Skip to main content Accessibility help

Genetic variation of Enterobius vermicularis among schoolchildren in Thailand

  • K. Tomanakan (a1) (a2), O. Sanpool (a1) (a2), P. Chamavit (a3), V. Lulitanond (a4), P.M. Intapan (a1) (a2) and W. Maleewong (a1) (a2)...


Enterobiasis, caused by the nematode Enterobius vermicularis, is a common health problem among schoolchildren in Thailand. We provide the first molecular identification of this nematode from Thai schoolchildren and document genetic variation among E. vermicularis eggs using sequence analyses of the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene and the nuclear ribosomal DNA second internal transcribed spacer (ITS2). A cross-sectional parasitological survey was conducted in schoolchildren (n = 491) in five regions of Thailand between May 2015 and December 2016. The diagnosis of Enterobius infection was made using the adhesive tape perianal swab technique. Enterobius eggs were recovered from 43 participants (8.75%). DNA was extracted from these eggs and the cox1 gene and partial ITS2 region amplified using the polymerase chain reaction (PCR). Nineteen amplified PCR products of the cox1 gene (441 bp) and 18 of the ITS2 region (623 bp) were subsequently sequenced. All sequences were identified as belonging to E. vermicularis based on database searches. Phylogenetic analysis and a median-joining network of available E. vermicularis cox1 sequences showed 66 haplotypes. We found haploclusters (types A and B) represented among the Thai sequences. Six haplotypes from Thailand fell into type A (of Nakano et al., 2006) (along with sequences from Japan and Korea) and five haplotypes into type B (with sequences from Japan, Iran, Czech Republic, Greece, Denmark and Sudan). The overall haplotype diversity (Hd) was 0.9888. Transmission of worms with type B haplotypes from primates to humans in Asia or from humans in Europe possibly occurs in Thailand.


Corresponding author

Author for correspondence: P.M. Intapan, E-mail:


Hide All
Beaver, PC, Jung, RC and Cupp, EW (1984) Examination of specimens for parasites. In Beaver, PC, Jung, RC and Cupp, EW (eds), Clinical Parasitology, 9th edn. Philadelphia: Lea & Febiger, pp. 733758.
Bethony, J et al. (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367, 15211532.
Blouin, MS (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527531.
Cerva, L, Schrottenbaum, M and Kliment, V (1991) Intestinal parasites: a study of human appendices. Folia Parasitologica (Praha) 38, 59.
Ferrero, MR et al. (2013) Genetic variation in mitochondrial DNA among Enterobius vermicularis in Denmark. Parasitology 140, 109114.
Hagh, VRH et al. (2014) Genetic classification and differentiation of Enterobius vermicularis based on mitochondrial cytochrome c oxidase (cox1) in northwest of Iran. Journal of Pure and Applied Microbiology 8, 39953999.
Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.
Hasegawa, H, Sato, H and Torii, H (2012) Redescription of Enterobius (Enterobius) macaci Yen, 1973 (Nematoda: Oxyuridae: Enterobiinae) based on material collected from wild Japanese macaque, Macaca fuscata (Primates: Cercopithecidae). Journal of Parasitology 98, 152915.
Iniguez, AM et al. (2006) SL1 RNA gene recovery from Enterobius vermicularis ancient DNA in pre-Columbian human coprolites. International Journal for Parasitology 36, 14191425.
Jongsuksantigul, P, Chaeychomsri, W and Techamontrikul, P (1992) Study on prevalence and intensity of intestinal helminthiasis and opisthorchiasis in Thailand. Journal of Tropical Medicine and Parasitology 15, 8095.
Kaewkes, S et al. (1983) Enterobiasis in young schoolchildren in Khon Kaen. Journal of Tropical Medicine and Parasitology 6, 1924.
Kang, S et al. (2009) The mitochondrial genome sequence of Enterobius vermicularis (Nematoda: Oxyurida) - an idiosyncratic gene order and phylogenetic information for chromadorean nematodes. Gene 429, 8797.
Kim, DH et al. (2013) Environmental factors related to enterobiasis in a southeast region of Korea. Korean Journal of Parasitology 51, 139142.
Kim, DH and Yu, HS (2014) Effect of a one-off educational session about enterobiasis on knowledge, preventative practices, and infection rates among schoolchildren in South Korea. PLoS ONE 9(11), e112149.
Kucik, CJ, Martin, GL and Sortor, BV (2004) Common intestinal parasites. American Family Physician 69, 11611168.
Kubiak, K, Dzika, E and Paukszto, Ł (2017) Enterobiasis epidemiology and molecular characterization of Enterobius vermicularis in healthy children in north-eastern Poland. Helminthologia 54, 284291.
Le, TH, Blair, D and McManus, DP (2000) Mitochondrial genomes of human helminths and their use as markers in population genetics and phylogeny. Acta Tropica 77, 243256.
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.
Li, HM et al. (2015) Risk factors for Enterobius vermicularis infection in children in Gaozhou, Guangdong, China. Infectious Diseases of Poverty 4, 28.
Nakano, T et al. (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. Parasitology Research 100, 5157.
Nei, M and Kumar, S (2000) Molecular Evolution and Phylogenetics. New York, NY: Oxford University Press.
Nithikathkul, C et al. (2001) The prevalence of Enterobius vermicularis among primary school students in Samutprakan Province, Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 32, 133137.
Pampiglione, S and Rivasi, F (2009) Enterobiasis in ectopic locations mimicking tumor-like lesions. International Journal of Microbiology 2009, 642481.
Park, JH et al. (2005) A survey of Enterobius vermicularis infection among children on western and southern coastal islands of the Republic of Korea. Korean Journal of Parasitology 43, 129134.
Piperaki, ET et al. (2011) Characterization of Enterobius vermicularis in a human population, employing a molecular-based method from adhesive tape samples. Molecular and Cellular Probes 25, 121125.
Polseela, P et al. (2004) Parasitic infection among primary schoolchildren in Meuang district, Phitsanulok province, Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 35, 120123.
Saksirisampant, W et al. (2006) Prevalence of intestinal parasitic infections among schoolchildren in the central region of Thailand. Journal of the Medical Association of Thailand 89, 19281933.
Serpytis, M and Seinin, D (2012) Fatal case of ectopic enterobiasis: Enterobius vermicularis in the kidneys. Scandinavian Journal of Urology and Nephrology 46, 7072.
Tamura, K et al. (2013) MEGA6 : molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 27252729.
Thompson, JD, Higgins, DG and Gibson, TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.
Zelck, UE, Bialek, R and Weiss, M (2011) Molecular phylogenetic analysis of Enterobius vermicularis and development of an 18S ribosomal DNA-targeted diagnostic PCR. Journal of Clinical Microbiology 49, 16021604.


Type Description Title
Supplementary materials

Tomanakan et al. supplementary material
Tomanakan et al. supplementary material 1

 Unknown (943 KB)
943 KB

Genetic variation of Enterobius vermicularis among schoolchildren in Thailand

  • K. Tomanakan (a1) (a2), O. Sanpool (a1) (a2), P. Chamavit (a3), V. Lulitanond (a4), P.M. Intapan (a1) (a2) and W. Maleewong (a1) (a2)...


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.