Prevalence of Enterobiasis Among the Kindergarten Children of Sabzevar, Northeast of Iran

Background: Enterobiasis is a common parasitic disease at all age groups, especially children. It results in perianal itching, insomnia, abdominal pain, diarrhea, and rarely appendicitis and fallopian tube inflammation in the affected patients. The prevalence of enterobiasis varies in different parts of Iran. However, the status of the enterobiasis prevalence among Sabzevar children remains unknown. Hence, this study aimed to investigate the prevalence of enterobiasis among the kindergarten children of Sabzevar, Razavi Khorasan province, the northeast of Iran. Methods: In this cross-sectional analytical-descriptive study, sampling was carried out on children aged below 7 years using the Scotch-tape technique in the kindergartens of Sabzevar in 2019. The samples were then examined by a light microscope. Finally, the data were recorded in a questionnaire and analyzed using SPSS software and Fisher exact test. Results: Based on the results, 6 (3.49%) out of 172 collected samples were found to be infected with enterobiasis. There was no significant association between gender and infection. Eventually, no significant relationship was found between the geographical living area and enterobiasis. Conclusions: These findings indicated that the overall prevalence of enterobiasis among Sabzevar kindergarten children was lower than that of many parts of Iran. However, educational programs for parents and kindergarten staff regarding enterobiasis infection and the transmission routes should be conducted to reduce the infection rate.

Further, the prevalence of enterobiasis differs in different parts of Iran. For instance, its prevalence is 22.2% in Babol (11) and 7.1% in Amol (12) in the northern parts. This value is 2.1% in Shahroud in the central parts (13). In the southern and western parts, the prevalence is 24.1% and 14.7% in Khash (14) and Kermanshah (15), respectively. However, the status of enterobiasis prevalence among Sabzevar children remains unknown. Accordingly, this study sought to evaluate the prevalence of enterobiasis among the kindergarten children of Sabzevar, Razavi Khorasan province, the northeast of Iran.

Sampling and Parasitological Examination
In this cross-sectional analytical-descriptive study, 172 kindergarten children (3-7 years old) were randomly examined for enterobiasis infection using the Scotch-tape technique in June 2019. Both male and female children from the northern and southern parts of the city were included in the study. Their parents were instructed and asked to collect a specimen from the perianal surface of the children before defecation in the morning using a piece of clear adhesive tape. The samples were then received on the next day. Ultimately, the samples were transferred to the parasitology laboratory at Sabzevar University of Medical Sciences and examined by an expert parasitologist under a light microscope using ×100 and ×400 magnification. Furthermore, demographic variables (i.e., gender and the living area) were collected using a researcher-designed questionnaire.

Statistical Analysis
The data were analyzed using SPSS software, version 22. Eventually, Fisher exact test was used to determine the possible association between gender, geographical living area, and enterobiasis, and a P value less than 0.05 was considered statistically significant.

Results
Out of 172 samples, 6 (3.49%) cases were positive for the E. vermicularis egg. In addition, 2 (1.16%) out of 6 samples were detected in girls and the remaining 4 cases (2.3%) belonged to boys. Further, 72 and 100 samples were collected from the northern and southern parts of the city, respectively. Furthermore, 2 (2.8%) and 4 (2.3%) samples out of the collected samples from the northern and southern areas were positive for enterobiasis, respectively. Although the infection rate was slightly higher in boys (4.25%) compared to girls (2.6%), no significant association was found between gender and enterobiasis. In addition, there was no significant relationship between the geographical living area and the infection (P > 0.05), the details of which are presented in Table 1.

Discussion
The aim of this study was to investigate the prevalence of E. vermicularis infection among the kindergarten children of Sabzevar, Iran. According to the results, the overall prevalence of enterobiasis among the studied children was 3.49%. This infection rate was considerably lower than most of those reported in other parts of the   (14), and 14.7% in Kermanshah (15). However, the prevalence of enterobiasis was higher in Sabzevar compared to some parts of the country, including 2.38 % in Isfahan (8) and 0.028% in Karaj (16). The results of our study indicated that enterobiasis was less prevalent in Sabzevar than those reported in other parts of the world, including 22.4%, 6.85%, 10.5%, 17.67%, 10.1%, and 34.05% in the Marshall Islands (7), Chongqing city of China (9), Gimhae-si of Korea (10), Sidi-bel-Abbes of Algeria (17), north-eastern Poland (18), and district Mardan of Pakistan (19), respectively. These contradictions in infection rates may be due to differences in culture, climate, lifestyle, and especially personal and collective hygiene in different parts of the world. E. vermicularis eggs are sensitive to high temperatures and dry weather, and hence, they cannot survive outside the host's body for a long time. On the other hand, a cool and humid weather favor conditions for the eggs. Sabzevar has a high temperature and dry climate in the summer. Thus, the lower rate of enterobiasis in Sabzevar may be at least partly due to these factors when compared with the northern cities of Iran (e.g., Babol and Amol) and other parts of the world which have a temperate and humid weather in this season. Moreover, the samples were collected once by the children's parents. To increase the chance of enterobiasis diagnosis, samples should be collected three times by the researcher his/herself. However, due to the poor collaboration of children's parents, we could not collect the samples more than once. Therefore, the findings of the present study may underestimate enterobiasis prevalence in Sabzevar. We also found that the infection rate in boys was slightly higher compared to girls. However, there was no significant association between gender and enterobiasis (P > 0.05), which is in line with the findings of previous studies reporting no significant difference in enterobiasis prevalence by gender (7,12). In contrast, Wu et al in Chongqing, China reported that enterobiasis was significantly more prevalent in girls compared to boys (9). In general, it seems that there is no explicit association between gender and enterobiasis prevalence.
Based on the finding of our study, no significant relationship was observed between the geographical living area and enterobiasis, which is in accordance with the results of Motevalli Haghi et al showing no significant relationship between parasitic infection and the geographical area of the studied children (20). However, several studies reported differences in enterobiasis prevalence regarding the geographical living area (10,18). Generally, enterobiasis is more prevalent in rural areas compared with the urban area due to poor hygiene and low socio-economic status.

Conclusions
Overall, although the overall prevalence of enterobiasis among Sabzevar kindergarten children was lower than that of many parts of Iran, the educational programs for parents and kindergarten staff regarding enterobiasis infection and transmission routes should be conducted to reduce the infection rate.