Skip to main content
SpringerLink
Log in

Prevalence, Morphological and Molecular Phylogenetic Analyses of the Rabbit Pinworm, Passalurus ambiguus Rudolphi 1819, in the Domestic Rabbits Oryctolagus cuniculus

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Introduction

Passalurus ambiguus, a pinworm nematode parasite, infects domestic and wild rabbits, hares, and rodents worldwide.

Materials and Methods

The current parasitological study was performed during January–December 2016, to investigate helminth parasites infecting the domestic rabbit species Oryctolagus cuniculus at the Department of Animal Production, Faculty of Agriculture, Cairo University, Cairo, Egypt.

Results

Of the twenty rabbit specimens examined for gastrointestinal nematodes, 75% were infected with adult oxyurid species, which were morphologically characterized using light and scanning electron microscopy studies. The oxyurid species had a triangular mouth opening surrounded by simple lips with four cephalic papillae and a pair of lateral amphidial pores with three teeth-like structures, an esophagus divided into a cylindrical corpus and globular bulb supported internally with tri-radiate valvular apparatus, and four caudal papillae distributed on the posterior end of males with a single short protruding spicule and ovijector apparatus opening ventrally by the vulva, surrounded by protruded lips in female worms. The species were compared morphometrically with other Passalurus species described previously; light differences were found in different body part sizes. Molecular characterization based on 18 small subunit (SSU) rDNA sequences showed ~ 85% similarity with other Chromadorea species. A preliminary genetic comparison between the 18S rDNA sequences of the isolated parasite and those of other oxyurid species suggested that it belonged to Passalurus ambiguus. The 18S rDNA sequence of the parasite was deposited in GenBank (accession no., MG310151.1).

Conclusion

The 18S rDNA gene of P. ambiguus was shown to yield a unique genetic sequence that confirms its taxonomic position within the Oxyuridae family.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Abade Dos Santos FA, Carvalho C, Nuno O, Correia JJ, Henriques M, Peleteiro MC, Fevereiro M, Duarte MD (2017) Detection of rabbit Haemorrhagic disease virus 2 during the wild rabbit (Oryctolagus cuniculus) eradication from the Berlengas archipelago, Portugal. BMC Vet Res 13(1):336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Abdel-Gaber R (2016) Syphacia obvelata (Nematode, Oxyuridae) infecting laboratory mice Mus musculus (Rodentia, Muridae): phylogeny and host–parasite relationship. Parasitol Res 115:975–985

    Article  PubMed  Google Scholar 

  3. Abdel-Gaber R, Fol M (2015) Aspicularis tetraptera (Nematode, Heteroxynematidae) of laboratory mice Mus musculus (Rodentia, Muridae): a potential risk of zoonotic infection for researchers. Ciência e Técnica Vitivinícola 30(8):125–136

    Google Scholar 

  4. Arkoulis N, Zerbinis H, Simatos G, Nisiotis A (2012) Enterobius vermicularis (pinworm) infection of the liver mimicking malignancy: presentation of a new case and review of current literature. Int J Surg Case Rep 3:6–9

    Article  PubMed  Google Scholar 

  5. Ashmawy KI, El-Sokkary MY, Abu-Akkada SS, Dewair AW (2010) Incidence of Passalurus ambiguus in domestic rabbits in Behera Province. Alex J Vet Sci 30(1):115–120

    Google Scholar 

  6. Baker DG (2007) Flynn’s parasites of laboratory animals, 2nd edn. Blackwell Publishing, Hoboken, p 813

    Book  Google Scholar 

  7. Bin Z, Chunsheng B (1987) Scanning electron microscopic observations of the integumental surface of adult Passalurus ambiguus. Acta Zool Sin 33(4):383–384

    Google Scholar 

  8. Boag B, Lello J, Fenton A, Tompkins DM, Hudson PJ (2001) Patterns of parasite aggregation in the wild European rabbit (Oryctolagus cuniculus). Int J Parasitol 31:1421–1428

    Article  CAS  PubMed  Google Scholar 

  9. Bush AO, Lafferty KD, Lotz JM, 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 

  10. Caballero E (1937) Passalurus abditus nouvelle espèce de nématode parasite d’un Rongeur mexicain. Annales de Parasitologie Humaine et comparée 15:504–506

    Article  Google Scholar 

  11. 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  PubMed Central  Google Scholar 

  12. Cheeke PR (1986) Potentials of rabbit production in tropical and subtropical agricultural systems. J Anim Sci 63:1581–1856

    Article  Google Scholar 

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

  14. Danheim BL, Ackert JE (1929) On the anatomy of the nematode Passalurus ambiguus (Rudolphi). Trans Am Microsc Soc 48:80–85

    Article  Google Scholar 

  15. De Ley P, Blaxter M (2002) Systematic position and phylogeny. In: Lee DL (ed) The biology of nematodes. Taylor and Francis, London and New York, pp 1–30

    Chapter  Google Scholar 

  16. Dufour B, Hugot JP, Lepetz S, Le Bailly M (2015) The horse pinworm (Oxyuris equi) in archaeology during the Holocene: review of past records and new data. Infect Genet Evol 33:77–83

    Article  PubMed  Google Scholar 

  17. Durden LA, Hu R, Oliver JH, Cilek JE (2000) Rodent ectoparasites from two locations in northwestern Florida. J Vector Ecol 25:222–228

    CAS  PubMed  Google Scholar 

  18. Floyd R, Rogers A, Lambshead P, Smith C (2005) Nematode-specific PCR primers for the 18S small subunit rRNA gene. Mol Ecol Notes 5:611–612

    Article  CAS  Google Scholar 

  19. Flynn RJ (1973) Parasites of laboratory animals. The Iowa State University Press, Ames, p 882

    Google Scholar 

  20. Frank R, Kuhn T, Mehlhorn H, Rueckert S, Pham D, Klimpel S (2013) Parasites of wild rabbits (Oryctolagus cuniculi) from an urban area in Germany, in relation to worldwide results. Parasitol Res 112:4255–4266

    Article  PubMed  Google Scholar 

  21. Fuentes GC, Newgren J (2008) Physiology and clinical pathology of laboratory New Zealand white rabbits housed individually and in groups. J Am Assoc Lab Anim Sci 47(2):35–38

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Georgi JR, Georgi ME (1990) Parasitology for veterinarians. Saunders, Philadelphia

    Google Scholar 

  23. Hall ER, Kelson KR (1959) The mammals of North America. The Ronald Press Company, New York, p 1083

    Google Scholar 

  24. Hall MC (1916) Nematode parasites of mammals of the orders Rodentia, Lagomorpha and Hyracoidea. Proc USA Natl Mus 50:1–258

    Article  Google Scholar 

  25. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  26. Hallal-Calleros C, Morales-Montor J, Vázquez-Montiel JA, Hoffman KL, Nieto-Rodríguez A, Flores-Pérez AI (2013) Hormonal and behavioral changes induced by acute and chronic experimental infestation with Psoroptes cuniculi in the domestic rabbit Oryctolagus cuniculus. Parasites Vectors 6:341–361

    Article  CAS  Google Scholar 

  27. Hugot JP (1980) Sur le genre Aspiculuris Schulz, 1924 (Nematoda, Heteroxynematidae), Oxyures parasites de Rongeurs Muroidea. Bulletin du Museum National d’Histoire Naturelle 2:723–735

  28. Hugot JP, Bain O, Cassone J (1982) Insemination traumatique et tube de ponte chex l’Oxyure parasite du lapin domestique. Compte Rendu Hebdomadaire Seances de l’Academie des Sciences t. 294(19 avril 1982) Ser. III:707–710

  29. Jobet E, Bougnoux ME, Morand S, Rivault C, Cloarec A, Hugot JP (1998) Use of random amplified polymorphic DNA (RAPD) for generating specific DNA probes for oxyuroid species (Nematoda). Parasite 5:47–50

    Article  CAS  PubMed  Google Scholar 

  30. Johnston TH, Mawson PM (1938) Some nematodes from Australian marsupials. Rec S Aust Mus 6:187–198

    Google Scholar 

  31. Kang S, Sultana T, Eom KS, Park YC, Soonthornpong N, Nadler SA, Park JK (2009) The mitochondrial genome sequence of Enterobius vermicularis (Nematoda: Oxyurida)—an idiosyncratic gene order and phylogenetic information for Chromadorean nematodes. Gene 429:87–97

    Article  CAS  PubMed  Google Scholar 

  32. 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 

  33. 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 

  34. Kim T, Kim J, Cho S, Min GS, Park C, Carreno RA, Nadler SA, Park JK (2014) Phylogeny of Rhigonematomorpha based on the complete mitochondrial genome of Rhigonema thysanophora (Nematoda: Chromadorea). Zoolog Scr 43:289–303

    Article  Google Scholar 

  35. 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 

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

    Article  PubMed  Google Scholar 

  37. Kylie J, McEwen SA, Boerlin P, Reid-Smith RJ, Weese JS, Turner PV (2017) Prevalence of antimicrobial resistance in fecal Escherichia coli and Salmonella enterica in Canadian commercial meat, companion, laboratory, and shelter rabbits (Oryctolagus cuniculus) and its association with routine antimicrobial use in commercial meat rabbits. Prev Vet Med 147:53–57

    Article  PubMed  Google Scholar 

  38. Li H, Shao R, Song N, Song F, Jiang P, Li Z, Cai W (2015) Higher–level phylogeny of paraneopteran insects inferred from mitochondrial genome sequences. Sci Rep 5:8527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. 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 1:1–824

  40. Liu GH, Li S, Zou FC, Wang CR, Zhu XQ (2016) The complete mitochondrial genome of rabbit pinworm Passalurus ambiguus: genome characterization and phylogenetic analysis. Parasitol Res 115:423–429

    Article  PubMed  Google Scholar 

  41. Liu GH, Shao R, Cai XQ, Li WW, Zhu XQ (2015) Gnathostoma spinigerum mitochondrial genome sequence: a novel gene arrangement and its phylogenetic position within the class chromadorea. Sci Rep 5:12691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Liu GH, Shao R, Li JY, Zhou DH, Li H, Zhu XQ (2013) The complete mitochondrial genomes of three parasitic nematodes of birds: a unique gene order and insights into nematode phylogeny. BMC Genomics 14:414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Martino PA, Luzi F (2008) Bacterial infections in rabbit as companion animal: a survey of diagnostic samples in Italy. 9th World Rabbit Congress, Verona, Italy, pp 1013–1014

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

    Article  Google Scholar 

  45. Nadler SA, D’Amelio S, Dailey MD, Paggi L, Siu S, Sakanari JA (2005) Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from northern Pacific marine mammals. J Parasitol 91:1413–1429

    Article  CAS  PubMed  Google Scholar 

  46. Neimanis AS, Ahola H, Zohari S, Larsson Pettersson U, Brojer C, Capucci L, Gavier-Widen D (2018) Arrival of rabbit haemorrhagic disease virus 2 to northern Europe: emergence and outbreaks in wild and domestic rabbits (Oryctolagus cuniculus) in Sweden. Transbound Emerg Dis. 65(1):213–220

    Article  CAS  PubMed  Google Scholar 

  47. Ogedengbe ME, El-Sherry S, Whale J, Barta JR (2014) Complete mitochondrial genome sequences from five Eimeria species (Apicomplexa; Coccidia; Eimeriidae) infecting domestic turkeys. Parasites Vectors 7:335

    Article  PubMed  PubMed Central  Google Scholar 

  48. Okerman L (1994) Diseases of domestic rabbits, 2nd edn. Blackwell Scientific Publications, Oxford (England), p 160

    Google Scholar 

  49. Park JK, Sultana T, Lee SH, Kang S, Kim HK, Min GS, Eom KS, Nadler SA (2011) Monophyly of clade III nematodes is not supported by phylogenetic analysis of complete mitochondrial genome sequences. BMC Genomics 12:392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Percy DH, Barthold SW (1993) Pathology of laboratory rodents and rabbits. Iowa State University Press, Iowa

    Google Scholar 

  51. Petter AJ, Quentin JC (2009) Oxyuroidea. In: Anderson RC, Chabaud AG, Willmott S (eds) Keys to the nematode parasites of vertebrates (Archival Volume). CAB Int, London, pp 218–247

    Chapter  Google Scholar 

  52. Pinto RM, Gomez DC, Menezes RC, Gomez CT, Noronha D (2004) Helminths of rabbits (Lagomorpha, Leporidae) deposited in the Helminthological Collection of the Oswaldo Cruz Institute. Revista Brasileira de Zoologia 21(3):599–604

    Article  Google Scholar 

  53. Pritt S, Cohen K, Sedlacek H (2012) The laboratory rabbit, guinea pig, hamster, and other rodents. Chapter 15 Parasitic Diseases, pp 415–446

  54. Rinaldi L, Russo T, Schioppi M, Pennacchio S, Cringoli G (2007) Passalurus ambiguus: new insights into copromicroscopic diagnosis and circadian rhythm of egg excretion. Parasitol Res 101:557–561

    Article  PubMed  Google Scholar 

  55. 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 

  56. 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 species of Syphacia from Melanomys caliginosus in Colombia. Parasitol Res 106:1117–1126

    Article  Google Scholar 

  57. Romero Rodriguez J, Pozo DG, Herrera JL (1973) Estudios sobre el genero Passalurus Dujardin, 1845, parasitando al Oryctolagus cuniculus domesticus (L.) y Lepus granatensis R. Revista Iberica de Parasitologia 33:315–329

    Google Scholar 

  58. Rudolphi CA (1819) Entozoarum synopsis cui accedunt mantissa duplex et indices locupletissimi. Berlin 8:811

    Google Scholar 

  59. Sheng L, Cui P, Fang SF, Lin RQ, Zou FC, Zhu XQ (2015) Sequence variability in four mitochondrial genes among rabbit pinworm (Passalurus ambiguus) isolates from different localities in China. Mitochondrial DNA 26:501–504

    Article  CAS  PubMed  Google Scholar 

  60. Singla LD, Singla N, Parshad VR, Juyal PD, Naresh KS (2008) Rodents as reservoirs of parasites in India. Integr Zool 3(1):21–26

    Article  PubMed  Google Scholar 

  61. Skinker MS (1931) Three new parasitic nematode worms. Proc US Natl Mus 79:1–9

    Article  Google Scholar 

  62. Solórzano-García B, Nadler SA, Ponce Perez, de León G (2015) Trypanoxyuris atelis and T. atelophora (Nematoda: Oxyuridae) in wild spider monkeys (Abeles geoffroyi) in tropical rain forest in Mexico: morphological and molecular evidence. Parasitol Int 64:229–235

    Article  PubMed  Google Scholar 

  63. 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 Res 61(4):561–564

    CAS  Google Scholar 

  64. Sultan K, Elhawary NM, Sorour SG, Sharaf HM (2015) Observations of the rabbit pinworm Passalurus ambiguus (Rudolphi, 1819) in domestic rabbits (Oryctolagus cuniculus) in Egypt using a scanning electron microscope. Trop Biomed 32(4):745–752

    PubMed  Google Scholar 

  65. Swofford DL (2000) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MA

  66. Szkucik K, Pyz-Łukasik R, Szczepaniak KO, Paszkiewicz W (2014) Occurrence of gastrointestinal parasites in slaughter rabbits. Parasitol Res 113:59–64

    Article  PubMed  Google Scholar 

  67. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  68. 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  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  70. Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM (1997) Nematóides Do Brasil. Parte V: Nematóides De Mamíferos. Revista Brasileira de Zoologia 14(1):1–452

    Article  Google Scholar 

  71. Wu HW (1933) Helminthological notes I. Sinensia 4:51–59

    Google Scholar 

  72. Yamaguti S (1961) Systema Helminthum. Volume I. The nematodes of vertebrates. Part I and II. Interscience Publisher, New York, pp 535–560

    Google Scholar 

  73. Yang X, Gasser RB, Koehler AV, Wang L, Zhu K, Chen L, Feng H, Hu M, Fang R (2015) Mitochondrial genome of Hypoderaeum conoideum–comparison with selected trematodes. Parasites Vectors 8:97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to extend their sincere appreciation to the Deanship of Scientific Research at King Saud University for its funding this Research Group No. RGP-VPP- 173.

Author information

Authors and Affiliations

  1. Zoology Department, College of Science, King Saud University, Riyadh, Saudi Arabia

    Rewaida Abdel-Gaber & Dalia Fouad

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

    Rewaida Abdel-Gaber

  3. Department of Biochemistry, College of Science, King Saud University, Riyadh, Saudi Arabia

    Farid Ataya & Mohamed Daoud

  4. Genetic Engineering Division, Molecular Biology Department, National Research Centre, Cairo, Egypt

    Farid Ataya

  5. Department of Zoology and Entomology, Faculty of Science, Helwan University, Helwan, Egypt

    Dalia Fouad

  6. Electron Microscopy Unit, Central Laboratory, King Saud University, Riyadh, Saudi Arabia

    Shatha Alzuhairy

Authors
  1. Rewaida Abdel-Gaber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Farid Ataya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dalia Fouad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohamed Daoud
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shatha Alzuhairy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rewaida Abdel-Gaber.

Ethics declarations

Conflicts of Interest

The authors declare no conflicts of interest.

Ethical Approval

All procedures contributing to this work comply with the ethical standards of the relevant national guides on the care and use of laboratory animals and have been approved and authorized by the Institutional Animal Care and Use Committee (IACUC) in Faculty of Science, Cairo University, Egypt [CU/I/S/18-16].

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abdel-Gaber, R., Ataya, F., Fouad, D. et al. Prevalence, Morphological and Molecular Phylogenetic Analyses of the Rabbit Pinworm, Passalurus ambiguus Rudolphi 1819, in the Domestic Rabbits Oryctolagus cuniculus. Acta Parasit. 64, 316–330 (2019). https://doi.org/10.2478/s11686-019-00047-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11686-019-00047-7

Keywords

Search

Navigation