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Comparative morphological and molecular identification of Haemonchus species in sheep

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Helminthologia

Summary

A combined approach in the determination of Haemonchus nematodes from sheep was applied in this trial. Using selected morphological characters 90.2 % females and 84.2 % males of Haemonchus contortus and 9.8 % females and 15.8 % males of Haemonchus placei were identified. Although cluster analysis based on morphological identification clearly separated two Haemonchus species, H. contortus was exclusively detected in all specimens using restriction cleavage of the ITS-2 region with FspBI endonuclease as well as through the sequencing analysis. Because sheep from both farms have never had contact with other ruminants, and the farmers apply only closed flock turnover, we assume that only H. contortus mono-infection occurred on both farms. This opinion is also supported by molecular data. The most striking result of our study was the finding which indicates that the discriminant function is not able to accurately identify Haemonchus males at the species level.

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References

  • Achi, Y. L., Zinsstag, J., Yao, K., Yeo, N., Dorchies, P., Jacquiet, P. (2003): Host specificity of Haemonchus spp. for domestic ruminants in the savanna in northern Ivory Coast. Vet. Parasitol., 116: 151–158. DOI: 10.1016/S0304-4017(03)00258-9

    Article  CAS  PubMed  Google Scholar 

  • Aumont, G., Gruner, L., Hostache, G. (2003): Comparison of the resistance to sympatric and allopatric isolates of Haemonchus contortus of Black Belly sheepin Guadeloupe (FWI) and of INRA 401 sheep in France. Vet. Parasitol., 116: 139–150. DOI: 10.1016/S0304-4017(03)00259-0

    Article  CAS  PubMed  Google Scholar 

  • Bártíková, H., Skálová, L., Lamka, J., Szotáková, B., Várady, M. (2010): The effects of flubendazole and its metabolites on the larval development of Haemonchus contortus (Nematoda: Trichostrongylidae): an in vitro study. Helminthologia, 47(4): 269–272. DOI: 10.2478/s11687-010-0042-7

    Article  Google Scholar 

  • Bensch, S., PÉREZ-TRIS, J., Waldenström, J., Hellgren, O. (2004): Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution, 58(7): 1617–1621

    Article  CAS  PubMed  Google Scholar 

  • Blouin, M. S., Yowell, C. A., Courtney, C. H., Dame, J. B. (1997): Haemonchus placei and Haemonchus contortus are distinct species based on mtDNA evidence. Int. J. Parasitol., 27(11): 1383–1387

    Article  CAS  PubMed  Google Scholar 

  • Brasil, B. S., Nunes, R. L., Bastianetto, E., Drummond, M. G., Carvalho, D. C., Leite, R. C., Molento, M. B., Oliveira, D. A. (2012): Genetic diversity patterns of Haemonchus placei and Haemonchus contortus populations isolated from domestic ruminants in Brazil. Int. J. Parasitol., 42: 469–479

    Article  PubMed  Google Scholar 

  • Bremner, K. C. (1955): Cytological studies on the specific distinctness of the Ovine and Bovine „strains“ of the nematode Haemonchus contortus (Rudolphi) Cobb (Nematoda: Trichostrongylidae). Aus. J. Zool., 3: 312–323

    Article  Google Scholar 

  • Chilton, N. B., Newton, L. A., Beveridge, I., Gasser, R. B. (2001): Evolutionary relationships of trichostrongyloid nematodes (Strongylida) inferred from ribosomal DNA sequence data. Mol. Phylogenet. Evol., 19(3): 367–386. DOI:10.1006/mpev.2001.0938

    Article  CAS  PubMed  Google Scholar 

  • Criscione, C. D., Poulin, R., Blouin, M. S. (2005): Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol. Ecol., 14(8): 2247–2257. DOI: 10.1111/j.1365-294X.2005.02587.x

    Article  CAS  PubMed  Google Scholar 

  • do Amarante, A.F. (2011): Why is it important to correctly identify Haemonchus species? Rev. Bras. Parasitol. Vet., 20(4): 263–268

    Article  PubMed  Google Scholar 

  • Gasser, R. B. (2006): Molecular tools—advances, opportunities and prospects. Vet. Parasitol., 136(2): 69–89. DOI: 10.1016/j.vetpar.2005.12.002

    Article  CAS  PubMed  Google Scholar 

  • Gibbons, L. M. (1979): Revision of the genus Haemonchus Cobb 1898 (Nematoda: Trichostrongylidae). Syst. Parasitol., 1: 3–24

    Article  Google Scholar 

  • Giudici, C. J., Cabaret, J., Durette-Desset, M. C. (1999): Description of Haemonchus placei (Place, 1893) (Nematoda, Trichostrongylidae, Haemonchinae), identification and intra-specific morphologic variability. Parasite, 6(4): 333–342

    CAS  PubMed  Google Scholar 

  • Gruner, L., Cortet, J., Sauvé, C., Hoste, H. (2004): Regulation of Teladorsagia circumcincta and Trichostrongylus colubriformis worm populations by grazing sheep with differing resistance status. Vet. Res., 35(1): 91–101. DOI: 10.1051/vetres:2003043

    Article  PubMed  Google Scholar 

  • Hall, T. A. (1999): BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids. Symp. Ser., 41: 95–98

    CAS  Google Scholar 

  • Hoberg, E. R., Lichtenfels, J. R., Gibbons, L. (2004): Phylogeny for species of Haemonchus (Nematoda: Trichostrongyloidea): considerations of their evolutionary history and global biogeography among Camelidae and Pecora (Artiodactyla). J. Parasitol., 90(5): 1085–1102

    Article  PubMed  Google Scholar 

  • Hoste, H., Torres-Acosta, J. F., Aguilar-Caballero, A. J. (2008): Nutrition-parasite interactions in goats: is immunoregulation involved in the control of gastrointestinal nematodes? Parasite Immunol., 30(2): 79–88. DOI: 10.1111/j.1365-3024.2007.00987.x

    CAS  PubMed  Google Scholar 

  • Hunt, P. W., Knox, M. R., Le Jambre, L. F., Mcnally, J., Anderson, L.J. (2008): Genetic and phenotypic differences between isolates of Haemonchus contortus in Australia. Int. J. Parasitol., 38: 885–900. DOI: 10.1016/j.ijpara.2007.11.001

    Article  CAS  PubMed  Google Scholar 

  • Jacquiet, P., Cabaret, J., Cheikh, D., Thiam, E. (1997): Identification of Haemonchus species in domestic ruminants based on morphometrics of spicules. Parasitol. Res., 83(1): 82–86

    Article  CAS  PubMed  Google Scholar 

  • Königová, A., Hrčková, G., Velebný, S., Dolinská, M., Molnár, L., Várady, M. (2012): Effect of albendazole therapy on susceptible and resistant Haemonchuscontortus larvae in Mongolian gerbils (Meriones unguiculatus) and distribution of inflammatory cells in the stomach wall. Helminthologia, 49(4): 211–220. DOI 10.2478/s11687-012-0040-z

    Article  Google Scholar 

  • Lichtenfels, J. R., Pilit, P. A., Le Jambre, L. F. (1986): Cuticular ridge patterns of Haemonchus contortus and Haemonchus placei (Nematoda: Trichostrongyloidea). Proceedings of the Helminthological Society of Washington, 53(1): 94–101

    Google Scholar 

  • Lichtenfels, J. R., Pilit, P. A., Le Jambre, L. F. (1988): Spicule lengths of the ruminant stomach nematodes Haemonchus contortus, Haemonchus placei, and their hybrids. Proceedings of the Helminthological Society of Washington, 55(1): 97–100

    Google Scholar 

  • Lichtenfels, J. R., Pilitt, P. A., Hoberg, E. P. (1994): New morphological characters for identifying individual specimens of Haemonchus spp. (Nematoda: Trichostrongyloidea) and a key to species in ruminants of North America. J. Parasitol., 80(1): 107–119

    Article  CAS  PubMed  Google Scholar 

  • Reinecke, R. K., De Villier, I. L., Joubert, G. (1982): The effect of predosing calves with Trichostrongylus axei on subsequent challenge with Haemonchus placei. Onderstepoort J. Vet. Res., 49(3): 159–161

    CAS  PubMed  Google Scholar 

  • Riggs N. L. (2001) Experimental cross-infections of Haemonchus placei (Place, 1893) in sheep and cattle. Vet. Parasitol., 94: 191–197

    Article  CAS  PubMed  Google Scholar 

  • Roberts, F. H. S., Turner, H. N., Mckevett, M. (1954): On the specific distinctness of the ovine and bovine „strains” of Haemocnhus contortus (Rudolphi) Cobb (Nematoda: Trichostrongylidae). Aus. J. Zool., 2: 275–295

    Article  Google Scholar 

  • Roepstorff, A., Nansen, P. (1998): Epidemiology, diagnosis and control of helminth parasites of swine. Rome, IT, FAO, 161 pp.

    Google Scholar 

  • Saddiqi, H. A., Jabbar, A., Sarwar, M., Iqbal, Z., Muhammad, G., Nisa, M., Shahzad, A. (2011): Small ruminant resistance against gastrointestinal nematodes: a case of Haemonchus contortus. Parasitol. Res., 109: 1483–1500. DOI: 10.1007/s00436-011-2576-0

    Article  PubMed  Google Scholar 

  • Scott, I., Sutherland, I. (2009): Gastrointestinal Nematodes of Sheep and Cattle: Biology and Control. Oxford, UK, Wiley-Blackwell, 242 pp.

    Google Scholar 

  • Stevenson, L. A., Chilton, N. B., Gasser, R. B. (1995): Differentiation of Haemonchus placei from H. contortus (Nematoda: Trichostrongylidae) by the ribosomal DNA second internal transcribed spacer. Int. J. Parasitol., 25(4): 483–488

    Article  CAS  PubMed  Google Scholar 

  • Strain, S. A., Stear, M. J. (2001): The influence of protein supplementation on the immune response to Haemonchus contortus. Parasite Immunol., 23: 527–531

    Article  CAS  PubMed  Google Scholar 

  • Šnábel, V., Königová, A., Dolinská, M., Wolstenholme, A. J., Várady, M. (2012): Allozyme analysis of Haemonchus contortus resistant and susceptible to anthelmintics, with an indication of dipeptidases associated with resistance. Helminthologia, 49(3): 128–133. DOI: 10.2478/s11687-012-0027-9

    Article  Google Scholar 

  • Taylor, M. A., Coop, R. L., Wall, R. L. (2007): Veterinary Parasitology. 3rd Edition, Oxford, UK, Blackwell Publishing, 874 pp.

    Google Scholar 

  • Terefe, G., Yacob, H. T., Grisez, C., Prevot, F., Dumas, E., Bergeaud, J. P., Dorchies, P., Hoste, H., Jacquiet, P. (2005): Haemonchus contortus egg excretion and female length reduction in sheep previously infected with Oestrus ovis (Diptera: Oestridae) larvae. Vet. Parasitol., 128(3–4): 271–283. DOI:10.1016/j.vetpar.2004.11.036

    Article  CAS  PubMed  Google Scholar 

  • Thomas, N., Teshale, S., Kumsa, B. (2007): Abomasal nematodes of sheep and goats slaughtered in Awassa (Ethiopia): species composition, prevalence and vulvar morphology. Helminthologia, 44(2): 70–75. DOI: 10.2478/s11687-007-0006-8

    Article  Google Scholar 

  • Thompson, J. D., Higgins, D. G., Gibson, T. J. (1994): CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22(22): 4673–4680

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Troell, K., Mattsson, J. G., Alderborn, A., Höglund, J. (2003): Pyrosequencing analysis identifies discrete populations of Haemonchus contortus from small ruminants. Int. J. Parasitol., 33(7): 765–771. DOI:10.1016/S0020-7519(03)00068-7

    Article  CAS  PubMed  Google Scholar 

  • van Wyk, J. A., Cabaret, J., Michael, L. M. (2004): Morphological identification of nematode larvae of small ruminants and cattle simplified. Vet. Parasitol., 119(4): 277–306. DOI:10.1016/j.vetpar.2003.11.012

    Article  PubMed  Google Scholar 

  • Várady, M., Čudeková, P., Čorba, J. (2007): In vitro detection of benzimidazole resistance in Haemonchus contortus: egg hatch test versus larval development test. Vet Parasitol., 149(1–2): 104–110. DOI: 10.1016/j.vetpar.2007.07.011

    Article  PubMed  Google Scholar 

  • Várady, M., Čorba, J., Letková, V., Kováč, G. (2009): Comparison of two versions of larval development test to detect anthelmintic resistance in Haemonchus contortus. Vet. Parasitol., 160(3–4): 267–271. DOI: 10.1016/j.vetpar.2008.11.010

    Article  PubMed  Google Scholar 

  • Zarlenga, D. S., Stringfellow, F., Nobary, M., Lichtenfels, J. R. (1994): Cloning and characterization of ribosomal RNA genes from three species of Haemonchus (Nematoda: Trichostrongyloidea) and identification of PCR primers for rapid differentiation. Exp. Parasitol., 78: 28–36

    Article  CAS  PubMed  Google Scholar 

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Vadlejch, J., Lukešová, D., Vašek, J. et al. Comparative morphological and molecular identification of Haemonchus species in sheep. Helminthologia 51, 130–140 (2014). https://doi.org/10.2478/s11687-014-0220-0

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  • DOI: https://doi.org/10.2478/s11687-014-0220-0

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