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Morphometry, molecular identification and histopathology of Passalurus ambiguus Rudolphi, 1819 in domestic rabbits (Oryctolagus cuniculus) in Qena, Upper Egypt

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Abstract

In Egypt, domestic rabbits are commercially used for meat production. Adversely, gastrointestinal helminthiasis largely delays such concern. Passalurus ambiguus is a common intestinal nematode that infects rabbits causing intestinal disorders and death in severe infection. Therefore, domestic rabbits collected from several locations (poultry slaughter shops, rabbits farms, markets and public owners) in Qena, Upper Egypt. Passalurus ambiguus worms were detected in 90 out of 200 rabbits (45%). Grossly, they appeared as small white nodules in the appendix of the rabbits examined. Adult worms were described morphologically using light and scanning electron microscopy. Adult male measured 4.622 mm (2.838–7.172 mm) in length and 0.278 mm (0.139–0.558 mm) in width. Adult female measured 5.622 mm (2.347–9.532 mm) in length and 0.314 mm (0.185–0.381 mm) in width. SEM showed a transverse cuticular striations on the body of both males and females, four papillae on the dorsal and ventral surface and the mouth was triangular and surrounded by three teeth. Phylogenetic data proved the occurrence of the intestinal nematode, Passalurus ambiguus. Microscopically, heavy worms infestated the appendiceal layers causing appendicitis manifested by granuloma with hyperplasia in the epithelial lining inducedobstruction in the lumen. It could be concluded that morphological features, molecular phylogenetic data, and histopathological findings clearly identified the present species as Passalurus ambiguus Rudolphi, 1819.

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References

  • Abdel-Gaber R (2016) Syphacia obvelata (Nematode, Oxyuridae) infecting laboratory mice Mus musculus (Rodentia, Muridae): phylogeny and host–parasite relationship. Parasitol Res 115(3):975–985

    Article  Google Scholar 

  • Abdel-Gaber R, Ataya F, Fouad D, Daoud M, Alzuhairy S (2019) Prevalence, morphological and molecular phylogenetic analyses of the rabbit pinworm, Passalurus ambiguus Rudolphi 1819, in the domestic rabbits Oryctolagus cuniculus. Acta Parasitol 64(2):316–330

    Article  Google Scholar 

  • Adamson ML (1989) Evolutionary biology of the Oxyurida (Nematoda): biofacies of a haplodiploid taxon. Adv Parasitol 28:175–228

    Article  CAS  Google Scholar 

  • Astasio-Arbiza P, Zapatero-Ramos LM, Solera-Puertas MA, González-Santiago PM (1988) Thelandros galloti n. sp. (Nematoda, Pharyngodonidae) sobre Gallotia galloti galloti Duméril y Bibron, 1839, lacértido endémico de Tenerife (Islas Canarias). Revist Parasitol 48(3):283–288

  • Bell KC, Demboski JR, Cook JA (2018) Sympatric parasites have similar host-associated, but asynchronous, patterns of diversification. Am Nat 192(3):E106–E119

    Article  Google Scholar 

  • 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 

  • Cao YF, Chen HX, Li Y, Zhou DW, Chen SL, Li L (2020) Morphology, genetic characterization and molecular phylogeny of pinworm Skrjabinema longicaudatum n. sp.(Oxyurida: Oxyuridae) from the endangered Tibetan antelope Pantholops hodgsonii (Abel)(Artiodactyla: Bovidae). Parasites and Vectors 13(1):1

    Article  Google Scholar 

  • Chabaud AG (1974) Keys to subclasses, orders and superfamilies No. 1. In: Anderson RC, Chabaud AG, Willmott S (eds) CIH keys to the nematode parasites of vertebrates. Commonwealth Agricultural Bureaux, Farnham Royal, UK), pp 1–17

    Google Scholar 

  • Danheim BL, Ackert JE (1929) On the anatomy of the nematode Passalurus ambiguus (Rudolphi). Trans Am Microscopical Soc 48(1):80–85

    Article  Google Scholar 

  • De Bellocq JG, Ferté H, Depaquit J, Justine JL, Tillier A, Durette-Desset MC (2001) Phylogeny of the Trichostrongylina (Nematoda) inferred from 28S rDNA sequences. Mol Phylogenet Evol 19(3):430–442

    Article  Google Scholar 

  • De Sousa A, Jorge F, Carretero MA, Harris DJ, Roca V, Perera A (2019) The importance of integrative approaches in nematode taxonomy: the validity of Parapharyngodon and Thelandros as distinct genera. J Helminthol 93(5):616–628

    Article  Google Scholar 

  • Dos Santos FAA, 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):1

    Google Scholar 

  • El-Akabawy LM, Zayan KA, Tantawy AA, Omar REM (2004) Anticoccidial efficacy of propolis and toltrazuril against Eimeria stiedae in New Zealand White Rabbit’s. Zagazig Veter J 32(1):129–145

    Google Scholar 

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

    Google Scholar 

  • Grice RL, Prociv P (1993) In vitro embryonation of Syphacia obvelata eggs. Int J Parasitol 23(2):257–260

    Article  CAS  Google Scholar 

  • Hugot JP (1988) Les nématodes Syphaciinae, parasites de rougeurs et de lagomorphes. Mémoires du Muséum. Natl d’Histoire Naturelle 141:13–149

    Google Scholar 

  • Hugot JP, Bain O, Cassone J (1983) Sur le genre Passalurus (Oxyuridae: Nematoda) parasite de leporidés. Syst Parasitol 5(4):305–316

    Article  Google Scholar 

  • Hugot JP, Gardner SL, Morand S (1996) The Enterobiinae subfam. Nov. (Nematoda, Oxyurida) pinworm parasites of primates and rodents. Int J Parasitol 26(2):147–159

    Article  CAS  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 

  • 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(1):8527

    Article  CAS  Google Scholar 

  • Li Y, Chen HX, Yang XL, Li L (2019) Morphological and genetic characterization of Syphabulea tjanschani (Ablasov, 1962) (Nematoda: Oxyuridae), with phylogenetic position of Syphabulea in Oxyuridae. Infect Genet Evol 67:159–166

    Article  CAS  Google Scholar 

  • Mejia-Madrid HH (2018) A molecular phylogeny of the Rhigonematomorpha De Ley & Blaxter, 2002 as inferred from SSU and LSU rDNA sequences. Nematology 20(6):547–565

    Article  CAS  Google Scholar 

  • Meyer MC, Olsen OW (1975) Essentials of parasitology, 2nd edn. WM. C. Brown Company Publishers, New York

    Google Scholar 

  • Milazzo C, Ribas A, Casanova JC, Cagnin M, Geraci F, Bella C (2010) Helminths of the brown rat (Rattus norvegicus) (Berkenhout, 1769) in the city of Palermo. Italy Helminthologia 47(4):238–240

    Article  Google Scholar 

  • Mykhailiutenko SM, Kruchynenko OV, Klymenko OS, Serdioucov JK, Dmytrenko NI, Tkachenko VV (2019) Pathomorphological changes in the large intestine of rabbits parasitised by Passalurus ambiguus (Nematoda, Oxyuridae). Regulatory Mech Biosyst 10(1):69–74

  • Ogedengbe ME, El-Sherry S, Whale J, Barta JR (2014) Complete mitochondrial genome sequences from five Eimeria species (Apicomplexa; coccidia; Eimeriidae) infecting domestic turkeys. Paras Vectors 7(1):335

    Article  Google Scholar 

  • Owen D (1972) Common parasites of laboratory rodents and lagomorphs, Laboratory animals centre handbook no. 1. Medical Research Council

  • 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(1):559

    Article  Google Scholar 

  • Petter AJ, Quentin JC (1976) Keys to genera of the Oxyuroidea-No. 4. In: Anderson RC, Chabaud AG, Willmott S (eds) CIH keys to the nematode parasites of vertebrates. Commonwealth Agricultural Bureaux, Farnham Royal UK, pp 1–30

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

    Chapter  Google Scholar 

  • Rodriguez RJ, Pozo GD, Herrera LJ (1974) Estudios sobre el genero Passalurus Dujardin, 1845, parasitando al Oryctolagus cuniculus domesticus (L.) y Lepus granatensis R. Rev Iberica Parasitol 33:315–329

    Google Scholar 

  • Rosario Robles RMR, 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 

  • Sheng L, Cui P, Fang SF, Lin RQ, Zou FC, Zhu XQ (2015) Sequence variability in four mitochondrial genesamong rabbit pinworm (Passalurus ambiguus) isolates from different localities in China. Mitochondrial DNA 26(4):501–504

    Article  CAS  Google Scholar 

  • Skinker MS (1931) Three new parasitic nematode worms. Proc US Natl Museum 79(2890):1–9

  • Solórzano-García B, Falcón-Ordaz J, Parra-Olea G, Pérez-Ponce de León G (2020) Batracholandros salamandrae (Oxyuroidea: Pharyngodonidae) in endemic salamanders (Amphibia: Plethodontidae) of the trans-Mexican volcanic belt: host range wide distribution or cryptic species complex? J Parasitol 106(5):633–643

    Article  Google Scholar 

  • Sotillo J, Trelis M, Cortés A, Luz Valero M, del Pino MS, 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 

  • Sultan K, Elhawary NM, Sorour SSG, 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

    CAS  PubMed  Google Scholar 

  • Taffs LF (1976) Pinworm infections in laboratory rodents: a review. Lab Anim 10(1):1–13

    Article  CAS  Google Scholar 

  • Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM (1997) Nematóides do brasil. Parte V: Nematóides de mamíferos. Rev Brasil Zool 14(1):1–14

    Article  Google Scholar 

  • Yamaguti S (1961) Systema Helminthum: Volume I. The nematodes of vertebrates. Part I and II. Interscience Publisher, New York

    Google Scholar 

  • Yang D, Ren Y, Fu Y, Xie Y, Nie H, Nong X, Gu X, Wang S, Peng X, Yang G (2013) Genetic variation of Taenia pisiformis collected from Sichuan, China, based on the mitochondrial cytochrome B gene. Korean J Parasitol 51(4):449–452

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Electron Microscopy Unit at South Valley University for their direct help and technical assistance with scanning electron microscopic investigations and EKB editing service for English editing of manuscript.

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Authors and Affiliations

  1. Department of Zoology, Faculty of Science, South Valley University, 83523, Qena, Egypt

    Nermean M. Hussein, Soheir A. H. Rabie & Wafaa A. Abuelwafa

  2. Department of Pathology, Faculty of Veterinary Medicine, South Valley University, 83523, Qena, Egypt

    Mouchira M. Mohi ElDin

Authors
  1. Nermean M. Hussein
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  2. Soheir A. H. Rabie
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  3. Wafaa A. Abuelwafa
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  4. Mouchira M. Mohi ElDin
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Contributions

Nermean M. Hussein: investigation, methodology, writing—review and editing. Soheir A. H. Rabie: supervision, writing—review and editing. Wafaa A. Abuelwafa: collecting samples, methodology, writing—original draft. Mouchira M. Mohi ElDin:, writing—review and editing the histopathological part.

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Correspondence to Nermean M. Hussein.

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The institutional ethics committee. Animal experiments followed the institutional ethical guidelines for the care and use of animals in research to the letter. Approval for animal studies were obtained from the Faculty of Veterinary medicine, South Valley University, Qena, Egypt (Approval number: 25/13/11.2021).

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Hussein, N.M., Rabie, S.A.H., Abuelwafa, W.A. et al. Morphometry, molecular identification and histopathology of Passalurus ambiguus Rudolphi, 1819 in domestic rabbits (Oryctolagus cuniculus) in Qena, Upper Egypt. J Parasit Dis 46, 511–525 (2022). https://doi.org/10.1007/s12639-022-01477-3

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