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Recent advances in the diagnosis, impact on production and prediction of Fasciola hepatica in cattle

Published online by Cambridge University Press:  07 November 2013

J. CHARLIER ,
J. VERCRUYSSE ,
E. MORGAN ,
J. VAN DIJK  and
D. J. L. WILLIAMS
J. CHARLIER*
Affiliation:
Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
J. VERCRUYSSE
Affiliation:
Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
E. MORGAN
Affiliation:
School of Veterinary Science, University of Bristol, Langford House, Langford, North Somerset BS40 5DU, UK
J. VAN DIJK
Affiliation:
Department of Epidemiology and Population Health, Institute of Infection and Global Health, University of Liverpool, Leahurst, Neston, Cheshire CH64 7TE, UK
D. J. L. WILLIAMS
Affiliation:
Veterinary Parasitology, Institute of Infection and Global Health, University of Liverpool, 146 Brownlow Hill, Liverpool L3 5RF, UK
*
* Corresponding author: Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium. E-mail: [email protected]
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Summary

Fasciola hepatica is a pathogenic trematode parasite of ruminants with a global distribution. Here, we briefly review the current epidemiology of bovine fasciolosis in Europe and discuss the progress made over the last decade in the diagnosis, impact on production and prediction of F. hepatica in cattle. Advances in diagnosis have led to significantly improved coprological and serological methods to detect presence of infection. Diagnostic test results have been correlated with intensity of infection and associated production losses, unravelling the impact on carcass weight and milk yield in modern cattle production systems. The economic impact of fasciolosis may, however, go beyond the direct impacts on production as evidence shows that F. hepatica can modulate the immune response to some co-infections. Control of bovine fasciolosis remains hampered by the limitations of the currently available flukicidal drugs: few drugs are available to treat dairy cows, many have low efficacies against juvenile stages of F. hepatica and there is evidence for the development of drug resistance. This makes research into the prediction of risk periods, and thus the optimum application of available drugs more pertinent. In this field, the recent research focus has been on understanding spatial risk and delivering region-specific spatial distribution maps. Further advances in epidemiological and economic research on bovine fasciolosis are expected to deliver farm-specific economic assessments of disease impact, to leverage non-chemotherapeutic management options and to enhance a more targeted use of anthelmintics.

Keywords

Fasciola hepaticaruminantimmunityglobal changeanthelminticscontrol
Type
Invited Review
Information
Parasitology , Volume 141 , Issue 3 , March 2014 , pp. 326 - 335
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Copyright © Cambridge University Press 2013 

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References

REFERENCES

Abdel-Rahman, S. M., O'Reilly, K. L. and Malone, J. B. (1998). Evaluation of a diagnostic monoclonal antibody-based capture enzyme-linked immunosorbent assay for detection of a 26- to 28-kd Fasciola hepatica coproantigen in cattle. American Journal of Veterinary Research 59, 533–537.CrossRefGoogle ScholarPubMed
Ai, L., Li, C., Elsheikha, H. M., Hong, S. J., Chen, J. X., Chen, S. H., Li, X., Cai, X. Q., Chen, M. X. and Zhu, X. Q. (2010). Rapid identification and differentiation of Fasciola hepatica and Fasciola gigantica by a loop-mediated isothermal amplification (LAMP) assay. Veterinary Parasitology 174, 228–233.CrossRefGoogle ScholarPubMed
Aitken, M. M., Hughes, D. L., Jones, P. W., Hall, G. A. and Collis, K. A. (1978). Effects of intravenous Salmonella dublin on cattle at different stages of Fasciola hepatica infection. Journal of Comparative Pathology 88, 433–442.Google Scholar
Anderson, N., Luong, T. T., Vo, N. G., Bui, K. L., Smooker, P. M. and Spithill, T. W. (1999). The sensitivity and specificity of two methods for detecting Fasciola infections in cattle. Veterinary Parasitology 83, 15–24.Google Scholar
Arias, M., Piñeiro, P., Hillyer, G. V., Suárez, J. L., Francisco, I., Cortiñas, F. J., Díez-Baños, P. and Morrondo, P. (2010). An approach of the laboratory to the field: assessment of the influence of cattle management on the seroprevalence of fascioliasis by using polyclonal- and recombinant-based ELISAs. Journal of Parasitology 96, 626–631.Google Scholar
Bennema, S. C., Ducheyne, E., Vercruysse, J., Claerebout, E., Hendrickx, G. and Charlier, J. (2011). Relative importance of management, meteorological and environmental factors in the spatial distribution of Fasciola hepatica in dairy cattle in a temperate climate zone. International Journal for Parasitology 41, 225–233.Google Scholar
Black, N. M. and Froyd, G. (1972). The possible influence of liver fluke infestation on milk quality. Veterinary Record 90, 71–72.Google Scholar
Bossaert, K., Lonneux, J.-F., Losson, B. and Peeters, J. (1999). Fasciolosis incidence forecasts in Belgium by means of climatic data. Annales de Medicine Veterinaire 143, 201–210.Google Scholar
Brady, M. T., O'Neill, S. M., Dalton, J. P. and Mills, K. H. (1999). Fasciola hepatica suppresses a protective Th1 response against Bordetella pertussis . Infection and Immunity 67, 5372–5378.Google Scholar
Charlier, J., Duchateau, L., Claerebout, E., Williams, D. and Vercruysse, J. (2007). Associations between anti-Fasciola hepatica antibody levels in bulk-tank milk samples and production parameters in dairy herds. Preventive Veterinary Medicine 78, 57–66.Google Scholar
Charlier, J., De Meulemeester, L., Claerebout, E., Williams, D. and Vercruysse, J. (2008). Qualitative and quantitative evaluation of coprological and serological techniques for the diagnosis of fasciolosis in cattle. Veterinary Parasitology 153, 44–51. doi: 10.1016/j.vetpar.2008.01.035.CrossRefGoogle ScholarPubMed
Charlier, J., Sanders, M. and Vercruysse, J. (2009 a). The direct costs of infections with gastrointestinal nematodes and liver fluke in the Flemish dairy population. Vlaams Diergeneeskundig Tijdschrift 78, 196–200.Google Scholar
Charlier, J., De Cat, A., Forbes, A. and Vercruysse, J. (2009 b). Measurement of antibodies to gastrointestinal nematodes and liver fluke in meat juice of beef cattle and associations with carcass parameters. Veterinary Parasitology 166, 235–240.CrossRefGoogle ScholarPubMed
Charlier, J., Bennema, S. C., Caron, Y., Counotte, M., Ducheyne, E., Hendrickx, G. and Vercruysse, J. (2011). Towards assessing fine-scale indicators for the spatial transmission risk of Fasciola hepatica in cattle. Geospatial Health 5, 239–245.CrossRefGoogle ScholarPubMed
Charlier, J., Hostens, M., Jacobs, J., Van Ranst, B., Duchateau, L. and Vercruysse, J. (2012 a). Integrating fasciolosis control in the dry cow management: the effect of closantel treatment on milk production. PLoS ONE 7, e43216.CrossRefGoogle ScholarPubMed
Charlier, J., van der Voort, M., Hogeveen, H. and Vercruysse, J. (2012 b). ParaCalc® – a novel tool to estimate the costs of worm infections on the dairy herd. Veterinary Parasitology 184, 204–211.CrossRefGoogle Scholar
Charlier, J., Meyns, T., Soenen, K. and Vercruysse, J. (2013). Monitoring gastrointestinal nematode and liver fluke infections in Belgium by bulk tank milk ELISA: are we making progress in parasite control? Vlaams Diergeneeskundig Tijdschrift 82, 17–22.Google Scholar
Claridge, J., Diggle, P., McCann, C. M., Mulcahy, G., Flynn, R., McNair, J., Strain, S., Welsh, M., Baylis, M. and Williams, D. J. L. (2012). Fasciola hepatica is associated with the failure to detect bovine tuberculosis in dairy cattle. Nature Communications 3, 853.Google Scholar
Conceição, M. A. P., Durao, R. M., Costa, I. H. and da Costa, J. M. C. (2002). Evaluation of a simple sedimentation method (modified McMaster) for diagnosis of bovine fascioliosis. Veterinary Parasitology 105, 337–343. doi: Pii S0304-4017(02)00016-X. CrossRefGoogle ScholarPubMed
Conceição, M. A. P., Durao, R. M. B., Costa, I. M. H., Castro, A., Louza, A. C. and Costa, J. C. (2004). Herd-level seroprevalence of fasciolosis in cattle in north central Portugal. Veterinary Parasitology 123, 93–103.Google Scholar
Cornelissen, J. B. W. J., Gaasenbeek, C. P. H., Boersma, W., Borgsteede, F. H. M. and van Milligen, F. J. (1999). Use of a pre-selected epitope of cathepsin-L-1 in a highly specific peptide-based immunoassay for the diagnosis of Fasciola hepatica infections in cattle. International Journal for Parasitology 29, 685–696. doi: 10.1016/S0020-7519(99)00017-X.CrossRefGoogle Scholar
Cringoli, G., Rinaldi, L., Veneziano, V., Capelli, G. and Malone, J. B. (2002). A cross-sectional coprological survey of liver flukes in cattle and sheep from an area of the southern Italian Apennines. Veterinary Parasitology 108, 137–143.Google Scholar
Dalton, J. P. (ed.) (1999). Fasciolosis. CABI, Wallingford, UK.Google Scholar
Dalton, J. P., Robinson, M. W., Mulcahy, G., O'Neill, S. M. and Donnelly, S. (2013). Immunomodulatory molecules of Fasciola hepatica: candidates for both vaccine and immunotherapeutic development. Veterinary Parasitology 195, 272–285.Google Scholar
Dargie, J. D. (1987). The impact on production and mechanisms of pathogenesis of trematode infections in cattle and sheep. International Journal for Parasitology 17, 453–463.Google Scholar
Durr, P. A., Tait, N. and Lawson, A. B. (2005). Bayesian hierarchical modeling to enhance the epidemiological value of abattoir surveys for bovine fasciolosis. Preventative Veterinary Medicine 71, 157–172.Google Scholar
Duscher, R., Duscher, G., Hofer, J., Tichy, A., Prosl, H. and Joachim, A. (2011). Fasciola hepatica – Monitoring the milky way? The use of tank milk for liver fluke monitoring in dairy herds as base for treatment strategies. Veterinary Parasitology 178, 273–278. doi: 10.1016/j.vetpar.2011.01.040.Google Scholar
Espino, A. M. and Finlay, C. M. (1994). Sandwich enzyme-linked-immunosorbent-assay for detection of excretory-secretory antigens in humans with fascioliasis. Journal of Clinical Microbiology 32, 190–193.Google Scholar
Fairweather, I. (2011). Reducing the future threat from (liver) fluke: realistic prospect or quixotic fantasy? Veterinary Parasitology 180, 133–143.Google Scholar
Fairweather, I. and Boray, J. C. (1999). Fasciolicides: efficacy, actions, resistance and its management. Veterinary Journal 158, 81–112.Google Scholar
Flanagan, A., Edgar, H. W. J., Gordon, A., Hanna, R. E. B., Brennan, G. P. and Fairweather, I. (2011). 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.Google Scholar
Flynn, R. J., Irwin, J. A., Olivier, M., Sekiya, M., Dalton, J. P. and Mulcahy, G. (2007). Alternative activation of ruminant macrophages by Fasciola hepatica . Veterinary Immunology and Immunopathology 120, 31–40.Google Scholar
Flynn, R. J., Mulcahy, G., Welsh, M., Cassidy, J. P., Corbett, D., Milligan, C., Andersen, P., Strain, S. and McNair, J. (2009). Co-infection of cattle with Fasciola hepatica and mycobacterium bovis – immunological consequences. Transboundary and Emerging Diseases 56, 269–274.CrossRefGoogle ScholarPubMed
Fox, N. J., White, P. C. L., 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.Google Scholar
Gaasenbeek, C. P. H., Over, H. J., Noorman, N. and de Leeuw, W. A. (1992). An epidemiological study of Fasciola hepatica in the Netherlands. Veterinary Quarterly 14, 140–144.CrossRefGoogle ScholarPubMed
Gettinby, G., Hope-Cawdery, M. J. and Grainger, J. N. R. (1974). Forecasting the incidence of fascioliasis from climatic data. International Journal of Biometeorology 18, 319–323.CrossRefGoogle ScholarPubMed
Golden, O., Flynn, R. J., Read, C., Sekiya, M., Donnelly, S. M., Stack, C., Dalton, J. P. and Mulcahy, G. (2010). Protection of cattle against a natural infection of Fasciola hepatica by vaccination with recombinant cathepsin L1 (rFhCL1). Vaccine 28, 5551–5557.Google Scholar
Gordon, D. K., Zadoks, R. N., Stevenson, H., Sargison, N. D. and Skuce, P. J. (2012). On farm evaluation of the coproantigen ELISA and coproantigen reduction test in Scottish sheep naturally infected with Fasciola hepatica . Veterinary Parasitology 187, 436–444.Google Scholar
Höglund, J., Dahlstrom, F., Engstrom, A., Hessle, A., Jakubek, E. B., Schnieder, T., Strube, C. and Sollenberg, S. (2010). Antibodies to major pasture borne helminth infections in bulk-tank milk samples from organic and nearby conventional dairy herds in south-central Sweden. Veterinary Parasitology 171, 293–299.Google Scholar
Kemper, N. and Henze, C. (2009). Effects of pastures’ re-wetting on endoparasites in cattle in northern Germany. Veterinary Parasitology 161, 302–306.CrossRefGoogle ScholarPubMed
Kenyon, F., Sargison, N. D., Skuce, P. J. and Jackson, F. (2009). Sheep helminth parasitic disease in south eastern Scotland arising as a possible consequence of climate change. Veterinary Parasitology 163, 293–297.CrossRefGoogle ScholarPubMed
Kuerpick, B., Fiedor, C., von Samson-Himmelstjerna, G., Schnieder, T. and Strube, C. (2012). Bulk milk-estimated seroprevalence of Fasciola hepatica in dairy herds and collecting of risk factor data in East Frisia, northern Germany. Berliner und Munchener Tierarztliche Wochenschrift 125, 345–350.Google ScholarPubMed
Kuerpick, B., Conraths, F. J., Staubach, C., Schnieder, T. and Strube, C. (2013 a). Seroprevalence and GIS-supported risk factor analysis of Fasciola hepatica-infections in dairy herds in Germany. Parasitology 140, 1051–1060.Google Scholar
Kuerpick, B., Schnieder, T. and Strube, C. (2013 b). Evaluation of a recombinant cathepsin L1 ELISA and comparison with the Pourquier and ES ELISA for the detection of antibodies against Fasciola hepatica . Veterinary Parasitology 193, 206–213.CrossRefGoogle ScholarPubMed
Leblanc, S., Lissemore, K. D., Kelton, D. F., Duffield, T. F. and Leslie, K. E. (2006). Major advances in disease prevention in dairy cattle. Journal of Dairy Science 89, 1267–1279.Google Scholar
Lindberg, A., Brownlie, J., Gunn, G. J., Houe, H., Moennig, V., Saatkamp, H. W., Sandvik, T. and Valle, P. S. (2006). The control of bovine viral diarrhoea virus in Europe: today and in the future. Revue Scientifique et Technique – Office International des Epizooties 25, 961–979.Google Scholar
Lopez-Diaz, M. C., Carro, M. C., Cadorgina, C., Diez-Banos, P. and Mezo, M. (1998). Puberty and serum concentrations of ovarian steroids during prepuberal period in Friesian heifers artificially infected with Fasciola hepatica . Theriogenology 50, 587–593.Google Scholar
Loyacano, A. F., Williams, J. C., Gurie, J. and DeRosa, A. A. (2002). Effect of gastrointestinal nematode and liver fluke infections on weight gain and reproductive performance of beef heifers. Veterinary Parasitology 107, 227–234.Google Scholar
Malone, J. B., Williams, T. E., Muller, R. A., Geaghan, J. P. and Loyacano, A. F. (1987). Fascioliasis in cattle in Louisiana, USA – development of a system to predict disease risk by climate using the Thornthwaite Water Budget. American Journal of Veterinary Research 48, 1167–1170.Google Scholar
Malone, J. B., Fehler, D. P., Loyacano, A. F. and Zukowski, S. H. (1992). Use of Landsat MSS imagery and soil type in a geographical information system to assess site specific risk on Red River basin farms in Louisiana. Annals of the New York Academy of Science 653, 389–397.CrossRefGoogle Scholar
Martinez-Perez, J. M., Robles-Perez, D., Rojo-Vazquez, F. A. and Martinez-Valladares, M. (2012). Comparison of three different techniques to diagnose Fasciola hepatica infection in experimentally and naturally infected sheep. Veterinary Parasitology 190, 80–86.Google Scholar
Mas-Coma, S., Valero, M. A. and Bargues, M. D. (2008). Effects of climate change on animal and zoonotic helminthiases. Revue scientifique et technique – Office Internationale des Epizooties 27, 443–457.Google Scholar
Matt, M., Schopf, K. and Mader, C. (2007). Leberegelmonitoring: flächendeckende serologische Untersuchungen zm Fasciola hepatica-Befall in Tirol. Wiener Tierarztliche Monatsschrifte 94, 210–213.Google Scholar
McCann, C. M., Baylis, M. and Williams, D. J. L. (2010 a). Seroprevalence and spatial distribution of Fasciola hepatica-infected dairy herds in England and Wales. Veterinary Record 166, 612–617.CrossRefGoogle ScholarPubMed
McCann, C. M., Baylis, M. and Williams, D. J. L. (2010 b). The development of linear regression models using environmental variables to explain the spatial distribution of Fasciola hepatica infection in dairy herds in England and Wales. International Journal for Parasitology 40, 1021–1028.Google Scholar
McIlroy, S. G., Goodall, E. A., Stewart, D. A., Taylor, S. M. and McCracken, R. M. (1990). A computerised system for the accurate forecasting of the annual prevalence of fasciolosis. Preventative Veterinary Medicine 9, 27–35.Google Scholar
Mezo, M., Gonzalez-Warleta, M., Carro, C. and Ubeira, F. M. (2004). An ultrasensitive capture ELISA for detection of Fasciola hepatica coproantigens in sheep and cattle using a new monoclonal antibody (MM3). Journal of Parasitology 90, 845–852.Google Scholar
Mezo, M., Gonzalez-Warleta, M. and Ubeira, F. M. (2007). The use of MM3 monoclonal antibodies for the early immunodiagnosis of ovine fascioliasis. Journal of Parasitology 93, 65–72.CrossRefGoogle ScholarPubMed
Mezo, M., Gonzalez-Warleta, M., Castro-Hermida, J. A., Muino, L. and Ubeira, F. M. (2010). Field evaluation of the MM3-SERO ELISA for detection of anti-Fasciola IgG antibodies in milk samples from individual cows and bulk milk tanks. Parasitology International 59, 610–615.Google Scholar
Mezo, M., González-Warleta, M., Castro-Hermida, J. A., Muiño, L. and Ubeira, F. M. (2011). Association between anti-F. hepatica antibody levels in milk and production losses in dairy cows. Veterinary Parasitology 180, 237–242.Google Scholar
Miller, C. M. D., Smith, N. C., Ikin, R. J., Boulter, N. R., Dalton, J. P. and Donnelly, S. (2009). Immunological interactions between 2 common pathogens, Th1-inducing protozoan Toxoplasma gondii and the Th2-inducing helminth Fasciola hepatica . PLoS ONE 4, e5692.CrossRefGoogle ScholarPubMed
Molloy, J. B., Anderson, G. R., Fletcher, T. I., Landmann, J. and Knight, B. C. (2005). Evaluation of a commercially available enzyme-linked immunosorbent assay for detecting antibodies to Fasciola hepatica and Fasciola gigantica in cattle, sheep and buffaloes in Australia. Veterinary Parasitology 130, 207–212.Google Scholar
Morgan, E. R., Charlier, J., Hendrickx, G., Biggeri, A., Catalan, D., von Samson-Himmelstjerna, G., Demeler, J., Müller, E., van Dijk, J., Kenyon, F., Skuce, P., Höglund, J., O'Kiely, P., Van Ranst, B., de Waal, T., Rinaldi, L., Cringoli, G., Torgerson, P., Hertzberg, H., Wolstenholme, A. and Vercruysse, J. (2013). Global change and helminth infections in grazing ruminants: impacts, trends and sustainable solutions. Agriculture 3, 484–502.CrossRefGoogle Scholar
Muino, L., Perteguer, M. J., Garate, T., Martinez-Sernandez, V., Beltran, A., Romaris, F., Mezo, M., Gonzalez-Warleta, M. and Ubeira, F. M. (2011). Molecular and immunological characterization of Fasciola antigens recognized by the MM3 monoclonal antibody. Molecular and Biochemical Parasitology 179, 80–90.Google Scholar
Nardelli, S., Farina, G., Lucchini, R., Valorz, C., Moresco, A., Dal Zotto, R. and Costanzi, C. (2008). Dynamics of infection and immunity in a dairy cattle population undergoing an eradication programme for Infectious Bovine Rhinotracheitis (IBR). Preventive Veterinary Medicine 85, 68–80.CrossRefGoogle Scholar
Ollerenshaw, C. B. and Rowlands, W. T. (1959). A method of forecasting the incidence of fascioliasis in Anglesey. Veterinary Record 71, 591–598.Google Scholar
Pfister, K. and Koch, S. (2004). Preliminary results from milk-serological studies on Fasciola hepatica infections in Bavarian dairy herds. Tierarztliche Praxis Ausgabe Grosstiere Nutztiere 32, 316–319.Google Scholar
Pritchard, G. C., Forbes, A. B., Williams, D. J., Salimi-Bejestani, M. R. and Daniel, R. G. (2005). Emergence of fasciolosis in cattle in East Anglia. Veterinary Record 157, 578–582.Google Scholar
Rapsch, C., Schweizer, G., Grimm, F., Kohler, L., Bauer, C., Deplazes, P., Braun, U. and Torgerson, P. R. (2006). Estimating the true prevalence of Fasciola hepatica in cattle slaughtered in Switzerland in the absence of an absolute diagnostic test. International Journal for Parasitology 36, 1153–1158.Google Scholar
Reichel, M. P. (2002). Performance characteristics of an enzyme-linked immunosorbent assay for the detection of liver fluke (Fasciola hepatica) infection in sheep and cattle. Veterinary Parasitology 107, 65–72.Google Scholar
Reichel, M. P., Vanhoff, K. and Baxter, B. (2005). Performance characteristics of an enzyme-linked immunosorbent assay performed in milk for the detection of liver fluke (Fasciola hepatica) infection in cattle. Veterinary Parasitology 129, 61–66.Google Scholar
Salem, A., Chauvin, A., Braun, J. P., Jacquiet, P. H. and Dorchies, P. H. (2011). Comparison of six methods for detection of Fasciola hepatica in naturally infected cattle. Revue De Medecine Veterinaire 162, 18–24.Google Scholar
Salimi-Bejestani, M. R., McGarry, J. W., Felstead, S., Ortiz, P., Akca, A. and Williams, D. J. L. (2005). Development of an antibody-detection ELISA for Fasciola hepatica and its evaluation against a commercially available test. Research in Veterinary Science 78, 177–181.CrossRefGoogle ScholarPubMed
Salimi-Bejestani, M. R., Daniel, R., Cripps, P., Felstead, S. and Williams, D. J. L. (2007). Evaluation of an enzyme-linked immunosorbent assay for detection of antibodies to Fasciola hepatica in milk. Veterinary Parasitology 149, 290–293.Google Scholar
Salimi-Bejestani, M. R., Cripps, P. and Williams, D. J. L. (2008). Evaluation of an ELISA to assess the intensity of Fasciola hepatica infection in cattle. Veterinary Record 162, 109–111.Google Scholar
Sánchez-Andrade, R., Paz-Silva, A., Suárez, J., Panadero, R., Díez-Baños, P. and Morrondo, P. (2000). Use of a sandwich-enzyme-linked immunosorbent assay (SEA) for the diagnosis of natural Fasciola hepatica infection in cattle from Galicia (NW Spain). Veterinary Parasitology 93, 39–46.Google Scholar
Sanchez-Vazques, M. J. and Lewis, F. I. (2013). Investigating the impact of fasciolosis on cattle carcase performance. Veterinary Parasitology 193, 307–311.Google Scholar
Schweizer, G., Braun, U., Deplazes, P. and Torgerson, P. R. (2005). Estimating the financial losses due to bovine fasciolosis in Switzerland. Veterinary Record 157, 188–193.Google Scholar
Simsek, S., Risvanli, A., Utuk, A. E., Yuksel, M., Saat, N. and Koroglu, E. (2007). Evaluation of relationship between repeat breeding and Fasciola hepatica and hydatid cyst infections in cows in Elazig district of eastern Turkey. Research in Veterinary Science 83, 102–104.Google Scholar
Smith, G. (2011). Models of macroparasitic infections in domestic ruminants: a conceptual review and critique. Revue Scientifique et Technique de l'Office International des Epizooties 30, 447–456.Google Scholar
Sutmoller, P., Barteling, S. S., Olascoaga, R. C. and Sumption, K. J. (2003). Control and eradication of foot-and-mouth disease. Virus Research 91, 101–144.Google Scholar
Tailliez, R. and Korach, S. (1970). Les antigènes de Fasciola hepatica – Isolement et caractérisation d’ un antigène spécifique du genre. Annales de l’ Institut Pasteur 118, 61–78.Google Scholar
Torgerson, P. and Claxton, J. (1999). Epidemiology and control. In Fasciolosis (ed. Dalton, J. P.), pp. 113–149. CABI Publishing, Wallingford, UK.Google Scholar
Tum, S., Puotinen, M. L. and Copeman, D. B. (2004). A geographic information system model for mapping risk of fasciolosis in cattle and buffaloes in Cambodia. Veterinary Parasitology 122, 141–149.Google Scholar
Vaessen, M. A., Veling, J., Frankena, K., Graat, E. A. and Klunder, T. (1998). Risk factors for Salmonella dublin infection on dairy farms. Veterinary Quarterly 20, 97–99.Google Scholar
van der Voort, M., Charlier, J., Lauwers, L., Vercruysse, J., Van Huylenbroeck, G. and Van Meensel, J. (2013). Conceptual framework for analysing farm-specific economic effects of helminth infections in ruminants and control strategies. Preventive Veterinary Medicine 109, 228–235.Google Scholar
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 3, 377–392.CrossRefGoogle Scholar
Vercruysse, J. and Claerebout, E. (2001). Treatment vs. non-treatment of helminth infections in cattle: defining the threshold. Veterinary Parasitology 98, 195–214.Google Scholar
Yilma, J. M. and Malone, J. B. (1998). A geographic information system forecast model for strategic control of fasciolosis in Ethiopia. Veterinary Parasitology 78, 103–127.Google Scholar