New insights of Enterobius vermicularis infection among preschool children in an urban area in Malaysia

Enterobiasis is a common intestinal parasitic infection caused by the nematode, Enterobius vermicularis (pinworm or threadworm). The disease is distributed worldwide and affecting almost one billion peoples from all socioeconomic classes (Burkhart & Burkhart, 2005). It is an infection which predominates in preschool and school children who are easily exposed to inadequate sanitation and overcrowded conditions and who have more active contact with each other than adults (Lohiya et al., 2000). The transmission of infection is usually by oral and respiratory tracts (Brooker & Bundy, 2009). Due to its contagious nature, enterobiasis tends to occur more among large family members and institutions such as nurseries and kindergartens, especially with crowded conditions (Gunawardena et al., 2013).

Although highly prevalent, this infection is often overlooked as most infections remain asymptomatic or cause only mild disturbances such as perianal itching, which may be intense and induce the victim to scratch the affected area resulting in excoriations, haemorrhages and secondary infections (Burkhart & Burkhart, 2005). Other common symptoms of the disease include abdominal discomfort, weight loss, insomnia and restlessness, irritability and emotional instability (Tsibouris et al., 2005). However, serious morbidity such as eosinophilic enterocolitis, appendicitis and pelvic inflammatory disease have been reported as consequences of enterobiasis (Sah & Bhadani, 2006).

It is difficult to detect E. vermicularis eggs in stool because they are detectable only in approximately 5 % of the cases (Chu et al., 2012). Therefore, diagnosis of pinworm is mainly based on detection of the characteristic eggs in the perianal region using swabs or adhesive tape. Alternatively, eggs may be seen in stool samples or scrapings from under finger nails and adult worms may be detected in the perianal skin at night. Swabbing needs to be done at night to coincide with oviposition or first thing in the morning prior to washing or cleaning the perianal region (Brooker & Bundy, 2009).

In Malaysia, only a few reports have been published regarding the prevalence of pinworm among children (Noor Hayati & Rajeswari, 1991; Rahman, 1991). A relatively high egg positive rate (40.4 %) has been reported by Norhayati et al. (1994) among children aged 1 – 8 years living in a rural area in Labu and Dengkil. Up to this date, there are no comprehensive data describing the epidemiology of enterobiasis among preschool children living in an urban area. Within this context, a cross-sectional study was undertaken to assess the prevalence and to identify underlying risk factors associated with E. vermicularis infection among children aged 1 – 6 years.

E. vermicularis infection is generally considered to be a nuisance rather than a fatal disease. However, the level of morbidity is significant especially in preschool children. Although this infection can be readily cured by anthelmintic, the prevalence of enterobiasis has not diminished over the past decade. This could be attributed to the relative ease of transmission causing frequent re-infections and the failure to clear parasites due to incomplete medication. As shown by the results of the present study, the overall egg positive rate of E. vermicularis was 12.5 % among preschool children in urban area. These findings are consistent with a previous study by Song et al. (2003), which reported a prevalence rate of 9.5 % among preschool children in a metropolitan city in Korea. To the best of our knowledge, the only past study on enterobiasis in urban area was done over twenty years ago. It reported a prevalence rate of 41.7 % among children aged 1 – 12 years living in a multi-storey flats in Malaysia (Noor Hayati & Rajeswari, 1991). Nowadays, the society particularly those who lived in urban area have been exposed to authentic information provided by the current media. This exposure has reinforced parental knowledge of public issues and has enable parents to produce more adequate care for their children. This explained why the infection rate of pinworm has tremendously declined as compared to previous local study. In such countries, a significant reduction in prevalence is obvious when comparing results of surveys done before and after year 2000. In Turkey, the overall rate of enterobiasis (45.9 %) observed in the period 1985 – 2000 decreased to 16 % in the period 2000 – 2008 (Degerli et al., 2009).

Current results also showed that the infection rate was almost comparable and no statistically significant differences were found between boys and girls, which conformed with the previous finding (Muge et al., 2008). It has been noted that the prevelance of enterobiasis is significantly higher among children aged 5 – 6 years in our study which is in parallel with Norhayati et al. (1994). The cause of this trend could be due to inadequate personal hygiene of the older children and playing with dirty toys. Furthermore, the play activity program for children of 5 – 6 years is slightly different from that of younger children, aged 1 – 4 years as they play outside of the kindergarten instead of taking a nap. Therefore, they have more opportunity to play with dirt and have more physical contact with their friends than their counterpart in nurseries. Another possible cause is also iterative self-infection if an earlier infection has remained untreated.

Another interesting finding of our study was the significant association observed between personal hygiene and E. vermicularis infection among preschool children. This study indicated that children with the habits of finger sucking evidenced significantly higher rates of enterobiasis than those who did not have this habit. It is well known that children who harbor this infection may scratch the contaminated perianal skin and unintentionally transfer the eggs on finger to the mouth. The present findings are consistent with a studies carried out by Sung et al. (2001) and Kim et al. (2010). However, other factors such as nail biting, frequency of bathing and failure to wash hands before meals were not found to be significantly associated with enterobiasis in the present study. The sanitary environment has been greatly improved by urbanization during the last decades and parents tend to pay more attention to their children than before, placing a higher priority on children’s welfare. Therefore, personal hygiene had little effect on the prevalence of E. vermicularis infection in our study, although personal hygiene and exposure to infected subjects are still important (Cook, 1994).

Epidemiologic studies have shown that children from large family members (>4) has three fold higher risk of acquiring pinworm and this finding is consistent with a previous study from Turkey (Muge et al., 2008). This could be attributed to the more frequent contact with other children. If children from the same family attend different establishments from which they get infected, they could infect other members of the family. By contrast, Song et al. (2003) and Norhayati et al. (1994) did not found any significant association between large family members and the risk of enterobiasis.

It is interesting to note that pre-medication with anthelminthics was found to have a great impact on decreasing the egg positive rate of pinworm in our study. In Malaysia, a nationwide survey and the mass treatment of infected persons have been undertaken to control trichuriasis, ascariasis and hookworm infection over several decades. This has resulted in the successful control of STHs to a level of 57 % (trichuriasis), 23.8 % (ascariasis) and 7.4 % (hookworm infection) in 2011 (Anuar et al., 2014). Even though the children’s parents were not informed about the nature of our study prior to the anal swab sampling, the taking of anthelmintic proved to significantly reduce the egg positive rate of pinworm in their children. This finding was also supported by Song et al. (2003). The findings of the present study may have been limited by several factors. Firstly, the unwillingness of some parents and children to participate in the study because of the invasion of their privacy. They were also discouraged as they believed that the results of the study might be easily traced since their demographic and socioeconomic data were recorded. These factors also impacted negatively on the sample size with a likelihood of underestimating the true prevalence of the infection in nurseries and kindergartens. Secondly, directors and teachers of nurseries and kindergartens included in the study hesitated to provide information regarding the characteristics of both places, such as the frequent of the toys were washed, the numbers of children in a class and how frequently that the classroom was cleaned. Hence, we were not able to assess the potential predictors associated with the environment of those places.

In conclusion, enterobiasis is still common among preschool children in an urban area in Malaysia. Due to its rapid rate of spread and high re-infection rate among children in the same class or among family members, a long term follow up of the infection rate should facilitate the establishment of an effective E. vermicularis program, especially when coupled with the vigilant and timely administration of appropriate medication. Furthermore, it is also necessary to identify environmental risk factors for enterobiasis in nurseries and kindergartens as the majority of pinworm infection might be transmitted in those places, in order to control the infection.