Enterobiasis is a human intestinal parasitic disease caused by human pinworm, Enterobius vermicularis. Despite being the most prevalent nematode infection in Europe and North America, predominantly among in school aged children, the data concerning infection rate and knowledge of genetic variability of pinworms are incomplete. The aim of the study was the estimation of prevalence and molecular typing of Enterobius vermicularis among healthy children in north-eastern Poland. In 2013 – 2015, 296 individuals (aged 2 – 18 years) from 12 kindergartens, schools and orphanages were examined by the adhesive cellophane tape method. Data on socio-demographic status were collected using a questionnaire. Molecular analysis was performed using the DNA of adult female pinworms and primers targeting the region of cytochrome oxidase I gene. The overall prevalence of enterobiasis was 10.1 %. Enterobius vermicularis infection rates were 3.9 % in children living in families and 32.8 % among the orphans (OR=0.08; 95 % CI: 0.04 – 0.19; p<0.001). There were no associations between distribution of enterobiasis and gender, pets possession and the season of examination. In 43.3 % of the infected children enterobiasis was asymptomatic. Based on a molecular marker three different haplotypes of pinworm were identified. All sequences clustered within type B, together with human E. vermicularis isolates from Denmark, Germany, Greece, and Japan. This paper provides complementary data on the occurrence and intraspecific variability of E. vermicularis in human population in Europe.
If the inline PDF is not rendering correctly, you can download the PDF file here.
Alum, A., Rubino, J.R., Ijaz, M.K. (2010): The global war against intestinal parasites-should we use a holistic approach? Int. J. Infect. Dis. 14: e732 – e738. DOI: 10.1016/j.ijid.2009.11.036
Arca, M.J., Gates, R.L., Groner, J.I., Hammond, S., Caniano, D. (2004): Clinical manifestations of appendiceal pinworms in children: an institutional experience and a review of the literature. Pediatr. Surg. Int. 20: 372 – 375. DOI: 10.1007/s00383-004-1151-5
Artan, M.O., Baykan, Z., Artan, C. (2008): Enterobiasis among preschool children: A study from Kayseri, Turkey. Jpn. J. Infect. Dis. 61: 482 – 483
Bitkowska, E., Wnukowska, N., Wojtyniak, B., Dzbeński, T.H. (2004): The occurrence of intestinal parasites among children attending first classes of the elementary schools in poland in the school year 2002/2003. Przegl. Epidemiol. 58: 295 – 302 (In Polish)
Bøås, H., Tapia, G., Sødahl, J., Rasmussen, T., Rønningen, K. (2012): Enterobius vermicularis and risk factors in healthy Norwegian children. Pediatr. Infect. Dis. J. 31: 927 – 930. DOI: 10.1097/INF.0b013e318258cdb5
Burkhart, C.N., Burkhart, C.G. (2005): Assessment of frequency, transmission, and genitourinary complications of enterobiasis (pinworms). Int. J. Dermatol. 44: 837 – 840. DOI: 10.1111/j.1365-4632.2004.02332.x.
Cazorla, D., Acosta, M., Garcia, E., Garvett, M., Ruiz, A. (2006): Enterobius vermicularis infection in preschool and schoolchildren of six rural communities from a semiarid region of (Venezuela): a clinical and epidemiological study. Helminthologia 43: 81 – 85. DOI: 10.2478/s11687-006-0016-y
Crotti, D., D’Annibale, M.L. (2006): Enterobiosis during 2002-2003 in Perugia Province: Beyond diagnostics. Infez. Med. 14: 92 – 98
Çulha, G., Duran, N. (2006): The relationship between Enterobius vermicularis infection and nocturnal enuresis. Eur. J. Gen. Med.3: 16 – 20
Değerli, S., Malatyali, E., Ozçelik, S., Celiksöz, A. (2009): Enterobiosis in Sivas, Turkey from past to present, effects on primary school children and potential risk factors. Turkiye Parazitol. Derg. 33: 95 – 100
Ferrero, M.R., Röser, D., Nielsen, H.V., Olsen, A., Nejsum, P. (2013): Genetic variation in mitochondrial DNA among Enterobius vermicularis in Denmark. Parasitology, 140: 109 – 114. DOI: 10.1017/S0031182012001308
Gale E. (2002): A missing link in the hygiene hypothesis? Diabetologia, 45: 588 – 594. DOI: 10.1007/s00125-002-0801-1
Garcia, L.S. (2007): Examination of other specimens from the intestinal tract and the urogenital system. In: Diagnostic Medical Parasitology. 5th Edition. ASM Press, Washington, D.C, pp. 850-858
Gauert, B. (1998): Comparative study of the incidence and dissemination of intestinal parasites in child day care centers of the district capital Schwerin. Gesundheitswesen, 60: 301 – 306
Herrström, P., Henricson, K. Å., Råberg, Å., Karlsson, A., Högstedt, B. (2001): Allergic disease and the infestation of Enterobius vermicularis in Swedish children 4-10 years of age. J. Investig. Allergol. Clin.Immunol. 11: 157 – 160
Iñiguez, A.M., Reinhard, K., Carvalho Gonçalves, M.L., Ferreira, L.F., Araújo, A., Paulo Vicente, A.C. (2006): SL1 RNA gene recovery from Enterobius vermicularis ancient DNA in pre-Columbian human coprolites. Int. J. Parasitol. 36: 1419 – 1425. DOI: 10.1016/j.ijpara.2006.07.005
Kang, I.S., Kim, D.H., An, H.G., Son, H.M., Cho, M.K., Park, M.K., Kang, S.A., Kim, B.Y., Yu, H.S. (2012): Impact of health education on the prevalence of enterobiasis in Korean preschool students. Acta Trop. 122: 59 – 63. DOI: 10.1016/j.actatropica.2011.11.017
Kang, S., Sultana, T., Eom, K.S., Park, Y.C., Soonthornpong, N., Nadler, S.A., Park, J. K. (2009): The mitochondrial genome sequence of Enterobius vermicularis (Nematoda: Oxyurida) - An idiosyncratic gene order and phylogenetic information for chromadorean nematodes. Gene, 429(1 – 2): 87 – 97. DOI: 10.1016/j.gene.2008.09.011.
Kang, S., Jeon, H.K., Eom, K.S., Park, J.K. (2006): Egg positive rate of Enterobius vermicularis among preschool children in Cheongju, Chungcheongbuk-do, Korea. Korean J. Parasitol. 44: 247 – 249. DOI: 10.3347/kjp.2006.44.3.247
Kim, D.H., Son, H.M., Kim, J.Y., Cho, M.K., Park, M.K., Kang, S.Y., Kim, B.Y., Yu, H.S. (2010): Parents’ knowledge about enterobiasis might be one of the most important risk factors for enterobiasis in children. Korean J. Parasitol. 48: 121 – 126. DOI: 10.3347/kjp.2010.48.2.121
Kim, D.H., Son, H.M., Lee, S.H., Park, M.K., Kang, S.A., Park, S.K., Choi, J.H., Park, J.H., Yu, H.S. (2015): Negligible egg positive rate of Enterobius vermicularis and no detection of head lice among orphanage children in Busan and Ulsan, Korea (2014). Korean J. Parasitol. 53(4): 497-499. DOI: 10.3347/kjp.2015.53.4.497
Kubiak, K., Wrońska, M., Dzika, E., Dziedziech, M., Poźniak, H., Leokajtis, M. Dzisko, J. (2015): The prevalence of intestinal parasites in children in preschools and orphanages in the Warmia-Masuria province (North-Eastern Poland). Przegl. Epidemiol. 69: 483 – 488, 601 – 604
Li, H.M., Zhou, C.H., Li, Z.S., Deng, Z.H., Ruan, C.W., Zhang, Q.M., Zhu, T.J., Xu, L.Q., Chen, Y.D. (2015): Risk factors for Enterobius vermicularis infection in children in Gaozhou, Guangdong, China. Infect. Dis. Poverty 4: 28. DOI: 10.1186/s40249-015-0058-9
Lymbery, A.J., Thompson, R.C.A. (2012): The molecular epidemiology of parasite infections: tools and applications. Mol. Biochem. Parasitol. 181: 102 – 116. DOI: 10.1016/j.molbiopara.2011.10.006
Nakano, T., Okamoto, M., Ikeda, Y., Hasegawa, H. (2006): Mitochondrial cytochrome c oxidase subunit 1 gene and nuclear rDNA regions of Enterobius vermicularis parasitic in captive chimpanzees with special reference to its relationship with pinworms in humans. Parasitol. Res. 100: 51 – 57. DOI: 10.1007/s00436-006-0238-4
Otu-Bassey, I.B., Useh, M.F., Alaribe, A.A. (2011): The post-treatment effects of enterobiasis on the occurrence of enuresis among children in Calabar, Nigeria. Asian Pac. J. Trop. Med. 4(4): 315-319. DOI: 10.1016/S1995-7645(11)60093-X
Panidis, S., Paramythiotis, D., Panagiotou, D., Batsis, G., Salonikidis, S., Kaloutsi, V., Michalopoulos, A. (2011): Acute appendicitis secondary to Enterobius vermicularis infection in a middle-aged man: a case report. J. Med. Case Rep. 5: 559. DOI: 10.1186/1752-1947-5-559
Patsantara, G.G., Piperaki, E.T., Tzoumaka-Bakoula, C., Kanariou, M.G. (2015): Immune responses in children infected with the pinworm Enterobius vermicularis in central Greece. J. Helminthol. 4: 1 – 5. DOI: 10.1017/S0022149X15000334
Pezzani, B.C., Minvielle, M.C., de Luca, M.M., Córdoba, M.A., Apezteguía, M.C., Basualdo, J.A. (2004): Enterobius vermicularis infection among population of General Mansilla, Argentina. World J. Gastroenterol. 10: 2535 – 2539
Piperaki, E.T., Spanakos, G., Patsantara, G., Vassalou, E., Vakalis, N., Tsakris, A. (2011): Characterization of Enterobius vermicularis in a human population, employing a molecular-based method from adhesive tape samples. Mol. Cell Probes 25: 121 – 125. DOI: 10.1016/j.mcp.2011.03.005
Ramezani, M.A., Dehghani, M.R. (2007): Relationship between Enterobius vermicularis and the incidence of acute appendicitis. Southeast Asian. J. Trop. Med. Public Health 38(1): 20-23
Remm, M. (2006): Distribution of enterobiasis among nursery school children in SE Estonia and of other helminthiases in Estonia. Parasitol. Res. 99: 729 – 736. DOI: 10.1007/s00436-006-0220-1
Remm, M.Remm, K. (2008): Case-based estimation of the risk of enterobiasis. Artif. Intell. Med. 43: 167 – 177. DOI: 10.1016/j.artmed.2008.04.002
Song, H.J., Cho, C.H., Kim, J.S., Choi, M.H., Hong, S.T. (2003): Prevalence and risk factors for enterobiasis among preschool children in a metropolitan city in Korea. Parasitol. Res. 91: 46 – 50. DOI: 10.1007/s00436-003-0836-3
St Georgiev, V. (2001): Chemotherapy of enterobiasis (oxyuriasis). Expert Opin. Pharmacother. 2: 267 – 275. DOI: 10.1517/146565188.8.131.527
Stepek, G., Buttle, D.J., Duce, I.R., Behnke, J.M. (2006): Human gastrointestinal nematode infections: Are new control methods required? Int. J. Exp. Pathol. 87: 325 – 341. DOI: 10.1111/j.1365-2613.2006.00495.x
Zahariou, A., Karamouti, M., Papaioannou, P. (2007): Enterobius vermicularis in the male urinary tract: a case report. J. Med. Case Rep. 1: 137. DOI: 10.1186/1752-1947-1-137
Zelck, U.E., Bialek, R., Weiss, M. (2011): Molecular phylogenetic analysis of Enterobius vermicularis and development of an 18S ribosomal DNA-targeted diagnostic PCR. J. Clin. Microbiol. 49:1602 – 1604. DOI: 10.1128/JCM.02454-10
HELMINTHOLOGIA is a scientific journal of the Slovak Academy of Sciences published quarterly in English by Institute of Parasitology SAS, Slovak Republic. The journal is a medium for publication of original previously unpublished scientific papers from different fields of helminthology. The role of the journal is to enrich the theoretical basis of helminthology and to contribute to the advancement in human and veterinary medicine and agronomy.