The main findings of our longitudinal localization-based school children’s pinworm cohort with prevalence and time-trend analysis are summarized as follows. The prevalence of pinworm infection showed a significant declining trend during the study reference period, both in males and females. Students residing in urban areas showed a significantly lower risk of enterobiasis. Interestingly, the trend of enterobiasis in urban and suburban areas decreased significantly from 2009 to 2018. However, there was no obvious trend of change in the rate of pinworm infection in rural areas. The occurrence of pinworm infection was higher in the younger age group in both males and females, but boys had a higher enterobiasis rate compared to girls. There was a negative correlation between BMI and pinworm infection throughout the study.
This study revealed that the overall pinworm infection among school-age children gradually decreased in Hualien from 2009 to 2018. Although the preventive strategy for pinworm infection had some variations between each local government in Taiwan after 2001, similar reducing trends of pinworm infection were observed in other areas of Taiwan . However, a high prevalence of enterobiasis was still observed without a decreasing trend in the rural area of Hualien. In line with previous study in Germany, locally clustered enterobiasis is still a vital issue in some resource-rich countries .
The non-obvious decline in the trend of pinworm infection rate in the suburban and rural areas of Hualien was an important finding of this study. There is no clear consensus on the association between urbanization and the prevalence of pinworm infection. In a study conducted in the Republic of Marshall Island, the prevalence of pinworm infection in urban areas was found to be higher than that in rural areas . Another study in Taiwan found that schoolchildren in rural areas are less likely to have pinworm infection than those residing in urban areas . On the other hand, studies conducted in China found that children in rural areas were at a higher risk of pinworm infection than those residing in urban areas [12, 18, 19]. The reasons for the non-significant decrease in the trend of pinworm infection in remote areas of Hualien are likely to be multifactorial. Many studies have highlighted the association between socioeconomic status and pinworm infection [1, 3]. In the present study, the urbanization category was based on population density, educational level, percentage of the elderly population, industrialization, percentage of the agricultural population, and medical resources. Hualien, the largest county in Taiwan by area, includes 13 districts with considerable differences in urbanization levels. The rural areas in our study, including Xiulin, Wanrong, and Zhuoxi, have a relatively low socioeconomic status, such as low educational level, low industrialization, and low family income. Furthermore, in Taiwan, there are significant urban-rural disparities with respect to availability of health care and medical resources are located mainly in the urban areas of Hualien. The above socioeconomic factors may be responsible for the persistently high prevalence of pinworm infection among school-age children in the remote areas of Hualien.
Another reason for the persistent high prevalence of enterobiasis in the rural areas of Hualien was the proportion of young children in the population of the districts. Pinworm infection has been shown to be more common in young children aged 4 to 11 years [5, 20, 21]. Children under the age of two or those over the age of 14 and adults are less affected by pinworm infection [5, 22]. Young children tend to play on the floor, and show frequent nail biting or finger sucking behaviors and poor hand-washing compliance before meals; the above factors are known risk factors for pinworm infection [1, 4, 5, 8, 20]. According to the demographic data from the Hualien Civil Affairs Department, the three districts with the lowest population density were compatible with the rural areas in our study . Despite the low population density, a higher percentage of children aged < 14 years in rural areas than in urban/suburban areas was a characteristic of Hualien according to the demographic data from the Hualien Civil Affairs Department , which may explain the high rate of enterobiasis in remote areas of Hualien.
Additionally, a previous study also revealed that small-size schools in remote areas is a potential risk factor for a higher rate of enterobiasis . In a large-scale survey of schoolchildren in Taiwan, smaller schools (< 100 children) showed higher positivity rates of pinworm infection than larger schools (> 100 children). The authors concluded that children of different ages frequently use the same classroom due to the limited educational resources in these regions, which facilitates the transmission of pinworm due to the crowded environment . According to the data of the Taiwan Ministry of Education, most schools in the rural areas of Hualien areas are small schools, which corresponded to the areas with the highest prevalence of pinworm infection. This finding was consistent with the findings of previous large-scale surveys . In brief, the multiple reasons may explain the persistently high prevalence of pinworm infection in rural areas, including high percentage of young children and small schools.
Appropriate policy intervention for prevention of pinworm infection is important. Screening and eradication with mebendazole are the main policy interventions for pinworm infection in Taiwan, which led to a prominent declining trend of pinworm infection in recent decades. After 2001, the work of pinworm prevention was carried out by the individual county/city governments. The policy for pinworm infection was individualized by the local government according to the local prevalence rates. The main difference in the policy for pinworm infection in Taiwan is with respect to the groups targeted for screening. According to the 2007 report of the Taiwan Centers for Disease Control, some counties, such as Kaohsiung City, screened all elementary school students, and some counties, such as Taipei, screened students in grades 1 and 4 . Due to the relatively low prevalence of pinworm infections in Taiwan, the screening groups among Taiwanese schoolchildren in recent years were mainly those in grades 1 and 4. However, this policy does not seem to be adequate to decrease the prevalence of pinworm infection in remote areas of Hualien. Therefore, it might be necessary to adjust the screening group policy in the hot pinworm zone.
In this study, we identified other risk factors for enterobiasis in children, including sex, age, and BMI. Sex-based differences in pinworm infection have been widely reported, and in our study, boys showed a significantly higher infection rate than girls. However, a previous study in Taiwan found no significant sex-based difference in pinworm infection . Most other studies have revealed higher infection rates in males [2, 4, 7, 14, 26]. The exception was a study conducted in Thailand, which found a higher risk of pinworm infection in girls compared to boys . This phenomenon may be attributable to the fact that the boys have comparatively poor personal hygiene and indulge in more intimate contact activities with other children [4, 10, 26].
Our study also found a higher prevalence of enterobiasis in the younger age group in both males and females. This finding was consistent with previous studies that showed a higher risk of pinworm infection in preschool children compared to that in school-age children, toddlers, and infants [3, 4, 8]. Although our study dataset did not include data on pinworm infection in toddlers and preschool children, older school-age children in our study had a lower pinworm infection rate than younger subjects. This phenomenon may be associated with improved personal hygiene in older children . Besides, the children in grade 4 with no pinworm infection may have a history of previous eradication of pinworm when they were in grade 1. However, there was no related data in this study to prove this hypothesis. Another potential reason may be related to the current screening method for pinworm infection in Taiwan, which entails the use of adhesive cellophane perianal swab for two consecutive days. Usually, this procedure is assisted by parents. Older children may be embarrassed to ask their parents for help and are likely to complete the procedure themselves. Therefore, the poor quality of perianal swabs may have introduced an element of bias in the detection of pinworm infection.
The negative correlation between BMI and pinworm infection was another interesting finding of this study. Underweight subjects in this study showed a trend for higher OR for enterobiasis infection compared to children in the normal BMI group, but without statistical significance. Malnutrition is associated with intestinal parasitic infection. Furthermore, childhood developmental disorder and growth showed an association with pinworm infection [5, 27, 28]. The above-mentioned reasons may explain the higher risk of enterobiasis among underweight students in our study. Instead, students in the overweight/obese BMI group had a significantly lower OR for enterobiasis compared to subjects with normal BMI. Similar findings have been reported in another study . The potential reasons for the causality or association between high BMI and low pinworm infection rate are still uncertain. A previous study revealed that children with high BMI are more likely to spend more time on watching television and show decreased physical activity , and the lifestyle of children with high BMI may decrease the risk of contact with people or the environment contaminated by pinworms. However, further study is required to clarify this hypothesis about the association between high BMI and low pinworm infection rate.
Some limitations of our study should be acknowledged. First, enterobiasis is well-known to be a multifactorial disease. Data pertaining to many other socio-demographic risk factors, such as the parental education levels, family income and living conditions, number of siblings, personal hygiene, long fingernails, and habitual frequent sucking of fingers, were not collected, leading to potential confounding in the final analysis [4, 8, 31]. Second, the data in this study were collected from the annual health examination of students in grades 1 and 4. Therefore, there were no data of other students except grades 1 and 4, and this may have introduced an element of selection bias. However, the large dataset used for this analysis is a study strength. Further studies are required for in-depth characterization of the trend of prevalence of pinworm infection in children in Hualien.