Comparative morphological and molecular identification of Haemonchus species in sheep

[1] 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 http://dx.doi.org/10.1016/S0304-4017(03)00258-910.1016/S0304-4017(03)00258-9Search in Google Scholar

[2] 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 http://dx.doi.org/10.1016/S0304-4017(03)00259-010.1016/S0304-4017(03)00259-0Search in Google Scholar

[3] 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 http://dx.doi.org/10.2478/s11687-010-0042-710.2478/s11687-010-0042-7Search in Google Scholar

[4] 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 http://dx.doi.org/10.1111/j.0014-3820.2004.tb01742.x10.1111/j.0014-3820.2004.tb01742.xSearch in Google Scholar

[5] 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 http://dx.doi.org/10.1016/S0020-7519(97)00125-210.1016/S0020-7519(97)00125-2Search in Google Scholar

[6] 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 http://dx.doi.org/10.1016/j.ijpara.2012.03.00310.1016/j.ijpara.2012.03.00322787588Search in Google Scholar

[7] 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 http://dx.doi.org/10.1071/ZO955031210.1071/ZO9550312Search in Google Scholar

[8] 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 http://dx.doi.org/10.1006/mpev.2001.093810.1006/mpev.2001.093811399147Search in Google Scholar

[9] 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 http://dx.doi.org/10.1111/j.1365-294X.2005.02587.x10.1111/j.1365-294X.2005.02587.x15969711Search in Google Scholar

[10] do Amarante, A.F. (2011): Why is it important to correctly identify Haemonchus species? Rev. Bras. Parasitol. Vet., 20(4): 263–268 http://dx.doi.org/10.1590/S1984-2961201100040000210.1590/S1984-29612011000400002Search in Google Scholar

[11] Gasser, R. B. (2006): Molecular tools—advances, opportunities and prospects. Vet. Parasitol., 136(2): 69–89. DOI: 10.1016/j.vetpar.2005.12.002 http://dx.doi.org/10.1016/j.vetpar.2005.12.00210.1016/j.vetpar.2005.12.00216457951Search in Google Scholar

[12] Gibbons, L. M. (1979): Revision of the genus Haemonchus Cobb 1898 (Nematoda: Trichostrongylidae). Syst. Parasitol., 1: 3–24 http://dx.doi.org/10.1007/BF0000977110.1007/BF00009771Search in Google Scholar

[13] 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 10.1051/parasite/199906433310633504Search in Google Scholar

[14] 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 http://dx.doi.org/10.1051/vetres:200304310.1051/vetres:2003043Search in Google Scholar

[15] 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 Search in Google Scholar

[16] 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 http://dx.doi.org/10.1645/GE-330910.1645/GE-330915562609Search in Google Scholar

[17] 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 10.1111/j.1365-3024.2007.00987.x18186768Search in Google Scholar

[18] 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 http://dx.doi.org/10.1016/j.ijpara.2007.11.00110.1016/j.ijpara.2007.11.00118068173Search in Google Scholar

[19] 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 http://dx.doi.org/10.1007/s00436005021310.1007/s0043600502139000240Search in Google Scholar

[20] 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 http://dx.doi.org/10.2478/s11687-012-0040-z10.2478/s11687-012-0040-zSearch in Google Scholar

[21] 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 Search in Google Scholar

[22] 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 Search in Google Scholar

[23] 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 http://dx.doi.org/10.2307/328335310.2307/3283353Search in Google Scholar

[24] 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 Search in Google Scholar

[25] Riggs N. L. (2001) Experimental cross-infections of Haemonchus placei (Place, 1893) in sheep and cattle. Vet. Parasitol., 94: 191–197 http://dx.doi.org/10.1016/S0304-4017(00)00381-210.1016/S0304-4017(00)00381-2Search in Google Scholar

[26] 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 http://dx.doi.org/10.1071/ZO954027510.1071/ZO9540275Search in Google Scholar

[27] Roepstorff, A., Nansen, P. (1998): Epidemiology, diagnosis and control of helminth parasites of swine. Rome, IT, FAO, 161 pp. Search in Google Scholar

[28] 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 http://dx.doi.org/10.1007/s00436-011-2576-010.1007/s00436-011-2576-0Search in Google Scholar

[29] Scott, I., Sutherland, I. (2009): Gastrointestinal Nematodes of Sheep and Cattle: Biology and Control. Oxford, UK, Wiley-Blackwell, 242 pp. Search in Google Scholar

[30] 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 http://dx.doi.org/10.1016/0020-7519(94)00156-I10.1016/0020-7519(94)00156-ISearch in Google Scholar

[31] Strain, S. A., Stear, M. J. (2001): The influence of protein supplementation on the immune response to Haemonchus contortus. Parasite Immunol., 23: 527–531 http://dx.doi.org/10.1046/j.1365-3024.2001.00410.x10.1046/j.1365-3024.2001.00410.xSearch in Google Scholar

[32] 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 http://dx.doi.org/10.2478/s11687-012-0027-910.2478/s11687-012-0027-9Search in Google Scholar

[33] Taylor, M. A., Coop, R. L., Wall, R. L. (2007): Veterinary Parasitology. 3rd Edition, Oxford, UK, Blackwell Publishing, 874 pp. Search in Google Scholar

[34] 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 http://dx.doi.org/10.1016/j.vetpar.2004.11.03610.1016/j.vetpar.2004.11.036Search in Google Scholar

[35] 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 http://dx.doi.org/10.2478/s11687-007-0006-810.2478/s11687-007-0006-8Search in Google Scholar

[36] 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 http://dx.doi.org/10.1093/nar/22.22.467310.1093/nar/22.22.4673Search in Google Scholar

[37] 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 http://dx.doi.org/10.1016/S0020-7519(03)00068-710.1016/S0020-7519(03)00068-7Search in Google Scholar

[38] 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 http://dx.doi.org/10.1016/j.vetpar.2003.11.01210.1016/j.vetpar.2003.11.01215154594Search in Google Scholar

[39] 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 http://dx.doi.org/10.1016/j.vetpar.2007.07.01110.1016/j.vetpar.2007.07.01117697753Search in Google Scholar

[40] 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 http://dx.doi.org/10.1016/j.vetpar.2008.11.01010.1016/j.vetpar.2008.11.01019110379Search in Google Scholar

[41] 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 http://dx.doi.org/10.1006/expr.1994.100310.1006/expr.1994.10038299758Search in Google Scholar