Skip to main content Accessibility help
×
Home

Identification of putative markers of triclabendazole resistance by a genome-wide analysis of genetically recombinant Fasciola hepatica

  • J. HODGKINSON (a1), K. CWIKLINSKI (a1), N. J. BEESLEY (a1), S. PATERSON (a2) and D. J. L. WILLIAMS (a1)...

Summary

Despite years of investigation into triclabendazole (TCBZ) resistance in Fasciola hepatica, the genetic mechanisms responsible remain unknown. Extensive analysis of multiple triclabendazole-susceptible and -resistant isolates using a combination of experimental in vivo and in vitro approaches has been carried out, yet few, if any, genes have been demonstrated experimentally to be associated with resistance phenotypes in the field. In this review we summarize the current understanding of TCBZ resistance from the approaches employed to date. We report the current genomic and genetic resources for F. hepatica that are available to facilitate novel functional genomics and genetic experiments for this parasite in the future. Finally, we describe our own non-biased approach to mapping the major genetic loci involved in conferring TCBZ resistance in F. hepatica.

Copyright

Corresponding author

*Corresponding author. Veterinary Parasitology, Department of Infection Biology, Institute of Infection and Global Health, University of Liverpool, Liverpool, L3 5RF, UK. Tel: +44 (0)151 7950223. E-mail: jhodgkin@liverpool.ac.uk

References

Hide All
Alasaad, S., Li, Q. Y., Lin, Q., Martín-Atance, P., Granados, J. E., Díez-Baños, P., Pérez, J. M. and Zhu, X. Q. (2008). Genetic variability among Fasciola hepatica samples from different host species and geographical localities in Spain revealed by the novel SRAP marker. Parasitology Research 103, 181186. doi: 10.1007/s00436-008-0952-1.
Aldemir, O. S. (2006). Differentiation of cattle and sheep originated Fasciola hepatica by RAPD-PCR. Revue de Médecine Vétérinaire 157, 6567.
Ali, H., Ai, L., Song, H. Q., Ali, S., Lin, R. Q., Seyni, B., Issa, G. and Zhu, X. Q. (2008). Genetic characterisation of Fasciola samples from different host species and geographical localities revealed the existence of F. hepatica and F. gigantica in Niger. Parasitology Research 102, 10211024. doi: 10.1007/s00436-007-0870-7.
Alvarez, L. L., Solana, H. D., Mottier, M. L., Virkel, G. L., Fairweather, I. and Lanusse, C. E. (2005). Altered drug influx/efflux and enhanced metabolic activity in triclabendazole-resistant liver flukes. Parasitology 131, 501510. doi: 10.1017/S0031182005007997.
Alvarez-Sanchez, M. A., Mainar-Jaime, R. C., Perez-Garcia, J. and Rojo-Vazquez, F. A. (2006). Resistance of Fasciola hepatica to triclabendazole and albendazole in sheep in Spain. Veterinary Record 159, 424425. doi: 10.1136/vr.159.13.424.
Backeljau, T., De Bruyn, L., De Wolf, H., Jordaens, K., Van Dongen, S., Verhagen, R. and Winnepenninckx, B. (1995). Random amplified polymorphic DNA (RAPD) and parsimony methods. Cladistics 11, 119130. doi: 10.1111/j.1096-0031.1995.tb00083.x.
Beveridge, I. (1998). Allozyme electrophoresis – difficulties encountered in studies on helminths. International Journal for Parasitology 28, 973979. doi: 10.1016/S0020-7519(98)00047-2.
Boray, J. C. (1990). Drug resistance in Fasciola hepatica. In Resistance of Parasites to Antiparasitic Drugs (ed. Boray, J. C., Martin, P. J. and Roush, R. T.), pp. 5160. MSD AGVET, Rahway, NJ.
Brennan, G. P., Fairweather, I., Trudgett, A., Hoey, E., McCoy, , McConville, M., Meaney, M., Robinson, M., McFerran, N., Ryan, L., Lanusse, C., Mottier, L., Alvarez, L., Solana, H., Virkel, G. and Brophy, P. M. (2007). Understanding triclabendazole resistance. Experimental and Molecular Pathology 82, 104109. doi: 10.1016/jyexmp.2007.01.009X.
Cantacessi, C., Hofmann, A., Young, N. D., Broder, U., Hall, R. S., Loukas, A. and Gasser, R. B. (2012). Insights into SCP/TAPS proteins of liver flukes based on large-scale bioinformatic analyses of sequence datasets. PLoS ONE 7, e31164. doi: 10.1371/journal.pone.0031164.
Charlier, J., Hostens, M., Jacobs, J., Van Ranst, B., Duchateau, L. and Vercruysse, J. (2012). Integrating fasciolosis control in the dry cow management: the effect of closantel treatment on milk production. PLoS ONE 7, 8. doi: 10.1371/journal.pone.0043216.
Chemale, G., Perally, S., LaCourse, E. J., Prescott, M. C., Jones, L. M., Ward, D., Meaney, M., Hoey, E., Brennan, G. P., Fairweather, I., Trudgett, A. and Brophy, P. M. (2010). Comparative proteomic analysis of triclabendazole response in the liver fluke Fasciola hepatica. Journal of Proteome Research 9, 49404951. doi: 10.1021/pr1000785.
Claridge, J., Diggle, P., McCann, C. M., Mulcahy, G., Flynn, R., McNair, J., Strain, S., Welsh, M., Baylis, M. and Williams, D. J. (2012). Fasciola hepatica is associated with the failure to detect bovine tuberculosis in dairy cattle. Nature Communications 3, 853. doi: 10.1038/ncomms1840.
Coles, G. C., Rhodes, A. C. and Stafford, K. A. (2000). Activity of closantel against triclabendazole-resistant Fasciola hepatica. Veterinary Record 146, 504. doi: 10.1136/vr.146.17.504-a.
Coles, G. C. and Stafford, K. A. (2001). Activity of oxyclozanide, nitroxynil, clorsulon and albendazole against adult triclabendazole-resistant Fasciola hepatica. Veterinary Record 148, 723724. doi: 10.1136/vr.148.23.723.
Dabo, A., Durand, P., Morand, S., Diakite, M., Langand, J., Imbert-Establet, D., Doumbo, O. and Jourdane, J. (1997). Distribution and genetic diversity of Schistosoma haematobium within its bulinid intermediate hosts in Mali. Acta Tropica 66, 1526. doi: 10.1016/S0001-706X(97)00670-0.
Daniel, R., van Dijk, J., Jenkins, T., Akca, A., Mearns, R. and Williams, D. J. L. (2012). A composite faecal egg count reduction test to detect resistance to tricalbendazole in Fasciola hepatica. Veterinary Record 171, 153. doi: 10.1136/vr.100588.
Dar, Y., Amer, S., Courtioux, B. and Dreyfuss, G. (2011). Microsatellite analysis of Fasciola spp. in Egypt. Parasitology Research 109, 17411744. doi: 10.1007/s00436-011-2520-3.
Devaney, E., Winter, A. D. and Britton, C. (2010). microRNAs: a role in drug resistance in parasitic nematodes? Trends in Parasitology 26, 428433. doi: 10.1016/j.pt.2010.05.003.
Devine, C., Brennan, G. P., Lanusse, C. E., Alvarez, L. I., Trudgett, A., Hoey, E. and Fairweather, I. (2010 a). Enhancement of the drug susceptibility of a triclabendazole-resistant isolate of Fasciola hepatica using the metabolic inhibitor ketoconazole. Parasitology Research 107, 337353. doi: 10.1007/s00436-010-1866-2.
Devine, C., Brennan, G. P., Lanusse, C. E., Alvarez, L. I., Trudgett, A., Hoey, E. and Fairweather, I. (2010 b). Potentiation of triclabendazole sulphoxide-induced tegumental disruption by methimazole in a triclabendazole-resistant isolate of Fasciola hepatica. Parasitology Research 106, 13511363. doi: 10.1007/s00436-010-1806-1.
Devine, C., Brennan, G. P., Lanusse, C. E., Alvarez, L. I., Trudgett, A., Hoey, E. and Fairweather, I. (2011). Erratum to: inhibition of triclabendazole metabolism in vitro by ketoconazole increases disruption to the tegument of a triclabendazole-resistant isolate of Fasciola hepatica. Parasitology Research 109, 12091223. doi: 10.1007/s00436-011-2554-6.
Devine, C., Brennan, G. P., Lanusse, C. E., Alvarez, L. I., Trudgett, A., Hoey, E. and Fairweather, I. (2012). Potentiation of triclabendazole action in vivo against a triclabendazole-resistant isolate of Fasciola hepatica following its co-administration with the metabolic inhibitor, ketoconazole. Veterinary Parasitology 184, 3747. doi: 10.1016/j.vetpar.2011.08.006.
Ellsworth, D. L., Rittenhouse, K. D. and Honeycutt, R. L. (1993). Artifactual variation in randomly amplified polymorphic DNA banding patterns. Biotechniques 14, 214217.
Erensoy, A., Kuk, S. and Ozden, M. (2009). Genetic identification of Fasciola hepatica by ITS-2 sequence of nuclear ribosomal DNA in Turkey. Parasitology Research 105, 407412. doi: 10.1007/s00436-009-1399-8.
Fairweather, I. (2005). Triclabendazole: new skills to unravel an old(ish) enigma. Journal of Helminthology 79, 227234. doi: 10.1079/JOH2005298.
Fairweather, I. (2009). Triclabendazole progress report, 2005–2009: an advancement of learning? Journal of Helminthology 83, 139150. doi: 10.1017/S0022149X09321173.
Fairweather, I. (2011). Liver fluke isolates: a question of provenance. Veterinary Parasitology 176, 18. doi: 10.1016/j.vetpar.2010.12.011.
Fairweather, I., McShane, D. D., Shaw, L., Ellison, S. E., O'Hagan, N. T., York, E. A., Trudgett, A. and Brennan, G. P. (2012). Development of an egg hatch assay for the diagnosis of triclabendazole resistance in Fasciola hepatica: Proof of concept. Veterinary Parasitology 183, 249259. doi: 10.1016/j.vetpar.2011.07.023.
Flanagan, A., Edgar, H. W. J., Forster, F., Gordon, A., Hanna, R. E. B., McCoy, M., Brennan, G. P. and Fairweather, I. (2011 b). Standardisation of a coproantigen reduction test (CRT) protocol for the diagnosis of resistance to triclabendazole in Fasciola hepatica. Veterinary Parasitology 176, 3442. doi: 10.1016/j.vetpar.2010.10.037.
Flanagan, A., Edgar, H. W. J., Gordon, A., Hanna, R. E. B., Brennan, G. P. and Fairweather, I. (2011 a). Comparison of two assays, a faecal egg count reduction test (FECRT) and a coproantigen reduction test (CRT), for the diagnosis of resistance to triclabendazole in Fasciola hepatica in sheep. Veterinary Parasitology 176, 170176. doi: 10.1016/j.vetpar.2010.10.057.
Fletcher, H. L., Hoey, E. M., Orr, N., Trudgett, A., Fairweather, I. and Robinson, M. W. (2004). The occurrence and significance of triploidy in the liver fluke, Fasciola hepatica. Parasitology 128, 6972. doi: 10.1017/S003118200300427X.
Fox, N. J., White, P. C., McClean, C. J., Marion, G., Evans, A. and Hutchings, M. R. (2011). Predicting impacts of climate change on Fasciola hepatica risk. PLoS ONE 6:e16126. doi: 10.1371/journal.pone.0016126.
Gaasenbeek, C. P. H., Moll, L., Cornelissen, J. B. W. J., Vellema, P. and Borgsteede, F. H. M. (2001). An experimental study on triclabendazole resistance of Fasciola hepatica in sheep. Veterinary Parasitology 95, 3743. doi: 10.1016/S0304-4017(00)00413-1.
Galtier, N., Nabholz, B., Glémin, S. and Hurst, G. D. D. (2009). Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Molecular Ecology 18, 45414550. doi: 10.1111/j.1365-294X.2009.04380.x.
Gilleard, J. (2006). Understanding anthelmintic resistance: the need for genomics and genetics. International Journal for Parasitology 36, 12271239. doi: 10.1016/j.ijpara.2006.06.010.
Gilleard, J. S. and Beech, R. N. (2007). Population genetics of anthelmintic resistance in parasitic nematodes. Parasitology 134, 11331146. doi: 10.1017/S0031182007000066.
González, L. C., Esteban, J. G., Bargues, M. D., Valero, M. A., Ortiz, P., Náquira, C. and Mas-Coma, S. (2011). Hyperendemic human fascioliasis in Andean valleys: an altitudinal transect analysis in children of Cajamarca province. Peru Acta Tropica 120, 119129. doi: 10.1016/j.actatropica.2011.07.002.
Gordon, D., Zadoks, R. and Skuce, P. (2012). Confirmation of triclabendazole resistance in liver fluke in the UK. Veterinary Record 171, 159160. doi: 10.1136/vr.e5381.
Halferty, L., Brennan, G. P., Hanna, R. E., Edgar, H. W., Meaney, M. M., McConville, M., Trudgett, A., Hoey, L. and Fairweather, I. (2008). Tegumental surface changes in juvenile Fasciola hepatica in response to treatment in vivo with triclabendazole. Veterinary Parasitology 155, 4958. doi: 10.1016/j.vetpar.2008.04.011.
Halferty, L., Brennan, G. P., Trudgett, A., Hoey, L. and Fairweather, I. (2009). Relative activity of triclabendazole metabolites against the liver fluke, Fasciola hepatica. Veterinary Parasitology 159, 126138. doi: 10.1016/j,vetpar.2008.10.007.
Hanna, R. E. B., Edgar, H., Moffett, D., McConnell, S., Fairweather, I., Brennan, G. P., Trudgett, A., Hoey, E. M., Cromie, L., Taylor, S. M. and Daniel, R. (2008). Fasciola hepatica: histology of the testis in egg producing adults of several laboratory-maintained isolates grown to maturity in cattle and sheep and in flukes from naturally infected hosts. Veterinary Parasitology 157, 222234. doi: 10.1016/j.vetpar.2008.07.022.
Hurtrez-Boussès, S., Durand, P., Jabbour-Zahab, R., Guégan, J. F., Meunier, C., Bargues, M. D., Mas-Coma, S. and Renaud, F. (2004). Isolation and characterization of microsatellite markers in the liver fluke (Fasciola hepatica). Molecular Ecology Notes 4, 689690. doi: 10.1111/j.1471-8286.2004.00786.x.
Ichikawa, M. and Itagaki, T. (2010). Discrimination of the ITS1 types of Fasciola spp. based on a PCR-RFLP method. Parasitology Research 106, 757761. doi: 10.1007/s00436-010-1724-2.
Itagaki, T. and Tsutsumi, K. (1998). Triploid form of Fasciola in Japan: genetic relationships between Fasciola hepatica and Fasciola gigantica determined by ITS-2 sequence of nuclear rDNA. International Journal for Parasitology 28, 777781. doi: 10.1016/S0020-7519(98)00037-X.
James, C. E. and Davey, M. W. (2009). Increased expression of ABC transport proteins is associated with ivermectin resistance in the model nematode Caenorhabditis elegans. International Journal for Parasitology 39, 213220. doi: 10.1016/j.ijpara.2008.06.009.
Jefferies, J. R., Campbell, A. M., van Rossum, A. J., Barrett, J. and Brophy, P. M. (2001). Proteomic analysis of Fasciola hepatica excretory-secretory products. Proteomics 1, 11281132. doi: 10.1002/1615-9861(200109)1:9<1128::AID-PROT1128>3.0.CO;2-0.
Jex, A. R., Young, N. D., Sripa, J., Hall, R. S., Scheerlinck, J. P., Laha, T., Sripa, B. and Gasser, R. B. (2012). Molecular changes in Opisthorchis viverrini (Southeast Asian liver fluke) during the transition from the juvenile to the adult stage. PLoS Neglected Tropical Diseases 6, e1916. doi: 10.1371/journal.pntd.0001916.
Johnson, P. C. D., Webster, L. M. I., Adam, A., Buckland, R., Dawson, D. A. and Keller, L. F. (2006). Abundant variation in microsatellites of the parasitic nematode Trichostrongylus tenuis and linkage to a tandem repeat. Molecular and Biochemical Parasitology 148, 210218. doi: 10.1016/j.molbiopara.2006.04.011.
Laoprom, N., Sithithaworn, P., Andrews, R. H., Ando, K., Laha, T., Klinbunga, S., Webster, J. P., Petney, T. N. (2012). Population genetic structuring in Opisthorchis viverrini over various spatial scales in Thailand and Lao PDR. PLOS Neglected Tropical Diseases 6, e1906. doi: 10.1371/journal.pntd.0001906.
Le, T. H., Blair, D. and McManus, D. P. (2001). Complete DNA sequence and gene organization of the mitochondrial genome of the liverfluke, Fasciola hepatica L. (Platyhelminthes; Trematoda). Parasitology 123, 609621. doi: 10.1017/S0031182001008733.
Li, G. and Quiros, C. F. (2001). Sequence-releated amplified polymorphism (SRAP), a new marker system based on a simple PCR reaction: its application to mapping and gene tagging in Brassica. Theoretical and Applied Genetics 103, 455461. doi: 10.1007/s001220100570.
Marcilla, A., Bargues, M. D. and Mas-Coma, S. (2002). A PCR-RFLP assay for the distinction between Fasciola hepatica and Fasciola gigantica. Molecular and Cellular Probes 16, 327333. doi: 10.1006/mcpr.2002.0429.
McCann, C. M., Baylis, M. and Williams, D. J. (2010). Seroprevalence and spatial distribution of Fasciola hepatica-infected dairy herds in England and Wales. Veterinary Record 166, 612617. doi: 10.1136/vr.b4836.
McConville, M., Brennan, G. P., Flanagan, A., Edgar, H. W. J., Hanna, R. E. B., McCoy, M., Gordon, A. W., Castillo, R., Hernandez-Campos, A. and Fairweather, I. (2009). An evaluation of the efficacy of compound alpha and triclabendazole against two isolates of Fasciola hepatica. Veterinary Parasitology 162, 7588. doi: 10.1016/j.vetpar.2009.02.004.
McCoy, M. A., Fairweather, I., Brennan, G. P., Kenny, J. M., Elison, S. and Forbes, A. B. (2005). The efficacy of nitroxynil and triclabendazole administered synchronously against juvenile triclabendazole-resistant Fasciola hepatica in sheep. Research in Veterinary Science 78, 33. doi: 10.1016/j.rvsc.2005.02.001.
McGarry, J. W., Ortiz, P. L., Hodgkinson, J. E., Goreish, I. and Williams, D. J. L. (2007). PCR-based differentiation of Fasciola species (Trematoda: Fasciolidae), using primers based on RAPD-derived sequences. Annals of Tropical Medicine and Parasitology 101, 415421. doi: 10.1179/136485907X176508.
McGonigle, L., Mousley, A., Marks, N. J., Brennan, G. P., Dalton, J. P., Spithill, T. W., Day, T. A. and Maule, A. G. (2008). The silencing of cysteine proteases in Fasciola hepatica newly excysted juveniles using RNA interference reduces gut penetration. International Journal for Parasitology 38, 149155. doi: 10.1016/j.ijpara.2007.10.007.
McVeigh, P., Maule, A. G., Dalton, J. P. and Robinson, M. W. (2012). Fasciola hepatica virulence-associated cysteine peptidases: a systems biology perspective. Microbes and Infection 14, 301310. doi: 10.1016/j.micinf.2011.11.012.
Meaney, M., Allister, J., McKinstry, B., McLaughlin, K., Brennan, G. P., Forbes, A. B. and Fairweather, I. (2007). Fasciola hepatica: ultrastructural effects of a combination of triclabendazole and clorsulon against mature fluke. Parasitology Research 100, 10911104. doi: 10.1007/s00436-006-0378-6.
Morphew, R. M., Eccleston, N., Wilkinson, T. J., McGarry, J., Perally, S., Prescott, M., Ward, D., Williams, D., Paterson, S., Raman, M., Ravikumar, G., Khalid Saifullah, M., Abbas Abidi, S. M., McVeigh, P., Maule, A. G., Brophy, P. M. and LaCourse, E. J. (2012). Proteomics and in silico approaches to extend understanding of the glutathione transferase superfamily of the tropical fluke Fasciola gigantica. Journal of Proteome Research 11, 58765889. doi: 10.1021/pr300654w.
Morphew, R. M., Wright, H. A., LaCourse, E. J., Porter, J., Barrett, J., Woods, D. J. and Brophy, P. M. (2011). Towards delineating functions within the Fasciola secreted cathepsin I protease family by integrating in vivo based sub-proteomics and phylogenetics. PLoS Neglected Tropical Diseases 5, e937. doi: 10.1371/journal.pntd.0000937.
Morphew, R. M., Wright, H. A., LaCourse, E. J., Woods, D. J. and Brophy, P. M. (2007). Comparative proteomics of excretory-secretory proteins released by the liver fluke Fasciola hepatica in sheep host bile and during in vitro culture ex host. Molecular and Cellular Proteomics 6, 963972. doi: 10.1074/mcp.M600375-MCP200.
Mottier, L., Alvarez, L., Fairweather, I. and Lanusse, C. (2006). Resistance-induced changes in triclabendazole transport in Fasciola hepatica: ivermectin reversal effect. Journal of Parasitology 92, 13551360. doi: 10.1645/GE-922R.1.
Prichard, R. K. and Roulet, A. (2007). ABC transporters and beta-tubulin in macrocyclic lactone resistance: prospects for marker development. Parasitology 134, 11231132. doi: 10.1017/S0031182007000091.
Ramadan, N. I. and Saber, L. M. (2004). Detection of genetic variability in nonhuman isolates of Fasciola hepatica and Fasciola gigantica by the RAPD-PCR technique. Journal of the Egyptian Society of Parasitology 34, 679689.
Reblánová, M., Špakulová, M., Orosová, M., Králová-Hromadová, I., Bazsalovicsová, E., Rajský, D. (2011). A comparative study of karyotypes and chromosomal location of rDNA genes in important liver flukes Fasciola hepatica and Fascioloides magna (Trematoda: Fasciolidae). Parasitology Research 109, 10211028. doi: 10.1007/s00436-011-2339-y.
Redman, E., Sargison, N., Whitelaw, F., Jackson, F., Morrison, A., Bartley, D. J. and Gilleard, J. S. (2012). Introgression of ivermectin resistance genes into a susceptible Haemonchus contortus strain by multiple backcrossing. PLoS Pathogens 8, 110. doi: e1002534.
Reed, M. B., Spithill, T. W., Strugnell, R. A. and Panaccio, M. (1998). Fasciola hepatica: stage-specific expression of novel gene sequences as identified by differential display. Experimental Parasitology 89, 169179.
Rinaldi, G., Morales, M. E., Cancela, M., Castillo, E., Brindley, P. J. and Tort, J. F. (2008). Development of functional genomic tools in trematodes: RNA interference and luciferase reporter gene activity in Fasciola hepatica. PLoS Neglected Tropical Diseases 9, e260. doi:10.1371/journal.pntd.0000260.
Robinson, M. W., Lawson, J., Trudgett, A., Hoey, E. M. and Fairweather, I. (2004). The comparative metabolism of triclabendazole sulphoxide by triclabendazole-susceptible and triclabendazole-resistant Fasciola hepatica. Parasitology Research 92, 205210. doi: 10.1007/s00436-003-1003-6.
Robinson, M. W., Menon, R., Donnelly, S. M., Dalton, J. P. and Ranganathan, S. (2009). An integrated transcriptomics and proteomics analysis of the secretome of the helminth pathogen Fasciola hepatica. Molecular and Cellular Proteomics 8, 18911907. doi: 10.1074/mcp.M900045-MCP200.
Ryan, L. A., Hoey, E., Trudgett, A., Fairweather, I., Fuchs, M., Robinson, M. W., Chambers, E., Timson, D., Ryan, E., Fetwell, T., Ivens, A., Bentley, G. and Johnston, D. (2008). Fasciola hepatica expresses multiple α- and β-tubulin isotypes. Molecular and Biochemical Parasitology 159, 7378. doi: 10.1016/j.molbiopara.2008.02.001.
Sargison, N. D. and Scott, P. R. (2011). Diagnosis and economic consequences of triclabendazole resistance in Fasciola hepatica in a sheep flock in south-east Scotland. Veterinary Record 168, 159. doi: 10.1136/vr.c5332.
Sargison, N. D., Wilson, D. J., Penny, C. D. and Bartley, D. J. (2010). Unexpected production loss caused by helminth parasites in weaned beef calves. Veterinary Record 167, 752754. doi: 10.1136/vr.c5428.
Semyenova, S. K., Morozova, E. V., Chrisanfova, G. G., Gorokhov, V. V., Arkhipov, I. A., Moskvin, A. S., Movsessyan, S. O. and Ryskov, A. P. (2006). Genetic differentiation in Eastern European and Western Asian populations of the liver fluke, Fasciola hepatica, as revealed by mitochondrial NAD1 and COX1 genes. Journal of Parasitology 92, 525530. doi: 10.1645/GE-673R.1.
Teofanova, D., Kantzoura, V., Walker, S., Radoslavov, G., Hristov, P., Theodoropoulos, G., Bankov, I. and Trudgett, A. (2011). Genetic diversity of liver flukes (Fasciola hepatica) from Eastern Europe. Infection, Genetics and Evolution 11, 109115. doi: 10.1016/j.meegid.2010.10.002.
van Dijk, J., Sargison, N. D., Kenyon, F. and Skuce, P. J. (2010). Climate change and infectious disease: helminthological challenges to farmed ruminants in temperate regions. Animal 4, 377392. doi: 10.1017/S1751731109990991.
Vara-Del Río, M. P., Villa, H., Martinez-Valladares, M. and Rojo-Vázquez, F. A. (2007). Genetic heterogeneity of Fasciola hepatica isolates in the northwest of Spain. Parasitology Research 101, 10031006. doi: 10.1007/s00436-007-0574-z.
Vargas, D., Vega, M. and González, C. G. (2003). Aproximación a una caracterización molecular de Fasciola hepatica por la técnica RAPDs – PCR. Parasitología Latinoamericana 58, 1116. doi: 10.4067/S0717-77122003000100002.
Vázquez-Prieto, S., Vilas, R., Mezo, M., González-Warleta, M., Ubeira, F. M. and Paniagua, E. (2011). Allozyme markers suitable for population genetic analysis of Fasciola hepatica. Veterinary Parasitology 176, 8488. doi: 10.1016/j.vetpar.2010.10.042.
Vilas, R., Paniagua, E., Outeiral, S. and Sanmartín, M. L. (2002). Electrophoretic and morphological differentiation of three sympatric species of the genus Lecithochirium (Trematoda: Hemiuridae), parasites of marine fishes. Parasitology Research 88, 10551060. doi: 10.1007/s00436-002-0708-2.
Vilas, R., Vásquez-Prieto, S. and Paniagua, E. (2012). Contrasting patterns of population genetic structure of Fasciola hepatica from cattle and sheep: Implications for the evolution of anthelmintic resistance. Infection, Genetics and Evolution 12, 4552. doi: 10.1016/j.meegid.2011.10.010.
Walker, S. M., McKinstry, B., Boray, J. C., Brennan, G. P., Trudgett, A., Hoey, E. M., Fletcher, H. and Fairweather, I. (2004). Response of two isolates of Fasciola hepatica to treatment with triclabendazole in vivo and in vitro. Parasitology Research 94, 427438. doi: 10.1007/s00436-004-1222-5.
Walker, S. M., Johnston, C., Hoey, E. M., Fairweather, I., Borgsteede, F., Gaasenbeek, C., Prodöhl, P. A. and Trudgett, A. (2011). Population dynamics of the liver fluke, Fasciola hepatica: the effect of time and spatial separation on the genetic diversity of fluke populations in the Netherlands. Parasitology 138, 215223. doi: 10.1017/S0031182010001149.
Walker, S. M., Prodöhl, P. A., Fletcher, H. L., Hanna, R. E. B., Kantzoura, V., Hoey, E. M. and Trudgett, A. (2007). Evidence for multiple mitochondrial lineages of Fasciola hepatica (liver fluke) within infrapopulations from cattle and sheep. Parasitology Research 101, 117125. doi: 10.1007/s00436-006-0440-4.
Wilkinson, R., Law, C. J., Hoey, E. M., Fairweather, I., Brennan, G. P. and Trudgett, A. (2012). An amino acid substitution in Fasciola hepatica P-glycoprotein from triclabendazole-resistant and triclabendazole-susceptible populations. Molecular and Biochemical Parasitology 186, 6972. doi: 10.1016/j.molbiopara.2012.08.008.
Winkelhagen, A. J., Mank, T., de Vries, P. J. and Soetekouw, R. (2012). Apparent triclabendazole-resistant human Fasciola hepatica infection, the Netherlands. Emerging Infectious Diseases 18, 10281029. doi: 10.3201/eid1806.120302.
Xu, M. J., Ai, L., Fu, J. H., Nisbet, A. J., Liu, Q. Y., Chen, M. X., Zhou, D. H. and Zhu, X. Q. (2012). Comparative characterisation of microRNAs from the liver flukes Fasciola gigantica and F. hepatica. PLoS ONE 7, e53387. doi:10.1371/journal.pone.0053387.
Young, N. D., Halls, R. S., Jex, A. R., Cantacessi, C. and Gasser, R. B. (2010). Elucidating the transcriptome of Fasciola hepatica – a key to fundamental and biotechnological discoveries for a neglected parasite. Biotechnology Advances 28, 222231. doi: 10.1016/j.biotechadv.2009.12.003.
Young, N. D., Jex, A. R., Cantacessi, C., Halls, R. S., Campbell, B. E., Spithill, T. W., Tangkawattana, S., Tangkawattana, P., Laha, T. and Gasser, R. B. (2011). A portrait of the transcriptome of the neglected trematode, Fasciola gigantica – biological and biotechnological implications. PLoS Neglected Tropical Diseases 5, e1004. doi: 10.1371/journal.pntd.0001004.

Keywords

Identification of putative markers of triclabendazole resistance by a genome-wide analysis of genetically recombinant Fasciola hepatica

  • J. HODGKINSON (a1), K. CWIKLINSKI (a1), N. J. BEESLEY (a1), S. PATERSON (a2) and D. J. L. WILLIAMS (a1)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed