Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-19T19:59:14.280Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  31 May 2013

J. HODGKINSON ,
K. CWIKLINSKI ,
N. J. BEESLEY ,
S. PATERSON  and
D. J. L. WILLIAMS
J. HODGKINSON*
Affiliation:
Veterinary Parasitology, Institute of Infection and Global Health, University of Liverpool, Liverpool, L3 5RF, UK
K. CWIKLINSKI
Affiliation:
Veterinary Parasitology, Institute of Infection and Global Health, University of Liverpool, Liverpool, L3 5RF, UK
N. J. BEESLEY
Affiliation:
Veterinary Parasitology, Institute of Infection and Global Health, University of Liverpool, Liverpool, L3 5RF, UK
S. PATERSON
Affiliation:
Centre for Genomic Research, University of Liverpool, Liverpool L69 7ZB, UK
D. J. L. WILLIAMS
Affiliation:
Veterinary Parasitology, Institute of Infection and Global Health, University of Liverpool, Liverpool, L3 5RF, UK
*
*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
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Fasciola hepaticaGalba truncatulaSNPsgenomemicrosatellitepopulation genetics
Type
Research Article
Information
Parasitology , Volume 140 , Issue 12: Genetic and genomic approaches to understanding drug resistance in parasites , October 2013 , pp. 1523 - 1533
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

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, 181–186. doi: 10.1007/s00436-008-0952-1.CrossRefGoogle ScholarPubMed
Aldemir, O. S. (2006). Differentiation of cattle and sheep originated Fasciola hepatica by RAPD-PCR. Revue de Médecine Vétérinaire 157, 65–67.Google Scholar
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, 1021–1024. doi: 10.1007/s00436-007-0870-7.CrossRefGoogle Scholar
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, 501–510. doi: 10.1017/S0031182005007997.CrossRefGoogle ScholarPubMed
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, 424–425. doi: 10.1136/vr.159.13.424.CrossRefGoogle ScholarPubMed
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, 119–130. doi: 10.1111/j.1096-0031.1995.tb00083.x.CrossRefGoogle ScholarPubMed
Beveridge, I. (1998). Allozyme electrophoresis – difficulties encountered in studies on helminths. International Journal for Parasitology 28, 973–979. doi: 10.1016/S0020-7519(98)00047-2.CrossRefGoogle ScholarPubMed
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. 51–60. MSD AGVET, Rahway, NJ.Google Scholar
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, 104–109. doi: 10.1016/jyexmp.2007.01.009X.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 4940–4951. doi: 10.1021/pr1000785.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Coles, G. C. and Stafford, K. A. (2001). Activity of oxyclozanide, nitroxynil, clorsulon and albendazole against adult triclabendazole-resistant Fasciola hepatica. Veterinary Record 148, 723–724. doi: 10.1136/vr.148.23.723.CrossRefGoogle ScholarPubMed
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, 15–26. doi: 10.1016/S0001-706X(97)00670-0.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Dar, Y., Amer, S., Courtioux, B. and Dreyfuss, G. (2011). Microsatellite analysis of Fasciola spp. in Egypt. Parasitology Research 109, 1741–1744. doi: 10.1007/s00436-011-2520-3.CrossRefGoogle ScholarPubMed
Devaney, E., Winter, A. D. and Britton, C. (2010). microRNAs: a role in drug resistance in parasitic nematodes? Trends in Parasitology 26, 428–433. doi: 10.1016/j.pt.2010.05.003.CrossRefGoogle ScholarPubMed
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, 337–353. doi: 10.1007/s00436-010-1866-2.CrossRefGoogle ScholarPubMed
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, 1351–1363. doi: 10.1007/s00436-010-1806-1.CrossRefGoogle Scholar
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, 1209–1223. doi: 10.1007/s00436-011-2554-6.CrossRefGoogle Scholar
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, 37–47. doi: 10.1016/j.vetpar.2011.08.006.CrossRefGoogle ScholarPubMed
Ellsworth, D. L., Rittenhouse, K. D. and Honeycutt, R. L. (1993). Artifactual variation in randomly amplified polymorphic DNA banding patterns. Biotechniques 14, 214–217.Google ScholarPubMed
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, 407–412. doi: 10.1007/s00436-009-1399-8.CrossRefGoogle ScholarPubMed
Fairweather, I. (2005). Triclabendazole: new skills to unravel an old(ish) enigma. Journal of Helminthology 79, 227–234. doi: 10.1079/JOH2005298.CrossRefGoogle ScholarPubMed
Fairweather, I. (2009). Triclabendazole progress report, 2005–2009: an advancement of learning? Journal of Helminthology 83, 139–150. doi: 10.1017/S0022149X09321173.CrossRefGoogle ScholarPubMed
Fairweather, I. (2011). Liver fluke isolates: a question of provenance. Veterinary Parasitology 176, 1–8. doi: 10.1016/j.vetpar.2010.12.011.CrossRefGoogle ScholarPubMed
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, 249–259. doi: 10.1016/j.vetpar.2011.07.023.CrossRefGoogle ScholarPubMed
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, 34–42. doi: 10.1016/j.vetpar.2010.10.037.CrossRefGoogle ScholarPubMed
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, 170–176. doi: 10.1016/j.vetpar.2010.10.057.CrossRefGoogle Scholar
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, 69–72. doi: 10.1017/S003118200300427X.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 37–43. doi: 10.1016/S0304-4017(00)00413-1.CrossRefGoogle Scholar
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, 4541–4550. doi: 10.1111/j.1365-294X.2009.04380.x.CrossRefGoogle ScholarPubMed
Gilleard, J. (2006). Understanding anthelmintic resistance: the need for genomics and genetics. International Journal for Parasitology 36, 1227–1239. doi: 10.1016/j.ijpara.2006.06.010.CrossRefGoogle ScholarPubMed
Gilleard, J. S. and Beech, R. N. (2007). Population genetics of anthelmintic resistance in parasitic nematodes. Parasitology 134, 1133–1146. doi: 10.1017/S0031182007000066.CrossRefGoogle ScholarPubMed
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, 119–129. doi: 10.1016/j.actatropica.2011.07.002.CrossRefGoogle ScholarPubMed
Gordon, D., Zadoks, R. and Skuce, P. (2012). Confirmation of triclabendazole resistance in liver fluke in the UK. Veterinary Record 171, 159–160. doi: 10.1136/vr.e5381.CrossRefGoogle ScholarPubMed
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, 49–58. doi: 10.1016/j.vetpar.2008.04.011.CrossRefGoogle ScholarPubMed
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, 126–138. doi: 10.1016/j,vetpar.2008.10.007.CrossRefGoogle ScholarPubMed
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, 222–234. doi: 10.1016/j.vetpar.2008.07.022.CrossRefGoogle ScholarPubMed
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, 689–690. doi: 10.1111/j.1471-8286.2004.00786.x.CrossRefGoogle Scholar
Ichikawa, M. and Itagaki, T. (2010). Discrimination of the ITS1 types of Fasciola spp. based on a PCR-RFLP method. Parasitology Research 106, 757–761. doi: 10.1007/s00436-010-1724-2.CrossRefGoogle ScholarPubMed
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, 777–781. doi: 10.1016/S0020-7519(98)00037-X.CrossRefGoogle ScholarPubMed
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, 213–220. doi: 10.1016/j.ijpara.2008.06.009.CrossRefGoogle ScholarPubMed
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, 1128–1132. doi: 10.1002/1615-9861(200109)1:9<1128::AID-PROT1128>3.0.CO;2-0.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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, 210–218. doi: 10.1016/j.molbiopara.2006.04.011.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 609–621. doi: 10.1017/S0031182001008733.CrossRefGoogle ScholarPubMed
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, 455–461. doi: 10.1007/s001220100570.CrossRefGoogle Scholar
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, 327–333. doi: 10.1006/mcpr.2002.0429.CrossRefGoogle ScholarPubMed
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, 612–617. doi: 10.1136/vr.b4836.CrossRefGoogle ScholarPubMed
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, 75–88. doi: 10.1016/j.vetpar.2009.02.004.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 415–421. doi: 10.1179/136485907X176508.CrossRefGoogle ScholarPubMed
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, 149–155. doi: 10.1016/j.ijpara.2007.10.007.CrossRefGoogle ScholarPubMed
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, 301–310. doi: 10.1016/j.micinf.2011.11.012.CrossRefGoogle ScholarPubMed
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, 1091–1104. doi: 10.1007/s00436-006-0378-6.CrossRefGoogle ScholarPubMed
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, 5876–5889. doi: 10.1021/pr300654w.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 963–972. doi: 10.1074/mcp.M600375-MCP200.CrossRefGoogle ScholarPubMed
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, 1355–1360. doi: 10.1645/GE-922R.1.CrossRefGoogle ScholarPubMed
Prichard, R. K. and Roulet, A. (2007). ABC transporters and beta-tubulin in macrocyclic lactone resistance: prospects for marker development. Parasitology 134, 1123–1132. doi: 10.1017/S0031182007000091.CrossRefGoogle ScholarPubMed
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, 679–689.Google Scholar
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, 1021–1028. doi: 10.1007/s00436-011-2339-y.CrossRefGoogle ScholarPubMed
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, 1–10. doi: e1002534.CrossRefGoogle ScholarPubMed
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, 169–179.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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, 205–210. doi: 10.1007/s00436-003-1003-6.CrossRefGoogle ScholarPubMed
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, 1891–1907. doi: 10.1074/mcp.M900045-MCP200.CrossRefGoogle ScholarPubMed
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, 73–78. doi: 10.1016/j.molbiopara.2008.02.001.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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, 752–754. doi: 10.1136/vr.c5428.CrossRefGoogle ScholarPubMed
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, 525–530. doi: 10.1645/GE-673R.1.CrossRefGoogle ScholarPubMed
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, 109–115. doi: 10.1016/j.meegid.2010.10.002.CrossRefGoogle ScholarPubMed
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, 377–392. doi: 10.1017/S1751731109990991.CrossRefGoogle ScholarPubMed
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, 1003–1006. doi: 10.1007/s00436-007-0574-z.CrossRefGoogle ScholarPubMed
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, 11–16. doi: 10.4067/S0717-77122003000100002.CrossRefGoogle Scholar
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, 84–88. doi: 10.1016/j.vetpar.2010.10.042.CrossRefGoogle ScholarPubMed
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, 1055–1060. doi: 10.1007/s00436-002-0708-2.Google ScholarPubMed
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, 45–52. doi: 10.1016/j.meegid.2011.10.010.CrossRefGoogle ScholarPubMed
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, 427–438. doi: 10.1007/s00436-004-1222-5.CrossRefGoogle ScholarPubMed
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, 215–223. doi: 10.1017/S0031182010001149.CrossRefGoogle ScholarPubMed
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, 117–125. doi: 10.1007/s00436-006-0440-4.CrossRefGoogle ScholarPubMed
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, 69–72. doi: 10.1016/j.molbiopara.2012.08.008.CrossRefGoogle ScholarPubMed
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, 1028–1029. doi: 10.3201/eid1806.120302.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 222–231. doi: 10.1016/j.biotechadv.2009.12.003.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed