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Fasciolosis in South America: epidemiology and control challenges

Published online by Cambridge University Press:  09 September 2016

C. Carmona  and
J.F. Tort
C. Carmona
Affiliation:
Unidad de Biología Parasitaria, Departamento de Biología Celular y Molecular, Facultad de Ciencias, Instituto de Higiene, Universidad de la Republica, UDELAR, Av. Alfredo Navarro 3051 CP 11600, Montevideo, Uruguay
J.F. Tort*
Affiliation:
Departamento de Genética, Facultad de Medicina, Universidad de la Republica, UDELAR, Avda. Gral. Flores 2125, CP 11800, Montevideo, Uruguay
*
*E-mail: jtort@fmed.edu.uy
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Abstract

Fasciolosis caused by Fasciola hepatica severely affects the efficiency of livestock production systems worldwide. In addition to the economic impact inflicted on livestock farmers, fasciolosis is an emergent zoonosis. This review emphasizes different aspects of the disease in South America. Available data on epidemiology in bovines and ovines in different countries, as well as a growing body of information on other domestic and wildlife definitive hosts, are summarized. The issue of drug resistance that compromises the long-term sustainability of current pharmacological strategies is examined from a regional perspective. Finally, efforts to develop a single-antigen recombinant vaccine in ruminants are reviewed, focusing on the cases of leucine aminopeptidase or thioredoxin glutathione reductase.

Type
Review Article
Information
Journal of Helminthology , Volume 91 , Issue 2 , March 2017 , pp. 99 - 109
Copyright
Copyright © Cambridge University Press 2016 

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References

Acosta, D., Goñi, F. & Carmona, C. (1998) Characterization and partial purification of a leucine aminopeptidase from Fasciola hepatica . Journal of Parasitology 84, 1–7.Google Scholar
Acosta, D., Cancela, M., Piacenza, L., Roche, L., Carmona, C. & Tort, J.F. (2008) Fasciola hepatica leucine aminopeptidase, a promising candidate for vaccination against ruminant fasciolosis. Molecular and Biochemical Parasitology 158, 52–64.Google Scholar
Ai, L., Chen, M.-X., Alasaad, S., Elsheikha, H.M., Li, J., Li, H.-L., Lin, R.-Q., Zou, F.-C., Zhu, X.-Q. & Chen, J.-X. (2011) Genetic characterization, species differentiation and detection of Fasciola spp. by molecular approaches. Parasites & Vectors 4, 101.Google Scholar
Aleixo, M.A., Freitas, D.F., Dutra, L.H., Malone, J., Martins, I.V.F. & Molento, M.B. (2015) Fasciola hepatica: epidemiology, perspectives in the diagnostic and the use of geoprocessing systems for prevalence studies. Semina: Ciências Agrárias 36, 1451.Google Scholar
Alvarez, J.D., Moriena, R.A., Ortiz, M.I. & Racioppi, O. (2009) Hallazgo de Fasciola hepatica (Trematoda: Digenea) en un carpincho (Hydrochaeris hydrochaeris) de la Provincia de Corrientes, Argentina. Revista Veterinaria 20, 132–134.Google Scholar
Alvarez Rojas, C.A., Jex, A.R., Gasser, R.B. & Scheerlinck, J.P.Y. (2014) Techniques for the diagnosis of Fasciola infections in animals. Room for improvement. Advances in Parasitology 85, 65–107.Google Scholar
Bennema, S.C., Scholte, R.G.C., Molento, M.B., Medeiros, C. & Carvalho, O.D.S. (2014) Fasciola hepatica in bovines in Brazil: data availability and spatial distribution. Revista do Instituto de Medicina Tropical de São Paulo 56, 35–41.Google Scholar
Bravo Antilef, M.J. (2015) Probables causas de muerte y principales hallazgos en la necropsia de pudues (Pudu puda) examinados durante 20 anos en el sur de Chile. PhD thesis, Universidad Austral de Chile.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. & Brophy, P.M. (2007) Understanding triclabendazole resistance. Experimental and Molecular Pathology 82, 104–109.Google Scholar
Cabada, M.M., Lopez, M., Cruz, M., Delgado, J.R., Hill, V. & White, A.C. (2016) Treatment failure after multiple courses of triclabendazole among patients with fascioliasis in Cusco, Peru: a case series. PLOS Neglected Tropical Diseases 10, e0004361.Google Scholar
Cafrune, M.M., Rebuffi, G.E., Cabrera, R.H. & Aguirre, D.H. (1996) F. hepatica en llamas (Lama glama) de la Puna Argentina. Veterinaria Argentina 13, 570–574.Google Scholar
Cancela, M., Ruétalo, N., Dell'Oca, N., da Silva, E., Smircich, P., Rinaldi, G., Roche, L., Carmona, C., Alvarez-Valín, F., Zaha, A. & Tort, J.F. (2010) Survey of transcripts expressed by the invasive juvenile stage of the liver fluke Fasciola hepatica . BMC genomics 11, 227.Google Scholar
Canevari, J., Ceballos, L., Sanabria, R., Romero, J., Olaechea, F., Ortiz, P., Cabrera, M., Gayo, V., Fairweather, I., Lanusse, C. & Alvarez, L. (2014) Testing albendazole resistance in Fasciola hepatica: validation of an egg hatch test with isolates from South America and the United Kingdom. Journal of Helminthology 88, 286–292.Google Scholar
Cañizales, I. & Guerrero, R. (2013) Chigüire (Hydrochoerus hydrochaeris) parasites, and parasite diseases. Boletín de la Academia de Ciencias Físicas, Matemáticas y Naturales. LXXII, 9–22.Google Scholar
Carnevale, S., Pantano, M.L., Kamenetzky, L., Malandrini, J.B., Soria, C.C. & Velásquez, J.N. (2015) Molecular diagnosis of natural fasciolosis by DNA detection in sheep faeces. Acta Parasitologica 60, 211–217.CrossRefGoogle ScholarPubMed
Ceballos, L., Moreno, L., Alvarez, L., Shaw, L., Fairweather, I. & Lanusse, C. (2010) Unchanged triclabendazole kinetics after co-administration with ivermectin and methimazole: failure of its therapeutic activity against triclabendazole-resistant liver flukes. BMC Veterinary Research 6, 8.Google Scholar
Charlier, J., Vercruysse, J., Morgan, E., van Dijk, J. & Williams, D.J.L. (2014a) Recent advances in the diagnosis, impact on production and prediction of Fasciola hepatica in cattle. Parasitology 141, 326–335.Google Scholar
Charlier, J., van der Voort, M., Kenyon, F., Skuce, P. & Vercruysse, J. (2014b) Chasing helminths and their economic impact on farmed ruminants. Trends in Parasitology 30, 361–367.Google Scholar
Chávez, A., Sánchez, L., Arana, C. & Suárez, F. (2012) Resistencia a antihelmínticos y prevalencia de fasciolosis bovina en la ganadería lechera de Jauja, Perú. Revista de Investigaciones Veterinarias del Peru 23, 90–97.Google Scholar
Correa, A., Escobar, J., Durand, P., Renaud, F., David, P., Jarne, P., Pointier, J.-P. & Hurtrez-Bousses, S. (2010) Bridging gaps in the molecular phylogeny of the Lymnaeidae (Gastropoda: Pulmonata), vectors of fascioliasis. BMC Evolutionary Biology 10, 381.Google Scholar
Corvo, I., Cancela, M., Cappetta, M., Pi-Denis, N., Tort, J.F. & Roche, L. (2009) The major cathepsin L secreted by the invasive juvenile Fasciola hepatica prefers proline in the S2 subsite and can cleave collagen. Molecular and Biochemical Parasitology 167, 41–47.Google Scholar
Cuervo, P.F., Cataldo, S. Di, Fantozzi, M.C., Deis, E., Isenrath, G.D., Viberti, G., Artigas, P., Peixoto, R., Valero, M.A., Sierra, R.M.Y. & Mas-Coma, S. (2015) Liver fluke (Fasciola hepatica) naturally infecting introduced European brown hare (Lepus europaeus) in northern Patagonia: phenotype, prevalence and potential risk. Acta Parasitologica 60, 536–543.CrossRefGoogle ScholarPubMed
Cwiklinski, K., Dalton, J.P., Dufresne, P.J., La Course, J., Williams, D.J., Hodgkinson, J. & Paterson, S. (2015a) The Fasciola hepatica genome: gene duplication and polymorphism reveals adaptation to the host environment and the capacity for rapid evolution. Genome Biology 16, 1–13.Google Scholar
Cwiklinski, K., de la Torre-Escudero, E., Trelis, M., Bernal, D., Dufresne, P.J., Brennan, G.P., O'Neill, S., Tort, J., Paterson, S., Marcilla, A., Dalton, J.P. & Robinson, M.W. (2015b) The extracellular vesicles of the helminth pathogen, Fasciola hepatica: biogenesis pathways and cargo molecules involved in parasite pathogenesis. Molecular & Cellular Proteomics 14, 3258–3273.Google Scholar
Dell'Oca, N., Basika, T., Corvo, I., Castillo, E., Brindley, P.J., Rinaldi, G. & Tort, J.F. (2014) RNA interference in Fasciola hepatica newly excysted juveniles: Long dsRNA induces more persistent silencing than siRNA. Molecular and Biochemical Parasitology 197, 28–35.Google Scholar
Dittmar, K. (2002) Arthropod and helminth parasites of the wild guinea pig, Cavia aperea, from the Andes and the Cordillera in Peru, South America. Journal of Parasitology 88, 409–411.Google Scholar
El-Kouba, M.M.A.N., Marques, S.M.T., Pilati, C. & Hamann, W. (2008) Aspectos gerais da fasciolose e de endoparasitose em capivaras (Hydrochaeris hydrochaeris Linnaeus, 1766) de três paques no paraná, Brasil. Revista de Medicina Veterinária 6, 4–15.Google Scholar
Elliott, T.P. & Spithill, T.W. (2014) The T687G SNP in a P-glycoprotein gene of Fasciola hepatica is not associated with resistance to triclabendazole in two resistant Australian populations. Molecular and Biochemical Parasitology 198, 45–47.Google Scholar
Elliott, T., Muller, A., Brockwell, Y., Murphy, N., Grillo, V., Toet, H.M., Anderson, G., Sangster, N. & Spithill, T.W. (2014) Evidence for high genetic diversity of NAD1 and COX1 mitochondrial haplotypes among triclabendazole resistant and susceptible populations and field isolates of Fasciola hepatica (liver fluke) in Australia. Veterinary Parasitology 200, 90–96.Google Scholar
Espinoza, J.R., Terashima, A., Herrera-Velit, P. & Marcos, L.A. (2010) Human and animal fascioliasis in Peru: impact in the economy of endemic zones. Revista Peruana de Medicina Experimental y Salud Pública 27, 604–612.Google Scholar
Fairweather, I. (2011). Liver fluke isolates: a question of provenance. Veterinary Parasitology 176, 1–8.Google Scholar
Fairweather, I. & Boray, J.C. (1999) Fasciolicides: efficacy, actions, resistance and its management. Veterinary Journal 158, 81–112.Google Scholar
Fernández, V., Estein, S., Ortiz, P., Luchessi, P., Solana, V. & Solana, H. (2015) A single amino acid substitution in isozyme GST mu in triclabendazole resistant Fasciola hepatica (Sligo strain) can substantially influence the manifestation of anthelmintic resistance. Experimental Parasitology 159, 274–279.Google Scholar
Flores, B., Pinedo, R.V., Suarez, F., Angelats, R. & Chavez, A. (2014) Prevalency of fascioliasis in llamas and alpacas in two rural communities of Jauja, Peru. Revista de Investigaciones Veterinarias del Peru 25, 284–292.Google Scholar
Freyre, A., Burgues, C., Seoane, L., Correa, I., Rodriguez-Piquinela, W., Ayala, R., Ayala, J.C. & Montanez, O. (1979) Parasitos encontrados en autopsias de carpincho (Hydrochoerus hydrochaeris) en Uruguay. Anales de la Facultad de Veterinaria (Uruguay) 16, 5–93.Google Scholar
Fugassa, M.H. (2015) Checklist of helminths found in Patagonian wild mammals. Zootaxa 4012, 271–328.Google Scholar
Gayo, V., Cuervo, P., Rosadilla, D., Birriel, S., Dell'Oca, L., Trelles, A., Cuore, U. & Sierra, R.M.Y. (2011) Natural Fasciola hepatica infection in nutria (Myocastor coypus) in Uruguay. Journal of Zoo and Wildlife Medicine 42, 354–356.Google Scholar
Gil, L.C., Díaz, A., Rueda, C., Martínez, C., Castillo, D. & Apt, W. (2014) [Resistant human fasciolasis: report of four patients.] Revista Médica de Chile 142, 1330–1333.Google Scholar
Guasconi, L., Serradell, M.C., Borgonovo, J., Garro, A.P., Varengo, H., Caffe, G. & Masih, D.T. (2012) Immunization with crude antigens plus aluminium hydroxide protects cattle from Fasciola hepatica infection. Journal of Helminthology 86, 64–69.Google Scholar
Hanna, R.E.B., Edgar, H.W.J., McConnell, S., Toner, E., McConville, M., Brennan, G.P., Devine, C., Flanagan, A., Halferty, L., Meaney, M., Shaw, L., Moffett, D., McCoy, M. & Fairweather, I. (2010) Fasciola hepatica: histological changes in the reproductive structures of triclabendazole (TCBZ)-sensitive and TCBZ-resistant flukes after treatment in vivo with TCBZ and the related benzimidazole derivative, Compound Alpha. Veterinary Parasitology 168, 240–254.Google Scholar
Hernandez, Z. & Gonzalez, S. (2011) Parasitological survey of the Uruguayan populations of wild Pampas deer (Ozotoceros bezoarticus L. 1758). Animal Production Science 52, 781–785.Google Scholar
Hodgkinson, J., Cwiklinski, K., Beesley, N.J., Paterson, S. & Williams, D.J.L. (2013) Identification of putative markers of triclabendazole resistance by a genome-wide analysis of genetically recombinant Fasciola hepatica . Parasitology 140, 1523–1533.CrossRefGoogle ScholarPubMed
Ichikawa-Seki, M., Ortiz, P., Cabrera, M., Hobán, C. & Itagaki, T. (2016) Molecular characterization and phylogenetic analysis of Fasciola hepatica from Peru. Parasitology International 65, 171–174.Google Scholar
INIA-CIID. (1991) Proyecto sistemas de produccion de cuyes. Peru, INIA (Instituto Nacional de Investigacion Agraria); Canada, CIID (Centro Internacional de Investigacion Para el Desarrollo). Available at http://www.inia.gob.pe/images/AccDirectos/publicaciones/cuyes/doc/PSP%20CUYES%20Tomo%202.pdf (accessed 21 August 2016).Google Scholar
Issia, L., Pietrokovsky, S., Sousa-Figueiredo, J., Stothard, J.R. & Wisnivesky-Colli, C. (2009) Fasciola hepatica infections in livestock flock, guanacos and coypus in two wildlife reserves in Argentina. Veterinary Parasitology 165, 341–344.Google Scholar
Iturbe, E. P. & Muñiz, P. F. (2012) Galba truncatula induced to infection with miracidia of Fasciola hepatica, collected in Huayllapampa, San Jerónimo, Cusco, Peru. Neotropical Helminthology 6, 325–338.Google Scholar
Kaplan, R.M. (2001) Fasciola hepatica: a review of the economic impact in cattle and considerations for control. Veterinary Therapeutics 2, 40–50.Google Scholar
Kelley, J.M., Elliott, T.P., Beddoe, T., Anderson, G., Skuce, P. & Spithill, T.W. (2016) Current threat of triclabendazole resistance in Fasciola hepatica . Trends in Parasitology 32, 458–469.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. & 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, 164–184.Google Scholar
Kuntz, A.N., Davioud-Charvet, E., Sayed, A.A., Califf, L.L., Dessolin, J., Arnér, E.S.J. & Williams, D.L. (2007) Thioredoxin glutathione reductase from Schistosoma mansoni: An essential parasite enzyme and a key drug target. PLoS Medicine 4, 1071–1086.Google Scholar
Larroza, M. & Olaechea, F. (2010) Comparación de la morfología y la viabilidad de huevos de fasciola hepática en distintos hospedadores en patagonia. Veterinaria Argentina 27, 1–5.Google Scholar
Led, J.E., Yannarella, F.G., Scasso, D.A. & Denegri, G.M. (1979) Lagidium viscaccia boxi nuevo reservorio silvestre de Fasciola hepatica (Linnaeus, 1758) en la República Argentina. Veterinaria 2, 31–39.Google Scholar
Maggioli, G., Piacenza, L., Carambula, B. & Carmona, C. (2004) Purification, characterization, and immunolocalization of a thioredoxin reductase from adult Fasciola hepatica . Journal of Parasitology 90, 205–211.Google Scholar
Maggioli, G., Acosta, D., Silveira, F., Rossi, S., Giacaman, S., Basika, T., Gayo, V., Rosadilla, D., Roche, L., Tort, J. & Carmona, C. (2011a) The recombinant gut-associated M17 leucine aminopeptidase in combination with different adjuvants confers a high level of protection against Fasciola hepatica infection in sheep. Vaccine 29, 9057–9063.Google Scholar
Maggioli, G., Silveira, F., Martín-Alonso, J.M., Salinas, G., Carmona, C. & Parra, F. (2011b) A recombinant thioredoxin-glutathione reductase from Fasciola hepatica induces a protective response in rabbits. Experimental Parasitology 129, 323–330.Google Scholar
Maggioli, G., Bottini, G., Basika, T., Alonzo, P., Salinas, G. & Carmona, C. (2016) Immunization with Fasciola hepatica thioredoxin glutathione reductase failed to confer protection against fasciolosis in cattle. Veterinary Parasitology 224, 13–19.Google Scholar
Mamani, W. & Condori, R. (2009) Anthelminthic resistance (Fasciola hepatica) in sheep against albendazole and triclabendazole, La Paz – Bolivia. Revista de Investigaciones Veterinarias del Peru 20, 254–262.Google Scholar
Marcilla, A., De La Rubia, J.E., Sotillo, J., Bernal, D., Carmona, C., Villavicencio, Z., Acosta, D., Tort, J., Bornay, F.J., Esteban, J.G. & Toledo, R. (2008) Leucine aminopeptidase is an immunodominant antigen of Fasciola hepatica excretory and secretory products in human infections. Clinical and Vaccine Immunology 15, 95–100.Google Scholar
Martin, J., Rosa, B.A., Ozersky, P., Hallsworth-Pepin, K., Zhang, X., Bhonagiri-Palsikar, V., Tyagi, R., Wang, Q., Choi, Y.J., Gao, X., McNulty, S.N., Brindley, P.J. & Mitreva, M. (2015) Helminth.net: expansions to Nematode.net and an introduction to Trematode.net. Nucleic Acids Research 43, D698–D706.Google Scholar
Martinez-Diaz, R.A., Martella, M.B., Navarro, J.L. & Ponce-Gordo, F. (2013) Gastrointestinal parasites in greater rheas (Rhea americana) and lesser rheas (Rhea pennata) from Argentina. Veterinary Parasitology 194, 75–78.Google Scholar
Martínez-Valladares, M. & Rojo-Vázquez, F.A. (2016) Loop-mediated isothermal amplification (LAMP) assay for the diagnosis of fasciolosis in sheep and its application under field conditions. Parasites & Vectors 9, 73.Google Scholar
Mas-Coma, S., Rodriguez, A., Bargues, M., Valero, M., Coello, J. & Angles, R. (1997) Secondary reservoir role of domestic animals other than sheep and cattle in fascioliasis transmission in the Northern Bolivian Altiplano. Research and Reviews in Parasitology 57, 39–46.Google Scholar
Mas-Coma, S., Anglés, R., Esteban, J.G., Bargues, M.D., Buchon, P., Franken, M. & Strauss, W. (1999) The Northern Bolivian Altiplano: a region highly endemic for human fascioliasis. Tropical Medicine and International Health 4, 454–467.Google Scholar
Mas-Coma, S., Bargues, M.D. & Valero, M.A. (2005) Fascioliasis and other plant-borne trematode zoonoses. International Journal for Parasitology 35, 1255–1278.Google Scholar
Mas-Coma, S., Valero, M.A. & Bargues, M.D. (2009) Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Advances in Parasitology 69, 41–146.Google Scholar
McCammick, E.M., McVeigh, P., McCusker, P., Timson, D.J., Morphew, R.M., Brophy, P.M., Marks, N.J., Mousley, A. & Maule, A.G. (2016) Calmodulin disruption impacts growth and motility in juvenile liver fluke. Parasites & Vectors 9, 46.Google Scholar
McGonigle, L., Mousley, A., Marks, N.J., Brennan, G.P., Dalton, J.P., Spithill, T.W., Day, T.A. & 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.Google Scholar
McVeigh, P., McCammick, E.M., McCusker, P., Morphew, R.M., Mousley, A., Abidi, A., Saifullah, K.M., Muthusamy, R., Gopalakrishnan, R., Spithill, T.W., Dalton, J.P., Brophy, P.M., Marks, N.J. & Maule, A.G. (2014) RNAi dynamics in juvenile Fasciola spp. liver flukes reveals the persistence of gene silencing in vitro. PLoS Neglected Tropical Diseases 8, e3185.Google Scholar
Meemon, K. & Sobhon, P. (2015) Juvenile-specific cathepsin proteases in Fasciola spp.: their characteristics and vaccine efficacies. Parasitology Research 114, 2807–2813.Google Scholar
Ménard, A., Agoulon, A., L'Hostis, M., Rondelaud, D., Collard, S. & Chauvin, A. (2001) Myocastor coypus as a reservoir host of Fasciola hepatica in France. Veterinary Research 32, 499–508.Google Scholar
Mera y Sierra, R., Artigas, P., Cuervo, P., Deis, E., Sidoti, L., Mas-Coma, S. & Bargues, M.D. (2009) Fascioliasis transmission by Lymnaea neotropica confirmed by nuclear rDNA and mtDNA sequencing in Argentina. Veterinary Parasitology 166, 73–79.Google Scholar
Morales, M.A., Luengo, J. & Pizarro, J.V. (2000) Distribucion y tendencia de la fasciolosis en ganado de abasto en Chile, 1989–1995. Parasitologia al dia 24, 115–118.Google Scholar
Moriena, R., Racioppi, O. & Alvarez, J.D. (2004) Fasciolosis en bovinos del nordeste argentino. Prevalencia según edad. Revista Veterinaria 15, 3–4.Google Scholar
Mottier, L., Alvarez, L., Fairweather, I. & Lanusse, C. (2006) Resistance-induced changes in triclabendazole transport in Fasciola hepatica: ivermectin reversal effect. Journal of Parasitology 92, 1355–1360.Google Scholar
Nansen, P. (1975) Resistance in cattle to Fasciola hepatica induced by gamma-ray attenuated larvae: results from a controlled field trial. Research in Veterinary Science 19, 278–283.Google Scholar
Nari, A., Cardozo, H., Solari, M.A., Petraccia, C. & Acosta, D. (1986) Estudio preliminar sobre el desarrollo de Lymnaea viatrix (D'Orbigny 1835) en condiciones controladas de temperatura y humedad. Veterinaria Montevideo 22, 13–17.Google Scholar
Olaechea, F., Lovera, V., Larroza, M., Raffo, F. & Cabrera, R. (2011) Resistance of Fasciola hepatica against triclabendazole in cattle in Patagonia (Argentina). Veterinary Parasitology 178, 364–366.Google Scholar
Oliveira, D.R., Ferreira, D.M., Stival, C.C., Romero, F., Cavagnolli, F., Kloss, A., Araújo, F.B. & Molento, M.B. (2008) Triclabendazole resistance involving Fasciola hepatica in sheep and goats during an outbreak in Almirante Tamandare, Paraná, Brazil. Brazilian Journal of Veterinary Parasitology 17, 149–153.Google Scholar
Ortiz, P., Scarcella, S., Cerna, C., Rosales, C., Cabrera, M., Guzmán, M., Lamenza, P. & Solana, H. (2013) Resistance of Fasciola hepatica against triclabendazole in cattle in Cajamarca (Peru): a clinical trial and an in vivo efficacy test in sheep. Veterinary Parasitology 195, 118–121.Google Scholar
Overend, D. & Bowen, F. (1995) Resistance of Fasciola hepatica to triclabendazole. Australian Veterinary Journal 72, 275–276.Google Scholar
Parkinson, M., O'Neill, S.M. & Dalton, J.P. (2007) Endemic human fasciolosis in the Bolivian Altiplano. Epidemiology Infection 135, 669–674.Google Scholar
Pereira De Souza, C. & Magalhães, K.G. (2000). Rearing of Lymnaea columella (Say, 1817), intermediate host of Fasciola hepatica (Linnaeus, 1758). Memorias do Instituto Oswaldo Cruz 95, 739–741.Google Scholar
Piacenza, L., Acosta, D., Basmadjian, I., Dalton, J. & Carmona, C. (1999) Vaccination with cathepsin L proteinases and with leucine aminopeptidase induce high levels of protection against fascioliasis in sheep. Infection and Immunity 67, 1954–1961.Google Scholar
Rinaldi, G., Morales, M.E., Cancela, M., Castillo, E., Brindley, P.J. & 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 2, e260.Google Scholar
Robinson, M.W., Menon, R., Donnelly, S.M., Dalton, J.P. & Ranganathan, S. (2009) An integrated transcriptomics and proteomics analysis of the secretome of the helminth pathogen Fasciola hepatica: proteins associated with invasion and infection of the mammalian host. Molecular & Cellular Proteomics: MCP 8, 1891–1907.Google Scholar
Rojas, J. de D. (2012) Resistance of Fasciola hepatica to triclabendazole in cattle of the Cajamarca countryside. Revista Veterinaria Argentina July, 1–6. Available at http://www.veterinariargentina.com/revista/2012/07/resistencia-de-fasciola-hepatica-al-triclabendazol-en-bovinos-de-la-campina-de-cajamarca-%E2%80%93-peru (accessed 21 August 2016).Google Scholar
Ross, F., Hernández, P., Porcal, W., López, G.V., Cerecetto, H., González, M., Basika, T., Carmona, C., Fló, M., Maggioli, G., Bonilla, M., Gladyshev, V.N., Boiani, M. & Salinas, G. (2012) Identification of thioredoxin glutathione reductase inhibitors that kill cestode and trematode parasites. PLoS ONE 7, e35033.Google Scholar
Ryan, L.A., Hoey, E., Trudgett, A., Fairweather, I., Fuchs, M., Robinson, M.W., Chambers, E., Timson, D.J., Ryan, E., Feltwell, T., Ivens, A., Bentley, G. & Johnston, D. (2008) Fasciola hepatica expresses multiple alpha- and beta-tubulin isotypes. Molecular and Biochemical Parasitology 159, 73–78.Google Scholar
Salinas, G., Selkirk, M.E., Chalar, C., Maizels, R.M. & Fernández, C. (2004) Linked thioredoxin-glutathione systems in platyhelminths. Trends in Parasitology 20, 340–346.Google Scholar
Sanabria, R., Ceballos, L., Moreno, L., Romero, J., Lanusse, C. & Alvarez, L. (2013) Identification of a field isolate of Fasciola hepatica resistant to albendazole and susceptible to triclabendazole. Veterinary Parasitology 193, 105–110.Google Scholar
Sanchís, J., Miguélez, S., Solari, M.A., Piñeiro, P., Macchi, M. I., Maldini, G. & Venzal, J. (2011) Seroprevalencia de la fasciolosis bovina en el departamento de Salto (Uruguay). Revista Ibero-Latinoamericana de Parasitologia 70, 163–171.Google Scholar
Santarem, V.A., Tostes, R.A., Alberti, H. & Sanches Ode, C. (2006) Fasciola hepatica in capybara. Acta Tropica 98, 311–313.Google Scholar
Scarcella, S., Fiel, C., Guzman, M., Alzola, R., Felipe, A., Hanna, R.E.B., Fairweather, I., McConnell, S. & Solana, H. (2011) Reproductive disruption in Fasciola hepatica associated with incomplete efficacy of a new experimental formulation of triclabendazole. Veterinary Parasitology 176, 157–164.Google Scholar
Scarcella, S., Lamenza, P., Virkel, G. & Solana, H. (2012) Expression differential of microsomal and cytosolic glutathione-S-transferases in Fasciola hepatica resistant at triclabendazole. Molecular and Biochemical Parasitology 181, 37–39.Google Scholar
Silva-Santos, I.C., Scaini, C.J. & Rodrigues, L.A.F. (1992) Myocastor coypus (Rodentia Capromyidae) como reservorio silvestre de Fasciola hepatica (Lineu, 1758). Revista Brasileira de Parasitologia Veterinaria 1, 27–30.Google Scholar
Simeonov, A., Jadhav, A., Sayed, A.A., Wang, Y., Nelson, M.E., Thomas, C.J., Inglese, J., Williams, D.L. & Austin, C.P. (2008) Quantitative high-throughput screen identifies inhibitors of the Schistosoma mansoni redox cascade. PLoS Neglected Tropical Diseases 2, e127.Google Scholar
Soares, M.P., da Silva, S.S., Nizoli, L.Q., Felix, S.R. & Schild, A.L. (2007) Chronic fascioliasis in farmed and wild greater rheas (Rhea americana). Veterinary Parasitology 145, 168–171.Google Scholar
Solana, H., Scarcella, S., Virkel, G., Ceriani, C., Rodríguez, J. & Lanusse, C. (2009) Albendazole enantiomeric metabolism and binding to cytosolic proteins in the liver fluke Fasciola hepatica . Veterinary Research Communications 33, 163–173.Google Scholar
Spithill, T., Smooker, P. & Copeman, D. (1999) Fasciola gigantica: epidemiology, control, immunology and molecular biology. pp. 465–525 in Dalton, J. (Ed.) Fasciolosis. Wallingford, Oxon, UK, CABI Publishers.Google Scholar
Spithill, T.W., Carmona, C., Piedrafita, D. & Smooker, P.M. (2012) Prospects for immunoprophylaxis against Fasciola hepatica (Liver Fluke). pp. 465–484 in Caffrey, C.R. (Ed.) Parasitic helminths: Targets, screens, drugs and vaccines. Weinheim, Germany, Wiley.Google Scholar
Statham, J.M.E. (2015) Control of liver fluke: an emerging issue in terms of veterinary residues. Veterinary Record 177, 519–522.Google Scholar
Teofanova, D., Hristov, P., Yoveva, A. & Radoslavov, G. (2012) Issues associated with genetic diversity studies of the liver fluke, Fasciola heptica (Platyhelminthes, Digenea, Fasciolidae). pp. 251–274 in Caliskan, M. (Ed.) Genetic diversity in microorganisms. InTech.Google Scholar
Ticona, S.D., Amanda, C.V., Casas, V.G., Chavera, C.A. & Li, E.O. (2010) Prevalencia de Fasciola hepatica en bovinos y ovinos de Vilcashuamán, Ayacucho. Revista de Investigaciones Veterinarias del Perú 21, 168–174.Google Scholar
Toet, H., Piedrafita, D.M. & Spithill, T.W. (2014) Liver fluke vaccines in ruminants: strategies, progress and future opportunities. International Journal for Parasitology 44, 915–927.Google Scholar
Ueno, H., Arandia, R., Morales, G. & Medina, G. (1975) Fascioliasis of livestock and snail host for Fasciola in the Altiplano region of Bolivia. National Institute of Animal Health Quarterly 15, 61–67.Google Scholar
Valencia-López, N., Malone, J.B., Carmona, C.G. & Velásquez, L.E. (2012) Climate-based risk models for Fasciola hepatica in Colombia. Geospatial Health 6, S67–S85.Google Scholar
Vaughan, J.L., Charles, J.A. & Boray, J.C. (1997) Fasciola hepatica infection in farmed emus (Dromaius novaehollandiae). Australian Veterinary Journal 75, 811–813.Google Scholar
Vignoles, P., Novobilsky, A., Hoeglund, J., Kasny, M., Pankrac, J., Dreyfuss, G., Pointier, J.-P. & Rondelaud, D. (2014) Lymnaea cubensis, an experimental intermediate host for Fascioloides magna . Folia Parasitologica 61, 185–188.Google Scholar
Walker, S.M., Prodohl, P.A., Fletcher, H.L., Hanna, R.E.B., Kantzoura, V., Hoey, E.M. & Trudgett, A. (2007) Evidence for multiple mitochondrial lineages of Fasciola hepatica (liver fluke) within infrapopulations from cattle and sheep. Parasitology Research 101, 117–125.Google Scholar
Wilkinson, R., Law, C.J., Hoey, E.M., Fairweather, I., Brennan, G.P. & 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.Google Scholar
Wilson, R.A., Wright, J.M., de Castro-Borges, W., Parker-Manuel, S.J., Dowle, A.A., Ashton, P.D., Young, N.D., Gasser, R.B. & Spithill, T.W. (2011) Exploring the Fasciola hepatica tegument proteome. International Journal for Parasitology 41, 1347–1359.Google Scholar
World Health Organization. (2007) Fact sheet on fascioliasis. Action against worms. pp. 1–8. Geneva, WHO.Google Scholar
Young, N.D., Hall, R.S., Jex, A.R., Cantacessi, C. & 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.Google Scholar