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Comparison of Egg Positive Rates of Enterobius vermicularis among Preschool Children in Three Korean Localities
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Comparison of Egg Positive Rates of Enterobius vermicularis among Preschool Children in Three Korean Localities

The Korean Journal of Parasitology 2011;49(4):441-443.
Published online: December 16, 2011

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Corresponding author (jo4u@cdc.go.kr)

Hong and Lee equally contributed as the first author of this work.

• Received: May 31, 2011   • Revised: August 10, 2011   • Accepted: August 10, 2011

© 2011, Korean Society for Parasitology

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • This survey was performed to investigate and compare egg positive rates (EPRs) of Enterobius vermicularis among preschool children in 3 Korean localities (Chuncheon-si, Inje-gun, and Paju-si) in 2008. A total of 7,048 preschool children were examined. Overall, the total EPR was 4.0%; the EPR was the highest in Chuncheon-si (5.6%), followed by Inje-gun (4.5%) and Paju-si (3.4%). The EPR of boys (4.9%) was higher than that of girls (3.1%). The EPR significantly increased with age, with the highest observed in 5~7-year-olds. These findings demonstrate that E. vermicularis infection is widely prevalent among preschool children in Chuncheon-si, Inje-gun, and Paju-si, Republic of Korea.
Enterobius vermicularis is one of the most highly prevalent gastrointestinal worms in children; more than 30% of children around the world are infected [1]. Especially, school-age children (5~14-year-olds) are predominantly subjected to E. vermicularis infection [2]. Enterobiasis is usually asymptomatic, but it may cause perianal pruritus, discomfort, insomnia, and restlessness in children. Reasons for the continued presence of the worm among children include improper treatment, reinfection, and rapid transmission among children [3,4]. For these reasons, a continuous epidemiologic survey of enterobiasis in children is being regionally undertaken. In the Republic of Korea, the prevalence of E. vermicularis infection has been reported in various regions with varied egg positive rates (EPRs). However, the majority of the survey was performed in primary school children, with limited data in preschool children. Recently, the EPRs in primary school children ranged from 9.8% to 18.6% [5-7], whereas they ranged from 7.9% to 18.1% in preschool children [7-9]. However, previous assessments of the prevalence of E. vermicularis infection in preschool children have been limited to local regions or cities, with no comparisons of the EPR among preschool children in different cities and different regions.
Therefore, the present survey was performed to investigate and compare the EPR of E. vermicularis in preschool children among 3 different localities of Korea. In 2008, a total of 7,048 preschool children were sampled from 188 kindergartens in Chuncheon-si (1,441 children from 23 kindergartens, urban area) located in a western part of Gangwon-do, an area of Inje-gun (788 children from 17 kindergartens, mountainous area) located in the central part of Gangwon-do, and in Paju-si (4,819 children from 148 kindergartens, rural area) in Gyeonggi-do (Fig. 1). In order to estimate the EPR of E. vermicularis, the adhesive cello-tape anal swab method was used only once. All examinations were carried out with permission of the preschool teachers and the children's parents. Pressings were performed by the parents at 7-9 a.m. who followed the authors' guidance, and all samples were collected by the teachers of the kindergartens. Thereafter, the samples were transported to the Division of Malaria and Parasitic Diseases, Korea National Institute of Health. Statistical analyses were conducted using the SPSS software (version 17.0 K); the chi-square test and the linearity test were used on all data. The statistical significance (P<0.05) was defined at 95% confidence interval.
Of the 7,048 children examined, 4.0% were found to be positive for E. vermicularis eggs; this value was lower compared to the EPR observed in other cities such as 7.9% in Cheongju [8], 10.7% in Busan [10], and 28.4% in Wonju-si [11]. Analysis by region revealed that the EPR was the highest in Chuncheon-si (5.7%), followed by Inje-gun (4.6%) and Paju-si (3.5%) (Table 1). There was no significant difference between the urban (Chuncheon-si and Paju-si) and mountainous (Inje-gun) areas. However, in the same region, the EPR was higher in urban areas (Chuncheon-si) than in mountainous areas (Inje-gun), which was similar to a previous report by Kim et al. [11] (P<0.0001) (Table 1). The reason why the EPR was higher in urban areas compared with mountainous and rural areas could be explained by epidemiological characteristics of E. vermicularis infection, such as high population density and crowded condition in kindergartens [10]. In addition, the EPR in kindergartens observed in this survey was lower when it was compared to a previous report in Chuncheon-si by Yoon et al. [12]. The risk factors for the lower EPR in the present study was not surveyed, therefore, further studies on changes of personal hygiene, life style in kindergartens, and environment should be performed. The EPRs recorded in Inje-gun and Paju-si could not be compared with other data, because there were no previous data on enterobiasis prevalence in preschool children in Inje-gun and Paju-si. In our study, we have proven that enterobiasis is indeed present among preschool children in these 2 localities.
With regard to gender, the total EPR in boys (4.9%) was significantly higher than that in girls (3.1%) (P=0.0001), and this tendency was observed in all localities (Table 1). The EPR in boys was significantly higher than that in girls in Chuncheon-si and Paju-si, but there was no statistical difference in Inje-gun (data not shown). The reason why the EPR was higher in boys than that in girls was not surveyed in the present study. Thus, further studies on high prevalence of E. vermicularis infection in boys compared to girls should be needed. With regard to age, E. vermicularis eggs were found to be prevalent across all ages, from less than 3-year-olds to 7-year-olds, in our study, and high EPRs were observed in 5~7-year-olds group (P<0.0001, Table 1). The EPR was also found to significantly increase with age (P=0.0017), as previously reported by Kang et al. [8]. Especially, the EPR in Paju-si had a high tendency to increase with age (P=0.0002) and similar tendency was shown in Inje-gun (P=0.012) (Table 2). Park et al. [7] and Kang et al. [8] previously reported that the EPR was highest in 5-year-olds, and Song et al. [9] reported that the EPR was particularly high in over 6-year-olds. In the present study, 7-year-olds showed the highest EPR compared with younger children in general (Table 2). However, the age group with the highest EPR differed between cities: 5-year-olds in Chuncheon-si, 6-year-olds in Inje-gun, and 7-year-olds in Paju-si. The reason for this difference is unclear at this point. Nevertheless, it may be assumed that many factors of personal hygiene, such as thumb-sucking. Fingernail trimming are associated with age groups with the level of EPR in each city [9,10], but further analysis of this observation is necessary.
The most important finding in this survey was not the observation that specific age groups showed the highest EPR in different localities, but the observation that enterobiasis was prevalent across all age groups in all surveyed localities. These days, many children are taken to the kindergarten during the daytime before entering primary schools. Consequently, E. vermicularis infection can easily occur and keep spreading rapidly in kindergartens. This study had 2 limitations. First, the scotch-tape sample collection for E. vermicularis was conducted by their parents, untrained personnel, who may not be able to follow exactly the recommended protocols. Second, it is well known that the EPR for E. vermicularis increases with repeated scotch-tape tests [11]. The sample collection and test in the present study was conducted only 1 time. Therefore, the actual EPR for E. vermicularis may have been higher than the results obtained in the present study. In conclusion, E. vermicularis infection is widely prevalent among preschool children in 3 different localities of Korea, Chuncheon-si, Inje-gun, and Paju-si.
This work was supported by a grant (NIH-4847-302-210-13, 2008) from the Korea National Institute of Health, Republic of Korea.
  • 1. Kucik CJ, Martin GL, Sortor BV. Common intestinal parasites. Am Fam Physician 2004;69:1161-1169.
  • 2. Cook GC. Enterobius vermicularis infection. Gut 1994;35:1159-1162.
  • 3. Lohiya GS, Tan-Figueroa L, Crinella FM, Lohiya S. Epidemiology and control of enterobiasis in a developmental center. West J Med 2000;172:305-308.
  • 4. Arca MJ, Gates RL, Groner JI, Hammond S, Caniano DA. Clinical manifestations of appendiceal pinworms in children: An institutional experience and a review of the literature. Pediatr Surg Int 2004;20:372-375.
  • 5. Lee KJ, Lee IY, Im K. Enterobius vermicularis egg positive rate in a primary school in Chungchongnam-do (Province) in Korea. Korean J Parasitol 2000;38:177-178.
  • 6. Lee KJ, Ahn YK, Ryang YS. Enterobius vermicularis egg positive rates in primary school children in Gangwon-do (Province), Korea. Korean J Parasitol 2001;39:327-328.
  • 7. Park JH, Han ET, Kim WH, Shin EH, Guk SM, Kim JL, Chai JY. A survey of Enterobius vermicularis infection among children on western and southern coastal islands of the Republic of Korea. Korean J parasitol 2005;43:129-134.
  • 8. Kang S, Jeon HK, Eom KS, Park JK. Egg positive rate of Enterobius vermicularis among preschool children in Cheongju, Chungcheongbuk-do, Korea. Korean J Parasitol 2006;44:247-249.
  • 9. Song HJ, Cho CH, Kim JS, Choi MH, Hong ST. Prevalence and risk factors for enterobiasis among preschool children in a metropolitan city in Korea. Parasitol Res 2003;91:46-50.
  • 10. Kim DH, Son HM, Kim JY, Cho MK, Park MK, Kang SY, Kim BY, Yu HS. Parents' knowledge about enterobiasis might be one of the most important risk factors for enterobiasis in children. Korean J Parasitol 2010;48:121-126.
  • 11. Kim JS, Lee HY, Ahn YK. Prevalence of Enterobius vermicularis infection and preventive effects of mass treatment among children in rural and urban areas, and children in orphanages. Korean J Parasitol 1991;29:235-243.
  • 12. Yoon HJ, Choi YJ, Lee SU, Park HY, Huh S, Yang YS. Enterobius vermicularis egg positive rate of pre-school children in Chunchon, Korea (1999). Korean J Parasitol 2000;38:279-281.
Fig. 1
The 3 localities on the map of South Korea.
kjp-49-441-g001.jpg
Table 1.
Egg positive rates of Enterobius vermicularis by sex among preschool children in 3 localities
Table 1.
Category No. of total examined No. of positive children (%) Adjusted
OR (95%CI) P-value
Total 7,048 285 (4.0)
Gender
 Girl 3,313 102 (3.1) 1 -
 Boy 3,735 183 (4.9) 1.6 (1.3-2.1) 0.0001
Age
 0-4 2,252 46 (2.0) 1 -
 5-7 4,796 239 (5.0) 2.5 (1.8-3.5) < 0.0001
Region
 Paju-si 4,819 167 (3.5) 1 -
 Inje-gun 788 36 (4.6) 1.2 (0.8-1.7) 0.3717
 Chuncheon-si 1,441 82 (5.7) 1.8 (1.4-2.4) < 0.0001
Table 2.
Distribution of egg positive rates for E. vermicularis by age among preschool children in 3 localities
Table 2.
City Age (No. of egg positive cases/ No. examined)
P-value for linearity test
< 3 3 4 5 6 7
Chuncheon-si (%) 4/90 (4.4) 10/180 (5.5) 12/254(4.7) 28/398 (7.0) 21/360 (5.8) 7/159 (4.4) 0.7498
Inje-gun (%) 0 (0) 0/19 (0) 1/93 (1.0) 9/235 (3.8) 16/242 (6.6) 10/199 (5.0) 0.0120
Paju-si (%) 4/414 (1.0) 3/451 (0.6) 12/751 (1.6) 38/1,064 (3.5) 51/1,153 (4.4) 59/986 (5.9) 0.0002
Total (%) 8/504 (1.5) 13/650 (2.0) 25/1,098 (2.2) 75/1,697 (4.4) 88/1,755 (5.0) 76/1,344 (5.6) 0.0017

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Comparison of Egg Positive Rates of Enterobius vermicularis among Preschool Children in Three Korean Localities
Korean J Parasitol. 2011;49(4):441-443.   Published online December 16, 2011
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Comparison of Egg Positive Rates of Enterobius vermicularis among Preschool Children in Three Korean Localities
Korean J Parasitol. 2011;49(4):441-443.   Published online December 16, 2011
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Comparison of Egg Positive Rates of Enterobius vermicularis among Preschool Children in Three Korean Localities
Image
Fig. 1 The 3 localities on the map of South Korea.
Comparison of Egg Positive Rates of Enterobius vermicularis among Preschool Children in Three Korean Localities
Category No. of total examined No. of positive children (%) Adjusted
OR (95%CI) P-value Total 7,048 285 (4.0) Gender  Girl 3,313 102 (3.1) 1 -  Boy 3,735 183 (4.9) 1.6 (1.3-2.1) 0.0001 Age  0-4 2,252 46 (2.0) 1 -  5-7 4,796 239 (5.0) 2.5 (1.8-3.5) < 0.0001 Region  Paju-si 4,819 167 (3.5) 1 -  Inje-gun 788 36 (4.6) 1.2 (0.8-1.7) 0.3717  Chuncheon-si 1,441 82 (5.7) 1.8 (1.4-2.4) < 0.0001 City Age (No. of egg positive cases/ No. examined)
P-value for linearity test < 3 3 4 5 6 7 Chuncheon-si (%) 4/90 (4.4) 10/180 (5.5) 12/254(4.7) 28/398 (7.0) 21/360 (5.8) 7/159 (4.4) 0.7498 Inje-gun (%) 0 (0) 0/19 (0) 1/93 (1.0) 9/235 (3.8) 16/242 (6.6) 10/199 (5.0) 0.0120 Paju-si (%) 4/414 (1.0) 3/451 (0.6) 12/751 (1.6) 38/1,064 (3.5) 51/1,153 (4.4) 59/986 (5.9) 0.0002 Total (%) 8/504 (1.5) 13/650 (2.0) 25/1,098 (2.2) 75/1,697 (4.4) 88/1,755 (5.0) 76/1,344 (5.6) 0.0017
Table 1. Egg positive rates of Enterobius vermicularis by sex among preschool children in 3 localities
Table 2. Distribution of egg positive rates for E. vermicularis by age among preschool children in 3 localities