Prevalence of Enterobius vermicularis among preschool children in 2003 and 2013 in Xinxiang city, Henan province, Central China

The present study was performed to assess the prevalence of Enterobius vermicularis infection among preschool children in Xinxiang city, Henan province, China and the changes in the egg positive rate for E. vermicularis over a 10 year period. A total of 510 preschool children in 17 kindergartens were examined using the cellophane-tape perianal swab method in 2003, while 1734 preschool children in 10 kindergartens were examined in 2013 using the same method. The overall egg positive rate for E. vermicularis was 12.75% (65 out of 510) in 2003 and 5.13% (89 out of 1734) in 2013; the former was significantly higher than the latter (p < 0.05). In both 2003 and 2013, the egg positive rate for 5 to 6-year-old children was significantly higher than that of 2 to 4-year-old children (p < 0.05). However, positive rates were not significantly dependent on gender or area. Among selected personal hygiene factors, no hand washing before eating, sucking fingers or toys, and scratching around the anus were all associated with enterobiasis. The present study confirmed that the prevalence of E. vermicularis infection among preschool children decreased significantly over the 10 year period in Xinxiang city, but infection was still prevalent. Improving sanitation and personal hygiene practices, especially hand washing, could help prevent the transmission of E. vermicularis.


Introduction
Enterobiasis is a nematode infection caused by the pinworm, Enterobius vermicularis [11]. The principal mode of transmission of E. vermicularis is direct contact between infected and uninfected persons [16]. For this reason, it is usually endemic in overcrowded conditions, such as kindergartens and primary schools, due to easy transmission from infected to uninfected children [12].
Enterobiasis is asymptomatic in most adults who have low worm burdens. However, in children, particularly those with high worm burdens, neurological symptoms including nervousness, restlessness, irritability, and distraction may occur, and these may influence child growth [13,14,18].
E. vermicularis infection is prevalent throughout the world, including in developed countries [4,8,13,14,18], and it is estimated that 4-28% of children are infected globally [1]. E. vermicularis infection is also widespread among preschool children in the People's Republic of China (China). According to the 2011 national parasitic survey, the average prevalence of E. vermicularis infection in children reached 17.8% in China, with the highest prevalence rates in Hainan (51.1%), Guangxi (26.7%), and Guangdong (26.7%) [2]. In 2011, the overall prevalence of E. vermicularis infection reached 54.86% in Gaozhou city, Guangdong province, southern China [12].
Currently, little information is available regarding the prevalence and possible risk factors of enterobiasis among kindergarten children in the central provinces of China. Therefore, in this study, we evaluated the prevalence of E. vermicularis among kindergarten children in Xinxiang city, Henan province, a province of central China, and performed a comparative analysis of the state of E. vermicularis prevalence in children in the years 2003 and 2013.

Ethics statement
The study was reviewed and approved by the Ethics Review Committee of the Xinxiang Medical University (Reference Nos. 2003008 and 2013012). All examinations were carried out with permission from the preschool teachers and the children's parents.

Subject recruitment
The study was conducted in Xinxiang city, Henan province, central China. A total of 510 preschool children (282 boys and 228 girls) in 17 kindergartens were recruited for the survey in 2003, while 1734 preschool children (918 boys and 816 girls) in 10 kindergartens were recruited in 2013. Seven of the selected 17 kindergartens in 2003 merged with the 10 remaining kindergartens before the year 2013. We therefore recruited preschool children from the 10 remaining kindergartens in 2013. After 10 years of development, the scale of enrollment of the 10 kindergartens expanded, along with the increase in the number of classrooms and teachers in these schools. The average number of teachers in each class increased from two to three. Conversely, the average number of students in each class decreased from 35 to 30. The infrastructures of kindergartens, such as toilets and playground equipment, are much cleaner and more spacious than 10 years ago.

Questionnaire survey
The questionnaire included questions on basic information regarding the children and their personal hygiene habits (see Table 2). Personal data included age, gender, and residential district. The children's personal hygiene habits section aimed to gather information on certain behaviors, including hand washing before eating, sucking fingers (including fingernail biting) or toys, and scratching around the anus.

Detection of E. vermicularis infection
Egg detection for E. vermicularis was performed using the cellophane-tape perianal swab method, as previously described [6], which was performed by parents between 07:30 and 09:30 in the morning, according to the instructions provided by the study researchers, and all samples were collected by the teachers at every kindergarten. Collected samples were then transported to the Department of Human Parasitology, Xinxiang Medical University, and examined under light microscope. The same detection procedure was performed on three consecutive days. If eggs were found, children were considered positive for E. vermicularis infection.

Statistical analysis
Statistical analysis was performed using SPSS 20 software for Windows (SPSS Inc, Chicago, Illinois, USA). Statistical analyses of E. vermicularis prevalence for different variables were performed by v 2 -test. The differences were considered statistically significant if p < 0.05.

Results
In 2003, a total of 65 (12.75%) of the 510 samples were positive for E. vermicularis eggs. After 10 years, the egg positive rate significantly decreased to 5.13% (89/1734) in 2013 (Table 1). Table 2 shows the personal hygiene practices and other factors that may potentially be associated with the egg positive rates of E. vermicularis. No significant differences in egg positive rates according to gender were observed in 2003 or 2013. The egg positive rate in rural areas was only slightly higher than that in urban areas in both 2003 and 2013. However, this difference was not significant (p > 0.05).
Among selected personal hygiene factors, hand washing before eating, sucking fingers or toys, and scratching around the anus, were all associated with enterobiasis. Children who wash their hands before eating had lower egg positive rates for E. vermicularis than those who did not (p < 0.05). Children with the habit of sucking fingers or toys were more commonly infected by E. vermicularis than those who did not have this habit; this result was significant in 2013 (p < 0.01) but not in 2003 (p > 0.05). Similar results were found in the children with the habit of scratching around the anus or not.

Discussion
Although enterobiasis is generally considered to be a nuisance rather than a serious disease, the level of morbidity is significant, particularly in children.
This study found that the overall prevalence of E. vermicularis infection in preschool children was 12. In the present study, the egg positive rate for E. vermicularis among 5 to 6-year-old children was also significantly higher than that among 2 to 4-year-old children in both 2003 and 2013. Five to 6-year-old children might have more frequent contact in kindergartens than children 2-4 years of age. The egg positive rate for E. vermicularis was also found to significantly increase with age, as previously reported [6,7]. With regard to gender, no significant statistical difference was observed between boys and girls, which was consistent with other reports [12,15,18].
According to previous reports regarding risk factors for E. vermicularis infection, inadequate personal hygiene increased the risk of enterobiasis among primary school children [9,11,17]. E. vermicularis can be transmitted from person to person by contaminated hands, especially in crowded conditions [3]. Children who did not mention that they should wash their hands with soap before eating had higher concentrations of E. vermicularis eggs on their hands (p < 0.05) than those who did [3]. In the present study, children who wash their hands before eating had lower egg positive rates for E. vermicularis than those who did not. These studies highlight the need to teach children to get into the recommended habit of washing hands at school and at home, under the supervision of teachers and parents, respectively, to prevent transmission of E. vermicularis.
Furthermore, in our study, children with the habit of sucking fingers or toys showed higher rates of E. vermicularis infection than those who did not have this habit. This was consistent with previous reports [5,9,10]. For younger children, guardians should pay close attention to cleaning toys and prohibit children from sucking fingers or toys. It is therefore necessary not only to carry out mass screening and regular whole group treatments for children, with correct medication methods, but also to develop pinworm eradication programs, such as health education programs on enterobiasis for parents, in order to control E. vermicularis infection in China.
In conclusion, the prevalence of E. vermicularis infection among preschool children decreased significantly over a period of 10 years in Xinxiang city, but E. vermicularis infection was still prevalent. Therefore, specific control measures are required to interrupt the transmission cycle of E. vermicularis. Larger scale studies are required to establish the extent of the infection in other parts of China.