children in the Edu group was shown to decrease from 9.9% to 2.7% at six months after treatment. Both at 3 months and 6 months after treatment, children in the control group had the highest E. vermicularis infection rate, i.e. 7.7% at 3 months and 7.9% at 6 months
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Table 1 Distribution of baseline characteristics of study participants (n = 436). Variable Gender Boys Girls Subtotal Age (years) ≤5 ≥6 Subtotal Child’s premedication with anthelmintics Yes No Subtotal Family’s premedication with anthelmintics Yes No Subtotal Housing Apartment Private residence Row house Subtotal Education of mother High school College and above Subtotal Occupation of mother Housewife Other professions Subtotal Education of father High school College and above Subtotal Occupation of father Officer Laborer Other professions Subtotal Family size ≤3 4 ≥5 Subtotal Number of siblings 1 ≥2 Subtotal Parent’s experience of education about enterobiasis Yes No Subtotal Parent’s knowledge of enterobiasis (M ± SD) Subtotal a
Group medication
Education
Control
X2 /ANOVA (p)
75 (49.3) 77 (50.7) 152
97 (56.4) 75 (43.6) 172
61 (54.5) 51 (45.5) 112
1.677 (.432)
71 (46.7) 81 (53.3) 152
100 (58.1) 72 (41.9) 172
65 (58.0) 47 (42.0) 112
5.172 (.075)
86 (56.6) 66 (43.4) 152
98 (57.3) 73 (42.7) 171
62 (55.4) 50 (44.6) 112
.105 (.949)
76 (50.0) 76 (50.0) 152
79 (46.2) 92 (53.8) 171
54 (48.2) 58 (51.8) 112
1.353 (.508)
126 (83.4) 12 (7.9) 13 (8.7) 151
143 (83.1) 13 (7.6) 16 (9.3) 172
92 (82.1) 15 (13.4) 5 (4.5) 112
5.135 (.274)
39 (25.8) 112 (74.2) 151
38 (22.1) 134 (77.9) 172
37 (33.3) 74 (66.7) 111
2.321 (.313)
87 (57.6) 64 (42.4) 151
81 (47.4) 90 (52.6) 171
50 (45.0) 61 (55.0) 111
5.047 (.080)
40 (26.5) 111 (73.5) 151
36 (20.9) 136 (79.1) 172
29 (25.9) 83 (74.1) 112
1.611 (.447)
61 (41.2) 48 (32.4) 39 (26.4) 148
78 (45.3) 64 (37.3) 30 (17.4) 172
49 (45.4) 46 (42.6) 13 (12.0) 108
9.251 (.055)
21 (13.9) 94 (62.3) 36 (23.8) 151
34 (19.8) 111 (64.5) 27 (15.7) 172
28 (25.0) 63 (56.3) 21 (18.7) 112
7.774 (.100)
17 (11.3) 134 (88.7) 151
25 (14.5) 147 (85.5) 172
24 (21.4) 88 (78.6) 112
5.258 (.072)
10 (6.7) 139 (93.3) 149 7.95 ± 1.54 152
19 (11.1) 152 (88.9) 171 7.83 ± 1.56 172
12 (11.1) 96 (88.9) 108 7.88 ± 1.41 112
.105 (.949)
.264a (.768)
Analysis of variance (ANOVA).
(Table 2). These results showed that parents’ education had some effect to prevent the spread of enterobiasis. Some children were suspected of new infection at three and six months after treatment; the number of new infections in the GM group was lower than in the Edu and control groups (Table 3). Although newly infected children were detected in the Edu group at
Table 2 Prevalence of E. vermicularis eggs positive rate before and after treatment. Group
Group medication Education Control Total
Number of positive/number examined (%) Baseline
3 months after
6 months after
27/152 (17.7%) 17/172 (9.9%) 15/112 (13.4%) 59/436 (13.5%)
1/136 (0.7%) 5/166 (3.0%) 8/104 (7.7%) 14/405 (3.4%)
1/130 (0.8%) 4/149 (2.7%) 8/101 (7.9%) 16/380 (4.2%)
each time point, the number was smaller than in the control group. Moreover, although children diagnosed positive for E. vermicularis eggs were treated with antihelminthic drugs after each diagnostic period, children re-infected with E. vermicularis were found in both Edu and control groups (Table 3). At six months from baseline, the parents’ knowledge about E. vermicularis infection has certainly increased in the Edu group. Moreover, during the 6 months after supplementary education, the percentage of families taking anthelmintic medication themselves increased in the Edu group to 58.1%, compared to 38.7% at baseline (Table 4). 4. Discussion To determine if the prevalence of E. vermicularis infection among children could be controlled by parent’s health education, we
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Table 3 Diagnosis of E. vermicularis infection before and after treatment (n = 436). Group
Diagnosis of E. vermicularis infection Baseline – 3 months after
No. cases/No. examined (%)
3 months after – 6 months after
No. cases/No. examined (%)
Group medication
Negative – Positivea
1/135 (0.7%)
Negative – Positivea Positive – Positiveb
1/129 (0.8%) 0/1 (0.0%)
Education
Negative – Positivea
5/166 (3.0%)
Negative – Positivea Positive – Positiveb
3/144 (2.1%) 1/5 (20.0%)
Control
Negative – Positivea
8/104 (7.7%)
Negative – Positivea Positive – Positiveb
6/93 (6.5%) 2/8 (25.0%)
a b
New infected case. Re-infection case.
Table 4 Parent’s knowledge about E. vermicularis infection and family’s medication (n = 242). Group
Group medication (n = 103)
Knowledge of E. vermicularis infection (M ± SD) 7.76 ± 1.86 Baseline 7.65 ± 1.93 6 months after Family’s medication with anthelmintics N (%) 53 (51.5%) Baseline 68 (66.0%) 6 months after *
Education (n = 62)
Control (n = 77)
7.80 ± 1.50 9.32 ± 1.73*
7.87 ± 1.25 7.63 ± 1.31
24 (38.7%) 36 (58.1%)
32 (41.6%) 14 (18.2%)
Analyzed by paired t-test (t = 5.762, p < .001).
compared enterobiasis infection rates between the parent education (Edu) group and the non-education (control) group, at three and six months after treatment. Most parasitologists have known that enterobiasis in children can easily be eradicated by adequate medical treatment and prevention. Since the mid 1970s, there have been many papers emphasizing ideal therapeutical strategies, especially group therapy and repeated medication for drug resistant larvae (Cho and Kang, 1975; Cho et al., 1976, 1985; Hong et al., 1980). However, most parents have known that antihelminthic medication could easily cure every helminthic infection, including E. vermicularis, by just one time treatment. Therefore, their children were probably taking medication only one time. Also, the parents pay less attention to factors associated with pinworm infection, because they believe that pinworm infection is not fatal and that the worm can be easily eliminated after taking antihelminthic medication only once (Kim et al., 2010). In addition, most directors and teachers in kindergartens have limited knowledge about E. vermincularis infection (personal communication). These factors could maintain steady E. vermicularis egg infection rates among preschool children during the last three decades. In this study, all children in the GM group were medicated with 500 mg albendazole twice, with 15 days interval at baseline. We found that the infection rate of E. vermicularis was dramatically decreased both three and six months after treatment (Table 2). These results revealed that taking anthelminthic medication against E. vermicularis infection is best if all children in the kindergarten receive the therapeutic dose at the same time. However, this is not easy, because consensus among staff of health government and social participants might be necessary, although this method has already been efficient for decreasing infection rates. At six months after treatment, we found recurrence of E. vermicularis infection in both education and control groups (Table 3). This phenomenon might be caused by untreated children diagnosed as negative at the previous examination, but still carrying the parasites. Only children diagnosed as infected were treated with medication in the education and control groups, as the usual community-based control method for enterobiasis in Korea. If children were infected with E. vermicularis eggs 14 days before the diagnosis time point, we could not detect the parasitic eggs, because
the total time from ingestion of the eggs to sexual maturity of the worm is 15–43 days (Roberts et al., 2009). Although the Edu group showed smaller changes than in the GM group, the infection rate in the Edu group was lower than in the control group (Table 2). In addition, new infection or reinfection rates in the Edu group were lower than in the control group (Table 3). In a previous study, the children of parents with little knowledge about enterobiasis had a higher risk of enterobiasis. In addition, although most of the parents knew that good personal hygiene helped to reduce the chances of E. vermicularis infection, they rarely knew about the correct methods for the treatment of E. vermicularis infection (Kim et al., 2010). In the present study, the parents’ knowledge about enterobiasis was significantly increased in the Edu group by sending the brochures to their homes. Moreover, 6 months after supplementary education, the percentage of families taking anthelmintic medication themselves increased in the Edu group with about 20%, compared to baseline (Table 4). In Thailand, a total of 777 children from 11 elementary schools were examined in order to determine the effects of supplying health education. The study showed a decrease in infections among children who received supplementary education (Nithikathkul et al., 2005). In this study, the knowledge about enterobiasis has improved after just one time education using brochures. Therefore, we believe that providing education focused on increasing the parents’ knowledge and practices is more effective than the existing community-based control method for enterobiasis in Korea. Interestingly, at both three and six months after treatment, the occurrence of new infection was found not only in the groups of education and control, but also in the GM group. One possible explanation is that one of the family numbers or siblings carried the E. vermicularis infection and could transmit it to the child. Another possibility is that some places or objects in the preschool might have been contaminated with E. vermicularis eggs. Pinworm eggs have been previously found in the dust from school rooms and school cafeterias, providing a source of infection (Roberts et al., 2009). Based on these results, although all investigated children are free from entorobiasis in the present, occurrence of new infection always will be possible, via new members of the community infected with E. vermicularis. Therefore, it may not be easy to achieve complete eradication of E. vermicularis among children in endemic places by one time parents’ education. Structured parent education programs need to be provided on a regular basis, at least once a year for newly enrolled parents. Furthermore, involvement of preschool directors and teachers into education is important, so that they could control environmental contamination with E. vermicularis eggs. In conclusion, although GM is the best method for eradication of enterobiasis, providing health information about enterobiasis to parents could reduce the prevalence, as well as the rate of new infection and/or re-infection with E. vermicularis in their children. Health educators should provide adequate information, including prevention and treatment of enterobiasis; such efforts will have a
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