1. bookVolumen 53 (2016): Heft 1 (March 2016)
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22 Apr 2006
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New insights of Enterobius vermicularis infection among preschool children in an urban area in Malaysia

Online veröffentlicht: 10 Mar 2016
Volumen & Heft: Volumen 53 (2016) - Heft 1 (March 2016)
Seitenbereich: 76 - 80
Eingereicht: 29 May 2015
Akzeptiert: 07 Oct 2015
Zeitschriftendaten
License
Format
Zeitschrift
eISSN
1336-9083
ISSN
0440-6605
Erstveröffentlichung
22 Apr 2006
Erscheinungsweise
4 Hefte pro Jahr
Sprachen
Englisch
Introduction

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.

Materials and Methods
Study area

This was a cross-sectional study conducted in Kota Damansara, Malaysia between April and May 2012. Kota Damansara is a township located under the Subang parliamentary constituency. It was spread across 4,000 acre (16 km2) of land with a metropolitan setting. The metropolitan areas are planned, less crowded with near adequate infrastructure social amenities but with good sanitation. A great number of the residents in the metropolitan area are high income earners and include senior civil or public servants and chief executive officers from the organized private sector. It had a population of 516,666 in 2010. The numbers of children under 10 years old was 71,829 (13.9 %) (Population & Housing Census of Malaysia, 2010).

Subject recruitment and consents

The study protocol was approved by the Ethical Review Committee of Universiti Kebangsaan Malaysia Medical Centre (UKM 1.5.3/289/FF–301–2012) and informed consent was obtained from each subject before enrollment. For enrollment, the letter containing data about the nature, implication and objectives of the study, copies of a questionnaire, a guide for swab examination and a consent form were sent to directors of enrolled nurseries and kindergartens. One hundred and thirty six children from four nurseries and four kindergartens underwent a screening for enterobiasis via the cellotape anal swab technique. 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 laboratory examinations were undertaken. The researchers then collected the slides with the questionnaire, on the same day.

Collection of anal swabs

All samples were collected between 06:00 and 08:00, just after the children had woken up but before they had bathed. Each subject was sampled only once due to poor co-operation of the subject and/or their parents.

Questionnaire survey

A pre-tested self-administered questionnaire completed by the parents were used to evaluate the risk factors and clinical manifestations associated with enterobiasis. The information collected included finger sucking, nail biting, frequency of bathing, hand washing behavior, the number of household members and recent pre-medication of anthelmintic. On return of the swabs and completed questionnaire, the parents were educated on transmission and prevention of enterobiasis through leaflets.

Detection of pinworm eggs

To each anal swab, two drops of xylene were added between the slide and the tape and spread over the entire length of the slide to dissolve the mucilage in the sample (Garcia, 2009). Each slide was then carefully examined by at least two medical technologist, under a light microscope at 10x and 40x for the characteristic of pinworm eggs. Data analysis For descriptive analysis, rate (percentage) was used to describe the characteristics of the studied subject, including the prevalence of E. vermicularis. A Chi-squares test (χ2) was used to test the associations between the variables. All variables that were significantly associated with the prevalence of E. vermicularis in the univariate model were included in a logistic regression analysis to identify the risk factors for enterobiasis. For each statistically significant factor, an Odds Ratio (OR) and 95 % confidence interval (CI) were computed by the univariate and multivariate logistic regression analyses. The level of significance was set as p < 0.05. All data were analyzed by using the SPSS software program for Windows version 20 (SPSS, Chicago, IL, USA).

Results
Demographic and socioeconomic profile

In April and May 2012, a total of 164 children between 1 and 6 years old were recruited for the survey. Of these recruited, 136 complied with the given instructions and returned the swabs and completed questionnaire (rate of compliance 82.9 %). Among this cohort, 56 children were from nurseries and the remaining (80) were from kindergartens. Median age of the children was 5 years [interquartile range (IQR) 3 – 6], with 45.6 % boys and 55.4 % girls. General characteristics of the children, including their demographic and socioeconomic profiles are presented in Table 1.

General characteristics of preschool children that participated in this study

CharacteristicsPreschool children
n(%)
Age groups (years)
1 – 456(41.2)
5 – 680(58.8)
Gender
Boy62(45.6)
Girl74(54.4)
Socioeconomic status
Father’s education (>6 years)136(100.0)
Mother’s education (>6 years)134(98.5)
High monthly household income (>RM900)136(100.0)
Working mothers112(82.4)
Working fathers136(100.0)
Large family members (>4)25(18.4)

n = Number examined

RM = Malaysian Ringgit (US$100 = RM359.92) (1st May 2015).

Prevalence and distribution of Enterobius vermicularis infection

The prevalence and distribution of enterobiasis are shown in Table 2. The overall egg positive of E. vermicularis was 12.5 % (17/136). The prevalence of this infection was not statistically significant between boys and girls. However, E. vermicilaris infection was significantly higher among older children, aged 5 – 6 years (OR = 3.75; 95 % CI = 1.02, 13.73; p = 0.035).

Prevalence of Enterobius vermicularis among preschool children according to age groups and gender in the present study

No. examinedNo. infectedPrevalence (%)
Age groups (years)
1–45635.4
5–6801417.5
Gender
Boy621016.1
Girl747 95
Total1361712.5
Risk factors for enterobiasis

Multiple logistic regression analysis further confirmed that being aged ≥5 years (OR = 3.45; 95 % CI = 1.08, 13.44; p = 0.048), finger sucking (OR = 3.41; 95 % CI = 1.08, 10.75; p = 0.035), being a member of a large family (OR = 3.16; 95 % CI = 1.03, 9.62; p = 0.043) and pre-medication of anthelmintics (OR = 3.43; 95 % CI = 1.17, 10.12 ; p = 0.025) as the real risk factors for enterobiasis in the population studied (Table 3).

Multivariate analysis of risk factors associated with pinworm infection among preschool children

VariablesOR95% CIp-value
Age groups3.451.08, 13.440.048
Finger sucking3.411.08, 10.750.036
Large family members3.161.03, 9.620.043
Pre-medication of anthelmintics3.431.17, 10.120.025

Significant association (p < 0.05)

Discussion

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.

Multivariate analysis of risk factors associated with pinworm infection among preschool children

VariablesOR95% CIp-value
Age groups3.451.08, 13.440.048
Finger sucking3.411.08, 10.750.036
Large family members3.161.03, 9.620.043
Pre-medication of anthelmintics3.431.17, 10.120.025

General characteristics of preschool children that participated in this study

CharacteristicsPreschool children
n(%)
Age groups (years)
1 – 456(41.2)
5 – 680(58.8)
Gender
Boy62(45.6)
Girl74(54.4)
Socioeconomic status
Father’s education (>6 years)136(100.0)
Mother’s education (>6 years)134(98.5)
High monthly household income (>RM900)136(100.0)
Working mothers112(82.4)
Working fathers136(100.0)
Large family members (>4)25(18.4)

Prevalence of Enterobius vermicularis among preschool children according to age groups and gender in the present study

No. examinedNo. infectedPrevalence (%)
Age groups (years)
1–45635.4
5–6801417.5
Gender
Boy621016.1
Girl747 95
Total1361712.5

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