Original Article

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

Background

Enterobiasis is considered as a common parasitic disease among children caused by Enterobius vermicularis, which is also called Oxyuriasis vermicularis or pinworm. Adult male and female pinworms are 2-5 and 8-13 mm long, respectively. They live in the human large intestine, and fertile female worms migrate out of the anus at nights to lay their eggs on the folds of the rectum (1). Due to the movement of the worm and the eggs laid around the anus, it can cause allergy in the anus which is occasionally highly severe and is usually experienced at nights. Itching in the anus, inflammation in the intestine, invasion to appendix, and neurological complications such as restlessness, anger, fatigue, insomnia, and nocturnal enuresis are reported in the affected individuals (1,2). In rare cases, infection with pinworm can cause intestinal problems and ectopic infections such as vaginitis and appendicitis (3,4).

The transmission of enterobiasis is facilitated by several factors such as poor hygiene and overcrowding in kindergartens, schools, and orphanages (5). The parasite can be directly transmitted via the anus-to-mouth rout or indirectly through infected objects such as toys, class desks, chairs, and the ground (6). Children are typically infected by various methods such as eating food contaminated with parasitic eggs, contaminated fingers, inhalation of the suspended eggs in the dust, and reverse migration of the larvae released from eggs around the anus into the colon (1).

The definitive diagnosis of enterobiasis relies on the finding of the egg or the parasite itself. Based on a fecal test, its diagnosis is less than 5%. Hence, the Scotch-tape test or Graham’s test is the best technique for diagnosing enterobiasis. This test is still the gold standard for enterobiasis diagnosis which can be simply done at home. In this method, using a glass tape or cellophane, a sample is taken from around the anus and then observed under a light microscope for E. vermicularis eggs. To enhance the chance of diagnosis, it is recommended to do sampling in the morning and before defecation or bathing (1).

The prevalence of enterobiasis is about 200 million people worldwide. Meanwhile, 30% of cases are children aged 5-10 years (7). Enterobiasis is prevalent in different parts of the world, especially countries with a temperate climate. In addition, its prevalence rate is about 30-50% in the United States and parts of Europe (5), 22.4% in the Marshall Islands (7,8), 6.85% in Chongqing of China (9), and 10.5% in the Gimhae-si of Korea (10).

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.

Methods

Study Area

Sabzevar (36°12′45″N 57°40′55″E) is a city in Razavi Khorasan province, the northeast of Iran (Figure 1). Its population is around 243,700 and has a cold semi-arid climate (The statistical center of Iran, https://www.amar.org.ir/english).

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Figure 1.

Geographical Location of the Studied Area, Sabzevar, Razavi Khorasan Province.

Figure 1.

Geographical Location of the Studied Area, Sabzevar, Razavi Khorasan Province.

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 country, including 22.2% in Babol (11), 7.1% in Amol (12), 24.1% in Khash (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.

Conflict of Interests

The authors declare that they have no conflict of interests.

Acknowledgments

We should convey our best attitudes to the Deputy of the Research and Technology of Sabzevar University of Medical Sciences and Sabzevar Welfare Organization for their help in conducting this project. This project was financially supported by the Deputy of the Research and Technology of Sabzevar University of Medical Sciences.

Ethical Approval

This work was reviewed and approved by the Ethics Committee of Sabzevar University of Medical Sciences (Ethical code: IR.MEDSAB.REC.1393.21). The children’s parents were also asked to sign an informed consent form in order to allow their children to take part in this study.

Authors’ Contributions

HE: Conceptualization, methodology, funding acquisition, and statistical analysis; RG: Data collection, methodology, and original draft preparation; MSM: Supervision, statistical analysis, and writing, reviewing, and editing the final manuscript. All authors read and approved the final manuscript.

Funding/Support

This project was financially supported by the Deputy of the Research and Technology of Sabzevar University of Medical Sciences.

References

1. Wendt S, Trawinski H, Schubert S, Rodloff AC, Mössner J, Lübbert C. The diagnosis and treatment of pinworm infection. Dtsch Arztebl Int 2019; 116(13):213-9. doi: 10.3238/arztebl.2019.0213 [Crossref] [ Google Scholar]
2. Kandi V, Vaish R, Palange P, Koka SS, Gurrapu P, Bhoomigari MR. Enterobius vermicularis: does it invade central nervous system?. Am J Infect Dis Microbiol 2019; 7(1):8-12. doi: 10.12691/ajidm-7-1-2 [Crossref] [ Google Scholar]
3. Mentessidou A, Theocharides C, Patoulias I, Panteli C. Enterobius vermicularis-associated pelvic inflammatory disease in a child. J Pediatr Adolesc Gynecol 2016; 29(2):e25-7. doi: 10.1016/j.jpag.2015.10.010 [Crossref] [ Google Scholar]
4. Habashi R, Lisi MP. Acute appendicitis and Enterobius vermicularis infestation. CMAJ 2019; 191(17):E477. doi: 10.1503/cmaj.181194 [Crossref] [ Google Scholar]
5. Burkhart CN, Burkhart CG. Assessment of frequency, transmission, and genitourinary complications of enterobiasis (pinworms). Int J Dermatol 2005; 44(10):837-40. doi: 10.1111/j.1365-4632.2004.02332.x [Crossref] [ Google Scholar]
6. Kim DH, Cho MK, Park MK, Kang SA, Kim BY, Park SK. Environmental factors related to enterobiasis in a southeast region of Korea. Korean J Parasitol 2013; 51(1):139-42. doi: 10.3347/kjp.2013.51.1.139 [Crossref] [ Google Scholar]
7. Fan CK, Chuang TW, Huang YC, Yin AW, Chou CM, Hsu YT. Enterobius vermicularis infection: prevalence and risk factors among preschool children in kindergarten in the capital area, Republic of the Marshall Islands. BMC Infect Dis 2019; 19(1):536. doi: 10.1186/s12879-019-4159-0 [Crossref] [ Google Scholar]
8. Abedi S, Eezadi S, Davari B. Prevalence of oxyuriasis in kindergartens of Isfahan, Iran. Hormozgan Med J 2004; 8(1):63-6. [ Google Scholar]
9. Wu CG, Luo XJ, Xie J, Jiang SG, Li SS, Xiao BZ. [Prevalence of Enterobius vermicularis infection of children and its influencing factors in Chongqing city]. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 2012; 24(6):703-6. [ Google Scholar]
10. Lee SE, Lee JH, Ju JW, Lee WJ, Cho SH. Prevalence of Enterobius vermicularis among preschool children in Gimhae-si, Gyeongsangnam-do, Korea. Korean J Parasitol 2011; 49(2):183-5. doi: 10.3347/kjp.2011.49.2.183 [Crossref] [ Google Scholar]
11. Norbakhsh Amiri SA, Rahimi MT, Mahdavi SA, Moosazadeh M, Ramzani O, Farrokhi Koshk A. Prevalence of Enterobius vermicularis infection among preschool children, Babol, North of Iran. J Parasit Dis 2016; 40(4):1558-62. doi: 10.1007/s12639-015-0727-4 [Crossref] [ Google Scholar]
12. Afrakhteh N, Marhaba Z, Mahdavi SA, Garoosian S, Mirnezhad R, Eshkevar Vakili M. Prevalence of Enterobius vermicularis amongst kindergartens and preschool children in Mazandaran Province, North of Iran. J Parasit Dis 2016; 40(4):1332-6. doi: 10.1007/s12639-015-0683-z [Crossref] [ Google Scholar]
13. Rahimi H, Dehghani M, Norouzi P, Fazli M. Frequncy of Giardia lamblia and Enterobius vermicularis infections in Shahroud kindergartens, 2013. J Ardabil Univ Med Sci 2015; 15(1):7-14. [ Google Scholar]
14. Ebrahimzadeh A, Saryazdipoor K, Gharaei A, Mohammadi S, Jamshidi A. Prevalence of Enterobius vermicularis infection among preschool children of Khash city kindergartens, Iran in 2012. J North Khorasan Univ Med Sci 2014; 6(3):477-81. doi: 10.29252/jnkums.6.3.477 [Crossref] [ Google Scholar]
15. Sha-Mohammadi Z, Ghahramani F, Mahboubi M, Jalilian F, Neiakane-Shahri M, Mohammadi M. Prevalence of Enterobius vermicularis (pinworm) in Kermanshah city nurseries, using Graham: 2014. J Biol Today’s World 2014; 3(1):24-7. [ Google Scholar]
16. Nasiri V, Esmailnia K, Karim G, Nasir M, Akhavan O. Intestinal parasitic infections among inhabitants of Karaj city, Tehran province, Iran in 2006-2008. Korean J Parasitol 2009; 47(3):265-8. doi: 10.3347/kjp.2009.47.3.265 [Crossref] [ Google Scholar]
17. Merad Y, Merbouh A, Benallal K, Belfodel S, Adjmi-Hamoudi H. Prevalence of enterobiasis among urban school children in Sidi-bel-Abbes, Algeria. Int J Innov Appl Stud 2018; 24(2):453-8. [ Google Scholar]
18. Kubiak K, Dzika E, Paukszto Ł. Enterobiasis epidemiology and molecular characterization of Enterobius vermicularis in healthy children in north-eastern Poland. Helminthologia 2017; 54(4):284-91. doi: 10.1515/helm-2017-0042 [Crossref] [ Google Scholar]
19. Niaz S, Abdullah Abdullah, Arif M, Zubair N, Khan S, Aurang Zeb M. Prevalence of Enterobius vermicularis in children of district Mardan, Pakistan. PSM Biol Res 2019; 4(2):58-62. [ Google Scholar]
20. Motevalli Haghi SM, Najm M, Fakhar M, Gholami S, Motevalli Haghi SF. Prevalence of Enterobius vermicularis infection among kindergartens in Mazandaran province, 2011. J Mazandaran Univ Med Sci 2013; 23(Suppl 1):241-7. [ Google Scholar]