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Evaluation of benzimidazole resistance status in Ascaridia galli

Published online by Cambridge University Press:  18 May 2017

B. TARBIAT*
Affiliation:
Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences (SLU), P.O. Box 7036 SE-750 07, Uppsala, Sweden
D. S. JANSSON
Affiliation:
Department of Animal Health and Antimicrobial Strategies, National Veterinary Institute (SVA), SE-751 89 Uppsala, Sweden
E. TYDÉN
Affiliation:
Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences (SLU), P.O. Box 7036 SE-750 07, Uppsala, Sweden
J. HÖGLUND
Affiliation:
Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences (SLU), P.O. Box 7036 SE-750 07, Uppsala, Sweden
*
*Corresponding author: Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences (SLU), P.O. Box 7036, SE-750 07, Uppsala, Sweden. E-mail: [email protected]

Summary

Susceptability of Ascaridia galli to benzimidazole (BZ) was investigated using faecal egg count reduction test (FECRT), in ovo larval development test (LDT) and genetic markers (mutations at codons 167, 198 and 200 of β-tubulin gene). Six flocks (F1−F6) of a commercial laying hen farm with different number of exposure to BZ were recruited. The FECR was calculated by analyzing individual faeces (F1, F2, F4 and F5) before and 10 days after treatment. The LDT was performed on parasite eggs from pooled samples from F1 to F6 and LC50 and LC99 were calculated. DNA was extracted from 120 worms and sequenced for β-tubulin gene. In all flocks, the FECRs were above 95% (lower CI above 90%). No significant difference was observed (p > 0·05) among obtained LC50 (F1/F4 and F2/F5 vs F3/F6) in the LDT. However, LC50 and LC99 were higher than suggested values for declaration of resistance in other nematode species. No variation was observed in codon positions involved in BZ resistance. Overall, our results indicated lack of evidence of resistance to BZ in A. galli. More research is needed to confirm these results and to further optimize the existing tools for detection and monitoring of anthelmintic resistance in A. galli.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Ancheta, P. B., Dumilon, R. A., Venturina, V. M., Cerbito, W. A., Dobson, R. J., LeJambre, L. F., Villar, E. C. and Gray, G. D. (2004). Efficacy of benzimidazole anthelmintics in goats and sheep in the Philippines using a larval development assay. Veterinary Parasitology 120, 107121.Google Scholar
Calvete, C. and Uriarte, J. (2013). Improving the detection of anthelmintic resistance: evaluation of faecal egg count reduction test procedures suitable for farm routines. Veterinary Parasitology 196, 438452.CrossRefGoogle ScholarPubMed
Coles, G. C. (2002). Cattle nematodes resistant to anthelmintics: why so few cases? Veterinary Research 33, 481489.Google Scholar
Coles, G. C. (2005). Anthelmintic resistance – looking to the future: a UK perspective. Research in Veterinary Science 78, 99108.Google Scholar
Coles, G. C., Bauer, C., Borgsteede, F. H., Geerts, S., Klei, T. R., Taylor, M. A. and Waller, P. J. (1992). World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology 44, 3544.Google Scholar
Coles, G. C., Jackson, F., Pomroy, W. E., Prichard, R. K., von Samson-Himmelstjerna, G., Silvestre, A., Taylor, M. A. and Vercruysse, J. (2006). The detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology 136, 167185.Google Scholar
Crook, E. K., O'Brien, D. J., Howell, S. B., Storey, B. E., Whitley, N. C., Burke, J. M. and Kaplan, R. M. (2016). Prevalence of anthelmintic resistance on sheep and goat farms in the mid-Atlantic region and comparison of in vivo and in vitro detection methods. Small Ruminant Research 143, 8996.Google Scholar
Daş, G. and Gauly, M. (2014). Response to Ascaridia galli infection in growing chickens in relation to their body weight. Parasitology Research 113, 19851988.Google Scholar
Ferdushy, T., Luna-Olivares, L. A., Nejsum, P., Thamsborg, S. M. and Kyvsgaard, N. C. (2015). The use of genetically marked infection cohorts to study changes in establishment rates during the time course of a repeated Ascaridia galli infection in chickens. International Journal for Parasitology 45, 393398.Google Scholar
Foreyt, W. J. (2001). Veterinary Parasitology Reference Manual, 5th Edn. Blackwell Publishing, UK.Google Scholar
Geurden, T., Hoste, H., Jacquiet, P., Traversa, D., Sotiraki, S., Frangipane di Regalbono, A., Tzanidakis, N., Kostopoulou, D., Gaillac, C., Privat, S., Giangaspero, A., Zanardello, C., Noé, L., Vanimisetti, B. and Bartram, D. (2014). Anthelmintic resistance and multidrug resistance in sheep gastro-intestinal nematodes in France, Greece and Italy. Veterinary Parasitology 201, 5966.Google Scholar
Ghisi, M., Kaminsky, R. and Mäser, P. (2007). Phenotyping and genotyping of Haemonchus contortus isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes. Veterinary Parasitology 144, 313320.CrossRefGoogle ScholarPubMed
Gill, J. H., Redwin, J. M. and Van Wyk, J. A. and Lacey, E. (1995). Avermectin inhibition of larval development in Haemonchus contortus — effects of ivermectin resistance. International Journal for Parasitology 25, 463470.CrossRefGoogle ScholarPubMed
Girma, K. (2016). Försäljning av djurläkemedel 2015 (Swedish Board of Agriculture Djurskydd och hälsa).Google Scholar
Howell, S. B., Burke, J. M., Miller, J. E., Terrill, T. H., Valencia, E., Williams, M. J., Williamson, L. H., Zajac, A. M. and Kaplan, R. M. (2008). Prevalence of anthelmintic resistance on sheep and goat farms in the southeastern United States. Journal of the American Veterinary Medical Association 233, 19131919.Google Scholar
Hubert, J. and Kerboeuf, D. (1992). A microlarval development assay for the detection of anthelmintic resistance in sheep nematodes. Veterinary Record 130, 442446.Google Scholar
James, C. E., Hudson, A. L. and Davey, M. W. (2009). Drug resistance mechanisms in helminths: is it survival of the fittest? Trends in Parasitology 25, 328335.Google Scholar
Kaplan, R. M. (2002). Anthelmintic resistance in nematodes of horses. Veterinary Research 33, 491507.Google Scholar
Kaplan, R. M. and Vidyashankar, A. N. (2012). An inconvenient truth: global worming and anthelmintic resistance. Veterinary Parasitology 186, 7078.CrossRefGoogle ScholarPubMed
Knapp-Lawitzke, F., Krücken, J., Ramünke, S., von Samson-Himmelstjerna, G. and Demeler, J. (2015). Rapid selection for β-tubulin alleles in codon 200 conferring benzimidazole resistance in an Ostertagia ostertagi isolate on pasture. Veterinary Parasitology 209, 8492.Google Scholar
Kotze, A. C., Hunt, P. W., Skuce, P., von Samson-Himmelstjerna, G., Martin, R. J., Sager, H., Krücken, J., Hodgkinson, J., Lespine, A., Jex, A. R., Gilleard, J. S., Beech, R. N., Wolstenholme, A. J., Demeler, J., Robertson, A. P., Charvet, C. L., Neveu, C., Kaminsky, R., Rufener, L., Alberich, M., Menez, C. and Prichard, R. K. (2014). Recent advances in candidate-gene and whole-genome approaches to the discovery of anthelmintic resistance markers and the description of drug/receptor interactions. International Journal for Parasitology: Drugs and Drug Resistance 4, 164184.Google Scholar
Kwa, M. S. G., Veenstra, J. G. and Roos, M. H. (1994). Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in β-tubulin isotype 1. Molecular and Biochemical Parasitology 63, 299303.CrossRefGoogle ScholarPubMed
Lacey, E. (1988). The role of the cytoskeletal protein, tubulin, in the mode of action and mechanism of drug resistance to benzimidazoles. International Journal for Parasitology 18, 885936.CrossRefGoogle ScholarPubMed
Lespine, A., Ménez, C., Bourguinat, C. and Prichard, R. K. (2012). P-glycoproteins and other multidrug resistance transporters in the pharmacology of anthelmintics: prospects for reversing transport-dependent anthelmintic resistance. International Journal for Parasitology: Drugs and Drug Resistance 2, 5875.Google Scholar
Levecke, B., Dobson, R. J., Speybroeck, N., Vercruysse, J. and Charlier, J. (2012). Novel insights in the faecal egg count reduction test for monitoring drug efficacy against gastrointestinal nematodes of veterinary importance. Veterinary Parasitology 188, 391396.Google Scholar
Lubega, G. W. and Prichard, R. K. (1991). Interaction of benzimidazole anthelmintics with Haemonchus contortus tubulin: binding affinity and anthelmintic efficacy. Experimental Parasitology 73, 203213.CrossRefGoogle ScholarPubMed
McKenna, P. B. (2006). A comparison of faecal egg count reduction test procedures. New Zealand Veterinary Journal 54, 202203.CrossRefGoogle ScholarPubMed
Prichard, R. (1994). Anthelmintic resistance. Veterinary Parasitology 54, 259268.CrossRefGoogle ScholarPubMed
Prichard, R. (2001). Genetic variability following selection of Haemonchus contortus with anthelmintics. Trends in Parasitology 17, 445453.Google Scholar
Rinaldi, L., Morgan, E. R., Bosco, A., Coles, G. C. and Cringoli, G. (2014). The maintenance of anthelmintic efficacy in sheep in a Mediterranean climate. Veterinary Parasitology 203, 139143.CrossRefGoogle Scholar
Robinson, D. N. and Spudich, J. A. (2004). Mechanics and regulation of cytokinesis. Current Opinion in Cell Biology 16, 182188.Google Scholar
Saunders, G. I., Wasmuth, J. D., Beech, R., Laing, R., Hunt, M., Naghra, H., Cotton, J. A., Berriman, M., Britton, C. and Gilleard, J. S. (2013). Characterization and comparative analysis of the complete Haemonchus contortus β-tubulin gene family and implications for benzimidazole resistance in strongylid nematodes. International Journal for Parasitology 43, 465475.Google Scholar
Silvestre, A. and Cabaret, J. (2002). Mutation in position 167 of isotype 1 β-tubulin gene of Trichostrongylid nematodes: role in benzimidazole resistance? Molecular and Biochemical Parasitology 120, 297300.CrossRefGoogle ScholarPubMed
Tarbiat, B., Jansson, D. S. and Höglund, J. (2015). Environmental tolerance of free-living stages of the poultry roundworm Ascaridia galli . Veterinary Parasitology 209, 101107.Google Scholar
Tarbiat, B., Jansson, D. S., Moreno, L., Lanusse, C., Nylund, M., Tydén, E. and Höglund, J. (2016 a). The efficacy of flubendazole against different developmental stages of the poultry roundworm Ascaridia galli in laying hens. Veterinary Parasitology 218, 6672.Google Scholar
Tarbiat, B., Jansson, D. S., Tydén, E. and Höglund, J. (2016 b). Comparison between anthelmintic treatment strategies against Ascaridia galli in commercial laying hens. Veterinary Parasitology 226, 109115.Google Scholar
Terrill, T. H., Kaplan, R. M., Larsen, M., Samples, O. M., Miller, J. E., Gelaye, S. (2001). Anthelmintic resistance on goat farms in Georgia: efficacy of anthelmintics against gastrointestinal nematodes in two selected goat herds. Veterinary Parasitology 97, 261268.Google Scholar
Thapa, S., Hinrichsen, L. K., Brenninkmeyer, C., Gunnarsson, S., Heerkens, J. L. T., Verwer, C., Niebuhr, K., Willett, A., Grilli, G., Thamsborg, S. M., Sørensen, J. T. and Mejer, H. (2015). Prevalence and magnitude of helminth infections in organic laying hens (Gallus gallus domesticus) across Europe. Veterinary Parasitology 214, 118124.Google Scholar
Tydén, E., Engström, A., Morrison, D. A. and Höglund, J. (2013). Sequencing of the β-tubulin genes in the ascarid nematodes Parascaris equorum and Ascaridia galli . Molecular and Biochemical Parasitology 190, 3843.Google Scholar
Tydén, E., Skarin, M., Andersson-Franko, M., Sjöblom, M. and Höglund, J. (2016). Differential expression of β-tubulin isotypes in different life stages of Parascaris spp after exposure to thiabendazole. Molecular and Biochemical Parasitology 205, 2228.Google Scholar
van Wyk, J. A. (2001). Refugia--overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance. Onderstepoort J Vet Res 68, 5567.Google Scholar
Várady, M., Čerňanská, D. and Čorba, J. (2006). Use of two in vitro methods for the detection of anthelmintic resistant nematode parasites on Slovak sheep farms. Veterinary Parasitology 135, 325331.Google Scholar
Várady, M., Čudeková, P. and Čorba, J. (2007). In vitro detection of benzimidazole resistance in Haemonchus contortus: egg hatch test versus larval development test. Veterinary Parasitology 149, 104110.Google Scholar
Vidyashankar, A. N., Hanlon, B. M. and Kaplan, R. M. (2012). Statistical and biological considerations in evaluating drug efficacy in equine strongyle parasites using fecal egg count data. Veterinary Parasitology 185, 4556.CrossRefGoogle ScholarPubMed
Williamson, S. M., Storey, B., Howell, S., Harper, K. M., Kaplan, R. M. and Wolstenholme, A. J. (2011). Candidate anthelmintic resistance-associated gene expression and sequence polymorphisms in a triple-resistant field isolate of Haemonchus contortus . Molecular and Biochemical Parasitology 180, 99105.Google Scholar
Yazwinski, T. A., Chapman, H. D., Davis, R. B., Letonja, T., Pote, L., Maes, L., Vercruysse, J. and Jacobs, D. E. (2003). World Association for the Advancement of Veterinary Parasitology (WAAVP) guidelines for evaluating the effectiveness of anthelmintics in chickens and turkeys. Veterinary Parasitology 116, 159173.Google Scholar