Skip to main content
SpringerLink
Log in

Syphacia obvelata (Nematode, Oxyuridae) infecting laboratory mice Mus musculus (Rodentia, Muridae): phylogeny and host-parasite relationship

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Syphacia obvelata is a pinworm nematode parasite infecting man and laboratory animals in high abundance. This parasitological study was carried out during the period of March 2014–February 2015 to investigate the helminth parasites infecting the laboratory mice Mus musculus in the Animal House at Cairo University, Egypt. The prevalence of S. obvelata in M. musculus was 75.0 %. The extent of infection with S. obvelata is analyzed according to the sex of the host mice. It was shown that the prevalence of male infection was greater than female worms. Morphological characterization revealed that the present Oxyurid species possesses a rounded cephalic end with less developed lips, esophagus divided into cylindrical corpus, and globular bulb supported internally with valvular apparatus; three mamelons are located at the ventral surface with a single chitinized spicule and a gubernaculum provided with an accessory hook in males, and ovijector apparatus opens ventrally by the vulva surrounded by protruded lips in female worms. Body of the male was 0.623–1.130 (0.830 ± 0.11) mm long and 0.092–0.130 (0.110 ± 0.01) mm wide; the esophagus was 0.164–0.280 (0.210 ± 0.01) mm long; the nerve ring and excretory pore are located at 0.035–0.132 (0.073 ± 0.01) and 0.087–0.191 (0.145 ± 0.01) mm from the anterior end, respectively, while the female measured 2.930–4.650 (3.540 ± 0.1) mm long and 0.120–0.232 (0.156 ± 0.001) mm wide; the esophagus was 0.213–0.410 (0.342 ± 0.01) mm long; the nerve ring, excretory pore, and vulval opening are located at 0.026–0.157 (0.121 ± 0.01), 0.134–0.243 (0.195 ± 0.01), and 0.323–0.632 (0.546 ± 0.11) mm from the anterior end, respectively; eggs measured 0.120–0.139 (0.129 ± 0.001) mm long and 0.030–0.052 (0.045 ± 0.001) mm wide. It compared morphometrically with other Syphacia species described previously and showed little differences in measurements. Molecular characterization based on small subunit ribosomal DNA (rDNA) was done to confirm the obtained morphological and morphometric results. A preliminary genetic comparison between SSU rDNA of the present parasite and other species of Oxyuridae places it as a putative sister taxon to other S. obvelata.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figs. 1–10
Figs. 11–20
Figs. 21–28
Fig. 29

Similar content being viewed by others

References

  • Abdel-Gaber R, Fol M (2015) Aspicularis tetrapetra (Nematode, Heteroxynematidae) of laboratory mice Mus musculus (Rodentia, Muridae): a potential risk of zoonotic infection for researchers. Cien Tec Viti 30(8):125–136

    Google Scholar 

  • Adamson ML (1994) Evolutionary factors influencing the nature of parasite specificity. Parasitology 109:S85–S95

    Article  PubMed  Google Scholar 

  • Ambroise-Thomas P (1990) Molecular probes in the study and diagnosis of parasitic diseases. Ann Parasitol Hum Comp 65(I):83–88

    PubMed  Google Scholar 

  • Baird SJE, Ribas A, Macholan M, Albrecht T, Pialek J, Gouy de Bellocq J (2012) Where are the wormy mice? A re-examination of hybrid parasitism in the European house mouse hybrid zone. Evolution 66(9):2757–2772

    Article  PubMed  Google Scholar 

  • Baker D (1998) Naturel pathogens of laboratory mice, rats and rabbits and their effects on research. Clin Microbiol Rev 11:231–266

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bazzano T, Restel TI, Pinto RM, Gomes DC (2002) Patterns of infection with nematodes Syphacia obvelata and Aspicularis tetraptera in conventionally maintained laboratory mice. Mem I Oswaldo Cruz 97:847–853

    Article  Google Scholar 

  • Behnke JM (1975) Immune expulsion of the nematode Aspiculuris tetraptera from mice given primary and challenge infections. Int J Parasitol 5:511–515

    Article  CAS  PubMed  Google Scholar 

  • Bluszcz A, Blaski M, Sabesta R, Szilman P (1987) Helmintofauna drobnych gryzoni (Rodentia) kilku miejscowosci okrêgu katowickiego [Helminth fauna of small rodents (Rodentia) of several locality from the environment of Katowice]. Acta Biol Siles Zool 6:127–129

    Google Scholar 

  • Bush AO, Lafferty KD, Lotz J, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revised. J Parasitol 83(4):575–583

    Article  CAS  PubMed  Google Scholar 

  • Chang TK, Liao CW, Haung YC (2009) Prevalence of Enterobius vermicularis infection among preschool children in kinder gardens of Taipei City, Taiwan in 2008. Korean J Parasitol 47:185–187

    Article  PubMed Central  PubMed  Google Scholar 

  • Cobbold TS (1864) Entozoa: an introduction to the study of helminthology, more particularly to the internal parasites of man. pp 508. Quoted from Petter and Quentin (1976)

  • Falcón-Ordaz J, Pulido-Flores G, Monks S (2010) New species of Aspiculuris (Nematoda: Heteroxynematidae), parasite of Mus musculus (Rodentia: Muridae), from Hidalgo, Mexico. Rev Mex Biodiv 81:669–676

    Google Scholar 

  • Farrar PL, Wanger JE, Kagiyama N (1994) Syphacia spp. In: Waggie K, Kagiyama N, Allen A, Nomura T (eds) Manual of microbiologic monitoring of laboratory animals, 2nd edn. Natl I Health, USA, pp 219–224

    Google Scholar 

  • Hasegawa H (1991) Syphacia (Syphacia) ohtaorum n. sp. (Nematoda: Oxyuridae) from Mus caroli on Okinawa Island, Japan. Syst Parasitol 18:221–226

    Article  Google Scholar 

  • Hugot JP (2005) Syphacia (Syphacia) millardiae n. sp. (Nematoda: Oxyurida: Syphaciinae) from the Soft-Furred Field Rat, Millardia meltada, in India. Comp Parasitol 72(1):1–5

    Article  Google Scholar 

  • Hugot JP, Quentin JC (1985) Etude morphologique de six espe’ces nouvelles ou peu connues appartenant au genre Syphacia (Oxyuridae, Nematoda), parasites de rongeurs Cricetides et Murides. Bull Mus Nat Hist Nat 4 Serie 7:383–400

    Google Scholar 

  • Hussey K (1957) Syphacia muris vs. Syphacia obvelata in laboratory rats and mice. J Parasitol 43:555–559

    Article  CAS  PubMed  Google Scholar 

  • Izdebska JN, Rolbiecki L (2006) Correlation between the occurrence of mites (Demodex spp.) and nematodes in house mice (Mus musculus Linnaeus, 1758) in the Gdañsk urban agglomeration. Biol Lett 43(2):175–178

    Google Scholar 

  • Kataranovski D, Vukićević-Radić OD, Kataranovski M, Radović DL, Mirkov II (2008) Helminth fauna of Mus musculus Linnaeus 1758 from the suburban area of Belgrade, Serbia. Arch Biol Sci 60(4):609–617

    Article  Google Scholar 

  • Khalil AI, Morsy GH, Lashein GH, Abd El-Mottaleb DI, Sharaf AA (2013) Molecular variations based on RAPD among Oxyurids in Egypt. PUJ 6(1):39–50

    Google Scholar 

  • Khalil AI, Lashein GH, Morsy GH, Abd El-Mottaleb DI (2014) Oxyurids of wild and laboratory rodents from Egypt. Life Sci J 11(3):94–107

    Google Scholar 

  • Klimpel S, Förster M, Günter S (2007) Parasite fauna of the bank vole Chletrionomys glareolus in an urban region of Germany: reservoir of zoonotic metazoan parasites? Parasitol Res 102:69–75

    Article  PubMed  Google Scholar 

  • Klimpel S, Abdel-Ghaffar F, Al-Rasheid KA, Aksu G, Fischer K, Strassen B, Mehlhorn H (2011) The effects of different plant extracts on nematodes. Parasitol Res 108(4):1047–1054

    Article  PubMed  Google Scholar 

  • Landaeta-Aqueveque CA, Robles MDR, Cattan PE (2007) The community of gastrointestinal helminths in the house mouse, Mus musculus, in Santiago, Chile. Parasitol Latinoam 62:165–169

    Article  Google Scholar 

  • Linnaeus C (1758) Systema Naturae, Ed. X. (Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata). Holmiae. Sys Nat, Ed. X. v. 1: i-ii+ 1–824

  • Magalhaes R, Vicente J, Noroña D et al (1994) Helminth parasites of conventionally maintained laboratory mice. Mem I Oswaldo Cruz 89:33–40

    Google Scholar 

  • Mahmoud AE, Attia RAH, Eldeek HEM, Abdel Baki L, Oshaish HA (2009) Oxyurid nematodes detected by colonoscopy in patients with unexplained abdominal pain. Parasitol Unit J 2(2):93–102

    Google Scholar 

  • Mc-Manus DP, Bowles J (1996) Molecular genetic approaches to parasite identification: their value in diagnostic parasitology and systematics. Int J Parasitol 26:687–704

    Article  CAS  Google Scholar 

  • Mehlhorn H, Schmahl G, Mevissen I (2005) Efficacy of a combination of imidacloprid and moxidectin against parasites of reptiles and rodents: case reports. Parasitol Res 97(1):S97–S101

    Article  PubMed  Google Scholar 

  • Millazzo C, Ribasa A, Casanova JC et al (2010) Helminths of the brown rat (Rattus norvegicus) (Berkenhout, 1769) in the city of Palermo, Italy. Helminthology 47(4):238–240

    Google Scholar 

  • Neifer S, Kremsner PG, Weinig M, Harms G, Sahlmüller G, Bienzle U, Heitmann M, Breuer F, Mehlhorn H (1991) Interferon-gamma treatment in mice experimentally infected with Trichinella spiralis. Parasitol Res 77(5):437–442

    Article  CAS  PubMed  Google Scholar 

  • Ogden C (1971) Observations in the sistematic of nematodes belonging to the genus Syphacia Seurat, 1976. Bull Brit Mus 20:255–291

    Google Scholar 

  • Okamoto M, Urushima H, Iwasa M, Hasegawa H (2007) Phylogenetic relationships of rodent pinworms (genus Syphacia) in Japan inferred from mitochondrial CO1 gene sequences. J Vet Med Sci 69(5):545–547

    Article  CAS  PubMed  Google Scholar 

  • Pakdel N, Naem S, Rezaei F, Chalehchaleh AA (2013) A survey on helminthic infection in mice (Mus musculus) and rats (Rattus norvegicus and Rattus rattus) in Kermanshah, Iran. Vet Res Forum 4(2):105–109

    PubMed Central  PubMed  Google Scholar 

  • Parel JDC, Galula JU, Ooi HK (2008) Characterization of rDNA sequences from Syphacia obvelata, Syphacia muris, and Aspiculuris tetraptera and development of a PCR-based method for identification. Vet Parasitol 153:379–383

    Article  CAS  PubMed  Google Scholar 

  • Perec-Matysiak A, Okulewicz A, Hildebrand J, Zalesny G (2006) Helminth parasites of laboratory mice and rats. Wiad Parazytol 52:99–102

    PubMed  Google Scholar 

  • Petter AJ, Quentin JC (2009) Keys to the genera of the Oxyuroidea. In: Anderson RC, Chabaud AG, Willmott S (eds) CIH keys to the nematode parasites of vertebrates. Com W Agri Bur, England, pp 1–30

    Google Scholar 

  • Robles MR, Navone GT (2007) A new species of Syphacia (Nematoda: Oxyuridae) from Oligoryzomys nigripes (Rodentia: Cricetidae) in Argentina. Parasitol Res 101(4):1069–1075

    Article  Google Scholar 

  • Robles MR, Navone GT (2010) Redescription of Syphacia venteli Travassos 1937 (Nematoda: Oxyuridae) from Nectomys squamipes in Argentina and Brazil and description of a new Syphacia from Melanomys caliginosus in Colombia. Parasitol Res 106(5):1117–1126

    Article  Google Scholar 

  • Rudolphi CA (1802) Forsetung der Beobachtungen uber die Eingeweide Wurmer. Archiv Zool Zoot 2:1–67

    Google Scholar 

  • Semenova SK, Romanova EA, Pyskov AP (1996) Genetic differentiation of helminthes on the basis of data of polymerase chain reaction using random primers. Genetics 32(2):304–309

    CAS  Google Scholar 

  • Seurat LG (1916) Sur les oxyures des Mammiféres. Can Cream Soc Biol 79:64–68

    Google Scholar 

  • Singh B (1997) Molecular methods for diagnosis and epidemiological studies of parasitic infections. Int J Parasitol 27(10):1135–1145

    Article  CAS  PubMed  Google Scholar 

  • Skrjabin KI, Schikhobalova ND (1948) Quoted from Petter and Quentin (1976)

  • Smales LR (2001) Syphacia longaecauda n. sp. (Nematoda: Oxyuridae) Syphacinea from Melomys spp. (Muridae: Hydromyinae) from Papua New Guinea and Irian Jaya, Indonesia. Parasitology 8:39–43

    CAS  Google Scholar 

  • Smales LR (2004) Syphacia (Syphacia) australasiensis sp. nov. (Nematoda: Oxyuridae) from Rattus leucopus (muridae) from Papua New Guiena and Australia. Trans R Soc S Aust 128:47–51

    Google Scholar 

  • Sotillo J, Trelis M, Cortés A, Luz Valero M, Sánchez del Pino M, Esteban JG, Marcilla A, Toledo R (2012) Proteomic analysis of the pinworm Syphacia muris (Nematoda: Oxyuridae), a parasite of laboratory rats. Parasitol Int 61(4):561–564

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Travassos L (1919) Quoted from Petter and Quentin (2009)

  • Verma S, Gaherwal S, Prakash MM, Kanhere RR (2013) Anthelmintic efficacy of Ocimum sanctum against Syphacia muris in mice. Acta Parasitol Glob 4(1):24–28

    Google Scholar 

  • Vermund SH, Wilson CM (2000) Pinworm (Enterobius vermicularis). Semin Pediatr Infect Dis 11:252–256

    Article  Google Scholar 

  • Weaver HJ, Smales LR (2006) Syphacia (Syphacia) abertoni n. sp. (Nematoda: Oxyuridae) from Zyzomys argurus (Thomas) (Rodentia: Muridae) from Northern Australia. Trans R Soc S Aust 131(2):260–210

    Google Scholar 

  • Weaver HJ, Smales LR (2008) New species of Syphacia (Syphacia) Seurat (Nematoda: Oxyuridae) from Pseudamys species (Rodentia: Muridae) from central Australia. Zootaxa 1775:39–50

    Article  Google Scholar 

  • Yamaguti S (1935) Studies on the helminth fauna of Japan. Part 13. Mammalian nematodes. Jpn J Zool 6:433–457

    Google Scholar 

Download references

Acknowledgments

This work is supported by Faculty of Science, Cairo University, Cairo, Egypt. Also, author extends her appreciations to members of Molecular Biology and Genetic Engineering Unit in the Holding Company for Biological Products and Vaccines (VACSERA) in completing this work.

Author information

Authors and Affiliations

  1. Zoology Department, Faculty of Science, Cairo University, Cairo, Egypt

    Rewaida Abdel-Gaber

Authors
  1. Rewaida Abdel-Gaber
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rewaida Abdel-Gaber.

Ethics declarations

Conflict of interest

I declare that we have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abdel-Gaber, R. Syphacia obvelata (Nematode, Oxyuridae) infecting laboratory mice Mus musculus (Rodentia, Muridae): phylogeny and host-parasite relationship. Parasitol Res 115, 975–985 (2016). https://doi.org/10.1007/s00436-015-4825-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4825-0

Keywords

Search

Navigation