Prevalence of Enterobius vermicularis Infection among Preschool Children in Kindergartens of Taipei City, Taiwan in 2008

Article information

Korean J Parasitol. 2009;47(2):185-187
Publication date (electronic) : 2009 May 27
doi : https://doi.org/10.3347/kjp.2009.47.2.185
1Department of Parasitology, Taipei Medical University College of Medicine, 250 Wu-Hsing Street, Taipei 110-31, Taiwan.
2School of Medical Laboratory Science & Biotechnology, Taipei Medical University College of Medicine, 250 Wu-Hsing Street, Taipei 110-31, Taiwan.
3Division of Gastroenterology, Department of Internal Medicine, Taipei Medical University College of Medicine, 250 Wu-Hsing Street, Taipei 110-31, Taiwan.
4Department of Laboratory Medicine, Taipei City Hospital Yang-Ming Branch, 105 Yusheng Street, Shihlin, Taipei 111, Taiwan.
Corresponding author (tedfan@tmu.edu.tw)
Received 2008 October 28; Revised 2009 March 24; Accepted 2009 March 31.

Abstract

The prevalence of Enterobius vermicularis infection among preschool children was reported to be low based on a 5-year screening program in Taipei City, Taiwan. The Taipei City government intended to terminate the E. vermicularis screening program among preschool children. Thus, we were entrusted with confirming whether pinworm infections among preschool children in Taipei City had truly declined. From each of 12 administrative districts 2-3 kindergartens were randomly selected for investigation. In total, 4,349 children were examined, of which 2,537 were boys and 1,812 were girls. The cellophane tape adhered to a glass slide was used, and all examinations were done by certified medical technologists. Results indicated that the overall prevalence rate of pinworm infections was 0.62% (27/4,349). Although the infection rate was higher among boys (0.67%, 17/2,537) than in girls (0.55%, 10/1,812), no significant difference was found (χ2 = 0.399, P = 0.62). According to the administrative district, the infection rate ranged from no positive cases of E. vermicularis infection in the Xinyi, Zhongzhen, and Wanhua Districts (0%; 0/299, 0/165, and 0/358, respectively), to 0.26% (1/131) in Songshan District, with the highest rate of 1.88% (7/373) in Wenshan District. Because the overall infection rate (0.62%, 27/4,349) in the present study was unchanged compared to that (0.40%, 197/49,541) previously reported in 2005, we propose that regular pinworm screening and treatment programs should be continued in some parts of Taipei City.

Enterobius vermicularis (pinworm) is the most successful intestinal nematode to thrive among human populations with over 400 million infected people worldwide [1]. The most commonly infected group are schoolchildren living in crowded environments such as summer camps and institutions, with hygiene and exposure being important factors [2]. Female worms deposit their eggs near the anus on the perianal skin. Some of these eggs are detached from the perianal region and lodge on clothing, bedding, and other surfaces. Infection takes place through ingestion or inhalation of infective eggs or retrograde migration of hatched juveniles from the anus to the intestines. Enterobiasis is usually asymptomatic or accompanied by perianal pruritus. However, there can be symptoms of restlessness, loss of appetite, insomnia, and irritability, particularly in children with high parasitic burdens [1,2]. In rare instances, pinworms can cause serious gastrointestinal problems and ectopic infections [3-6]. Diagnosis of pinworm infection is made upon the microscopic detection of eggs. Since only about 5% of eggs turn up in stools, the cellophane tape test should be used for screening instead of stool examinations [1]. While pinworms can be readily treated by mebendazole, a strict regime of treatment needs to be followed to control the parasite because of its ease of transmission and reinfection [7].

Taipei City, which has undertaken an annual mass pinworm screening and treatment program since 1990 [8], had a decreasing prevalence rate among preschool children of 4.3% in 1990 to 0.40% (197/49,541) in 2007 [8,9]. The city government's screening used a traditional method of cellophane tapes, and samples were primarily collected by children's parents. Using this method, the adhesive side of the tape is applied to the perianal region and then folded together for microscopic inspection. However, there is difficulty in identifying eggs due to overlapping tape layers with this method and to parents who might not be familiar with performing the procedure correctly that might have led to false negative results and an underestimation of the infection rate [8-10]. In this study, we investigated the prevalence of pinworm infection among preschool children in kindergartens in Taipei City using the modified cellophane tape method described by Kucik et al. [1].

From each of 12 city districts, 2-3 kindergartens were randomly selected for investigation. In total, 4,349 children were examined between 09:00 and 12:00 in the morning, of which 2,537 were boys and 1,812 were girls. The cellophane tape adhering to glass slides was used, and all examinations were done by certified medical technologists. Parents were notified of the procedure beforehand and were asked not to shower their children or have them defecate in the morning of the examination, with letters of consent sent to be signed and returned before the examinations were undertaken. Collected specimens were screened microscopically for pinworm eggs by at least 3 medical technologists. All of the data were processed by statistical software SPSS version 10.0 (SPSS, Chicago, Illinois, USA). The chi-square test was used for the statistical analysis. P value of ≤ 0.05 indicated a significant difference between 2 results.

Results indicated that the overall prevalence rate of pinworm infections was rather low (0.62%, 27/4,349) (Table 1). Compared to other countries, our present figure was much lower than that reported in Busan City (8.9%, 13/146) [11], Chungchongnam-do (14.8%, 28/189) [12], and Cheongju City (13.4%, 75/561) [13], Korea, and also in southeastern Estonia (24.4%, 233/954) [14]. In the present study, the E. vermicularis infection rate was found to be higher among boys (0.67%, 17/2,537) than in girls (0.55%, 10/1,812), but the difference was not significant (χ2 = 0.399, P = 0.62) (Table 1). This finding was previously reported worldwide [11-14]. Preschool children contact each other more frequently in kindergartens and are also exposed to unsatisfactory sanitary environments [15]. Inadequate personal hygiene can also increase the risk of E. vermicularis infection among preschool children, particularly boys. Other factors, including playing on the floor, nail biting, a failure to wash hands before meals, and living in non-apartment dwellings, were also reported to be associated with the prevalence of enterobiasis [16].

Prevalence of Enterobius vermicularis infection among preschool children in kindergartens of Taipei City in 2008

According to administrative districts, the highest rate was found in Wenshan District (1.9%, 7/373), followed by Beitou (1.2%, 7/608), Nangang (0.79%, 3/380), Daan (0.75%, 3/401), Neihu (0.62%, 2/323), Datong (0.42%, 2/473), Shilin (0.39%, 1/258), Zhongshan (0.31%, 1/318), and Songshan Districts (0.26%, 1/391). No positive cases of E. vermicularis eggs were found in samples obtained in Xinyi (0%, 0/299), Zhongzhen (0%, 0/165), or Wanhua Districts (0%, 0/358) (Table 1). Although Jang et al. [8] indicated that families with a low economic status have a higher association with E. vermicularis infection among preschool children in Taipei City, the average annual incomes for families in Wenshan and Beitou Districts are not lower compared to those of other districts [8]; it was proposed that parents might overlook the importance of personal hygiene of children, thus resulting in a higher prevalence of E. vermicularis infection in both districts.

The pinworm has the largest geographic distribution among human intestinal parasites. A part of the reasons for successful maintenance of its prevalence may include the mildness of symptoms in most infections, leading health officials to often focus their efforts on other relevant parasites instead [1]. However, the importance of pinworm infections among children should not be overlooked. Although the symptoms of infection are often mild, the itchiness and restlessness which children experience from the infections can be discomforting and effect their learning, and the shame of having "worms" can have a negative impact on their mental health. In rare cases, enterobiasis has led to serious consequences such as appendicitis [5], eosinophilic colitis [4,5], intestinal obstruction, intestinal perforation, and ectopic infections [6].

In addition, pinworms have also been suggested as a possible vector for Dientamoeba fragilis, a protozoan regarded as a neglected cause of diarrhea [17]. Taipei City Government has performed a long-term pinworm screening and treatment program since 1990, in which all family members of a child determined to have a pinworm infection are informed and assigned to see an appointed doctor at Taipei Municipal Hospital, and this demarche indeed produced an ideal outcome of decreasing adolescent pinworm prevalence in Taipei City. We still suggest that the city government continue its annual screening program and use the modified cellophane test method used in this study in the future to confirm the accuracy of its annual pinworm screening.

ACKNOWLEDGEMENTS

We are grateful for the financial support by Department of Health, Taipei City Government, Taiwan.

References

1. Kucik CJ, Martin GL, Sortor BV. Common intestinal parasites. Am Fam Physician 2004. 691161–1168. 15023017.
2. Cook GC. Enterobius vermicularis infection. Gut 1994. 351159–1162. 7959218.
3. Petro M, Iavu K, Minocha A. Unusual endoscopic and microscopic view of Enterobius vermicularis: a case report with a review of the literature. South Med J 2005. 98927–929. 16217987.
4. Liu LX, Chi J, Upton MP, Ash LR. Eosinophilic colitis associated with larvae of the pinworm Enterobius vermicularis. Lancet 1995. 346410–412. 7623572.
5. Arca MJ, Gates RL, Groner JI, Hammond S, Caniano DA. Clinical manifestations of appendiceal pinworms in children: an institutional experience and a review of literature. Pediatr Surg Int 2004. 20372–375. 15141320.
6. Quasem A, Salam A. Ectopic enterobiasis: a case report and review of literature. Pak J Med Sci 2007. 23785–787.
7. Lohiya GS, Tan-Figueroa L, Crinella FM, Lohiya S. Epidemiology and control of enterobiasis in a developmental center. West J Med 2000. 172305–308. 10832422.
8. Jang MH, Hsu HJ, Lo HM, Hsu CS, Chen RC, Chiu AW. Prevalence of Enterobius vermicularis infection among children attending preschools in Taipei City. Taipei City Med J 2007. 4565–572.
9. Hsieh HC. Human parasites in Taiwan. Chin J Parasitol 1994. 71–6.
10. Fan PC. Review of enterobiasis in Taiwan and offshore islands. J Microbiol Immunol Infect 1998. 31203–210. 10496160.
11. 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. 43129–134. 16340301.
12. Lee KJ, Lee IY, Im KI. Enterobius vermicularis egg positive rate in a primary school in Chungchongnam-do (Province) in Korea. Korean J Parasitol 2000. 38177–178. 11002654.
13. 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. 44247–249. 16969064.
14. Remm M. Distribution of enterobiasis among nursery school children in SE Estonia and of other helminthiases in Estonia. Parasitol Res 2006. 99729–736. 16752158.
15. Kim BJ, Lee BY, Chung HK, Lee YS, Lee KH, Chung HJ, Ock MS. Egg positive rate of Enterobius vermicularis of primary school children in Geoje island. Korean J Parasitol 2003. 4175–77. 12666734.
16. Sung JF, Lin RS, Huang KC, Wang SY, Lu YJ. Pinworm control and risk factors of pinworm infection among primary-school children in Taiwan. Am J Trop Med Hyg 2001. 65558–562. 11716114.
17. Girginkardesler N, Kurt O, Kilimcioğlu AA, Ok UZ. Transmission of Dientamoeba fragilis: evaluation of the role of Enterobius vermicularis. Parasitol Int 2008. 5772–75. 17921047.

Article information Continued

Table 1.

Prevalence of Enterobius vermicularis infection among preschool children in kindergartens of Taipei City in 2008

Category No. examined No. positive (%) Chi-square test
χ2 P value
Gender
 Boys 2,357 17 (0.67)
 Girls 1,821 10 (0.55) 0.40 0.62
Administrative district
 Wenshan district 373 7 (1.9) - -
 Beitou district 608 7 (1.2) - -
 Nangang district 380 3 (0.79) - -
 Daan district 401 3 (0.75) - -
 Neihu district 323 2 (0.62) - -
 Datong district 473 2 (0.42) - -
 Shilin district 258 1 (0.39) - -
 Zhongshan district 318 1 (0.31) - -
 Songshan district 391 1 (0.26) - -
 Xinyi district 299 0 (0.00) - -
 Zhongzhen district 165 0 (0.00) - -
 Wanhua district 358 0 (0.00) - -
Total 4,349 27 (0.62) - -