Variation in allele frequencies in benzimidazole resistant and susceptible isolates of Haemonchus contortus during patent infection in lambs
- EU Regulation
- January 23, 2023
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Flay, K. J., Fraser, I. H. & Muguiro, D. H. A review: Haemonchus contortus infection in pasture-based sheep production systems, with a focus on the pathogenesis of anaemia and changes in haematological parameters. Animals 12, 1238. https://doi.org/10.3390/ani12101238
Amarante, A. F. T., Bagnola, J., Amarante, M. R. V. & Barbosa, M. A. Host specificity of sheep and cattle nematodes in Sao Paulo state, Brazil. Vet. Parasitol. 73, 89–104. https://doi.org/10.1016/s0304-4017(97)00036-8 (1997).
Papadopoulos, E., Gallidis, E. & Ptochos, S. Anthelmintic resistance in sheep in Europe: A selected review. Vet. Parasitol. 189, 85–88. https://doi.org/10.1016/j.vetpar.2012.03.036 (2012).
Rose Vineer, H. et al. Increasing importance of anthelmintic resistance in European livestock: Creation and meta-analysis of an open database. Parasite 27, 69. https://doi.org/10.1051/parasite/2020062 (2020).
Martin, P. J., Anderson, N. & Jarrett, R. G. Detecting benzimidazole resistance with faecal egg count reduction tests and in vitro assays. Aust. Vet. J. 66, 236–240. https://doi.org/10.1111/j.1751-0813.1989.tb13578.x (1989).
Várady, M., Čudeková, P. & Čorba, J. In vitro detection of benzimidazole resistance in Haemonchus contortus: egg hatch test versus larval development test. Vet. Parasitol. 149, 104–110. https://doi.org/10.1016/j.vetpar.2007.07.011 (2007).
Borgsteede, F. H. M. & Couwenberg, T. Changes in LC50 in an in vitro egg development assay during the patent period of Haemonchus contortus in sheep. Res. Vet. Sci. 42, 413–414 (1987).
Kerboeuf, D. & Hubert, J. Changes in the response of Haemonchus contortus eggs to the ovicidal activity of thiabendazole during the course of infection. Ann. Rech. Vet. 18, 365–370 (1987).
Várady, M., Praslička, J. & Čorba, J. Changes of ED50 in in vitro egg hatch assays for detection of benzimidazole and levamisole resistance of Haemonchus contortus and Ostertagia circumcinta in lambs. Helminthologia 32, 219–223 (1995).
von Samson-Himmelstjerna, G. et al. Molecular detection of benzimidazole resistance in Haemonchus contortus using real-time PCR and pyrosequencing. Parasitology 136, 349–358. https://doi.org/10.1017/S003118200800543X (2009).
Lacey, E. The role of the cytoskeletal protein, tubulin, in the mode of action and mechanism of drug resistance to benzimidazoles. Int. J. Parasitol. 18, 885–936. https://doi.org/10.1016/0020-7519(88)90175-0 (1988).
Kwa, M. S. G., Kooyman, F. N. J., Boersema, J. H. & Roos, M. H. Effect of selection for benzimidazole resistance in Haemonchus contortus on beta-tubulin isotype 1 and isotype 2 genes. Biochem. Biophys. Res. Commun. 191, 413–419. https://doi.org/10.1006/bbrc.1993.1233 (1993).
Silvestre, A. & Cabaret, J. Mutation in position 167 of isotype 1 beta-tubulin gene of Trichostrongylid nematodes: Role in benzimidazole resistance? Mol. Biochem. Parasitol. 120, 297–300. https://doi.org/10.1016/s0166-6851(01)00455-8 (2002).
Mottier, M. L. & Prichard, R. K. Genetic analysis of a relationship between macrocyclic lactone and benzimidazole anthelmintic selection on Haemonchus contortus. Pharmacogenet. Genom. 18, 129–140. https://doi.org/10.1097/FPC.0b013e3282f4711d (2008).
Ghisi, M., Kaminsky, R. & Mäser, P. Phenotyping and genotyping of Haemonchus contortus isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes. Vet. Parasitol. 144, 313–320. https://doi.org/10.1016/j.vetpar.2006.10.003 (2007).
Avramenko, R. W. et al. Deep amplicon sequencing as a powerful new tool to screen for sequence polymorphisms associated with anthelmintic resistance in parasitic nematode populations. Int. J. Parasitol. 49, 13–26. https://doi.org/10.1016/j.ijpara.2018.10.005 (2019).
Martínez-Valladares, M. et al. Teladorsagia circumcincta beta tubulin: the presence of the E198L polymorphism on its own is associated with benzimidazole resistance. Parasit. Vectors 13, 453. https://doi.org/10.1186/s13071-020-04320-x (2020).
Mohammedsalih, K. M. et al. New codon 198 β-tubulin polymorphisms in highly benzimidazole resistant Haemonchus contortus from goats in three different states in Sudan. Parasit. Vectors 13, 114. https://doi.org/10.1186/s13071-020-3978-6 (2020).
Mohammedsalih, K. M. et al. Susceptible trichostrongyloid species mask presence of benzimidazole-resistant Haemonchus contortus in cattle. Parasit. Vectors 14, 101. https://doi.org/10.1186/s13071-021-04593-w (2021).
Redman, E. et al. The emergence of resistance to the benzimidazole anthlemintics in parasitic nematodes of livestock is characterised by multiple independent hard and soft selective sweeps. PLoS Negl. Trop. Dis. 9, e0003494. https://doi.org/10.1371/journal.pntd.0003494 (2015).
Baltrušis, P., Komáromyová, M., Várady, M., von Samson-Himmelstjerna, G. & Höglund, J. Assessment of the F200Y mutation frequency in the β tubulin gene of Haemonchus contortus following the exposure to a discriminating concentration of thiabendazole in the egg hatch test. Exp. Parasitol. 217, 107957. https://doi.org/10.1016/j.exppara.2020.107957 (2020).
Hinney, B. et al. High frequency of benzimidazole resistance alleles in trichostrongyloids from Austrian sheep flocks in an alpine transhumance management system. BMC Vet. Res. 16, 132. https://doi.org/10.1186/s12917-020-02353-z (2020).
Höglund, J. et al. Anthelmintic resistance in Swedish sheep flocks based on a comparison of the results from the faecal egg count reduction test and resistant allele frequencies of the beta-tubulin gene. Vet. Parasitol. 161, 60–68. https://doi.org/10.1016/j.vetpar.2008.12.001 (2009).
Kwa, M. S. G., Veenstra, J. G. & Roos, M. H. Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in beta-tubulin isotype 1. Mol. Biochem. Parasitol. 63, 299–303. https://doi.org/10.1016/0166-6851(94)90066-3 (1994).
Kotze, A. C. & Prichard, R. K. Anthelmintic Resistance in Haemonchus contortus: History, mechanisms and diagnosis. Adv. Parasitol. 93, 397–428. https://doi.org/10.1016/bs.apar.2016.02.012 (2016).
Várady, M. & Čorba, J. Changes in LD50 value in an in vitro larval development test for the detection of susceptibility to a thiabendazole, levamisole, morantel and pyrantel in Oesophagostomum dentatum. Helminthologia 40, 211–215 (2003).
Baltrušis, P., Halvarsson, P. & Höglund, J. Exploring benzimidazole resistance in Haemonchus contortus by next generation sequencing and droplet digital PCR. Int. J. Parasitol. Drugs Drug. Resist. 8, 411–419. https://doi.org/10.1016/j.ijpddr.2018.09.003 (2018).
Gilleard, J. S. & Redman, E. Genetic diversity and population structure of haemonchus contortus. Adv. Parasitol. 93, 31–68. https://doi.org/10.1016/bs.apar.2016.02.009 (2016).
Dineen, J. K. & Wagland, B. M. The dynamics of the host-parasite relationship. IV. The response of sheep to graded and to repeated infection with Haemonchus contortus. Parasitology 56, 639–650. https://doi.org/10.1017/s0031182000071663 (1966).
Cringoli, G. et al. Gastrointestinal strongyle Faecal Egg Count in goats: circadian rhythm and relationship with worm burden. Vet. Res. Commun. 32, 191–193. https://doi.org/10.1007/s11259-008-9163-6 (2008).
Rinaldi, L. et al. Is gastrointestinal strongyle faecal egg count influenced by hour of sample collection and worm burden in goats? Vet. Parasitol. 163, 81–86. https://doi.org/10.1016/j.vetpar.2009.03.043 (2009).
Coyne, M. J., Smith, G. & Johnstone, C. A study of the mortality and fecundity of Haemonchus contortus in sheep following experimental infections. Int. J. Parasitol. 21, 847–853. https://doi.org/10.1016/0020-7519(91)90153-x (1991).
Barger, I. A. & Le Jambre, L. F. Regulation of Haemonchus contortus populations in sheep: mortality of established worms. Int. J. Parasitol. 18, 269–273. https://doi.org/10.1016/0020-7519(88)90067-7 (1988).
Čudeková, P., Várady, M., Dolinská, M. & Königová, A. Phenotypic and genotypic characterisation of benzimidazole susceptible and resistant isolates of Haemonchus contortus. Vet. Parasitol. 172, 155–159. https://doi.org/10.1016/j.vetpar.2010.04.022 (2010).
Redman, E. et al. Microsatellite analysis reveals marked genetic differentiation between Haemonchus contortus laboratory isolates and provides a rapid system of genetic fingerprinting. Int. J. Parasitol. 38, 111–122. https://doi.org/10.1016/j.ijpara.2007.06.008 (2008).
van Wyk, J. A. & Malan, F. S. Resistance of field strains of Haemonchus contortus to ivermectin, closantel, rafoxanide and the benzimidazoles in South Africa. Vet. Rec. 123, 226–228. https://doi.org/10.1136/vr.123.9.226 (1988).
Ministry of Agriculture, Fisheries and Food. Manual of Veterinary Parasitological Techniques, Reference Book. Her Majesty’s Stationary Office, London. pp 159 (1986).
