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Epidemiological investigation of a severe rumen fluke outbreak on an Irish dairy farm

Published online by Cambridge University Press:  16 November 2017

James O'Shaughnessy
Affiliation:
Department of Agriculture, Food and the Marine, Backweston, Celbridge, Co. Kildare, Ireland
Andres Garcia-Campos
Affiliation:
UCD Veterinary Sciences Centre, University College Dublin, Belfield, Dublin 4, Ireland
Conor G. McAloon
Affiliation:
UCD Veterinary Sciences Centre, University College Dublin, Belfield, Dublin 4, Ireland
Seamus Fagan
Affiliation:
Regional Veterinary Laboratory, Coosan, Athlone, Co. Westmeath, Ireland
Theo de Waal
Affiliation:
UCD Veterinary Sciences Centre, University College Dublin, Belfield, Dublin 4, Ireland
Maire McElroy
Affiliation:
Department of Agriculture, Food and the Marine, Backweston, Celbridge, Co. Kildare, Ireland
Micheal Casey
Affiliation:
Department of Agriculture, Food and the Marine, Backweston, Celbridge, Co. Kildare, Ireland
Barbara Good
Affiliation:
Teagasc, Animal & Grassland Research and Innovation Centre, Mellows Campus, Athenry, Co. Galway, Ireland
Grace Mulcahy
Affiliation:
UCD Veterinary Sciences Centre, University College Dublin, Belfield, Dublin 4, Ireland
John Fagan
Affiliation:
Regional Veterinary Laboratory, Coosan, Athlone, Co. Westmeath, Ireland
Denise Murphy
Affiliation:
Regional Veterinary Laboratory, Coosan, Athlone, Co. Westmeath, Ireland
Annetta Zintl*
Affiliation:
UCD Veterinary Sciences Centre, University College Dublin, Belfield, Dublin 4, Ireland
*
Author for correspondence: Annetta Zintl, E-mail: [email protected]

Abstract

Although the rumen fluke, Calicophoron daubneyi is now very common and widespread throughout Western Europe, reports of clinical cases are still rare. This study explores the epidemiological background to a severe rumen fluke outbreak in 6-month-old heifers on a dairy farm in Ireland. Sequence analysis of the cytochrome oxidase subunit 1 (Cox1) gene of the rumen fluke metacercariae on pasture failed to identify predominant, possibly pathogenic subtypes. However, estimates of metacercarial load indicated that the animals were exposed to a daily dose of about 5334 C. daubneyi metacercariae for a period of 3 weeks resulting in the build-up of very large numbers of immature worms in the small intestine. It is hypothesized that specific environmental conditions may favour this parasite over its competitor, the liver fluke, Fasciola hepatica, possibly by allowing it to emerge earlier. The possibility that C. daubneyi may be better adapted to the Irish climate than F. hepatica together with the fact that selective treatment against F. hepatica effectively frees the niche for C. daubneyi, may result in the gradual replacement of F. hepatica by C. daubneyi.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

*

Joint first authors

References

Abrous, M, Rondelaud, D and Dreyfuss, G (1999) Paramphistomum daubneyi and Fasciola hepatica: influence of temperature changes on the shedding of cercariae from dually infected Lymnaea truncatula. Parasitology Research 85, 765769.Google Scholar
Anon (2016) Northern Ireland disease surveillance report, July to September 2016. Veterinary Record 179, 482485.CrossRefGoogle Scholar
Bargues, MD, Vigo, M, Horak, P, Dvorak, J, Patzner, RA, Pointier, JP, Jackiewicz, M, Meier-Brook, C and Mas-Coma, S (2001) European Lymnaeidae (Mollusca: Gastropoda), intermediate hosts of trematodiases, based on nuclear ribosomal DNA ITS-2 sequences. Infection, Genetics and Evolution 1, 85107.Google Scholar
Carmona, C, Dowd, AJ, Smith, AM and Dalton, JP (1993) Cathepsin L proteinase secreted by Fasciola hepatica in vitro prevents antibody-mediated eosinophil attachment to newly excysted juveniles. Molecular and Biochemical Parasitology 62, 917.Google Scholar
Dawes, B and Hughes, D (1970) Fascioliasis: the invasive stages in mammals. Advances in Parasitology 8, 259274.CrossRefGoogle ScholarPubMed
Deplazes, P, Eckert, J, Mathis, A, Samson-Himmelstjerna, GV and Zahner, H (2016) Parasitology in Veterinary Medicine, 1st edn. The Netherlands: Wageningen Academic Publishers.Google Scholar
Dinnik, J (1962) Paramphistomum daubneyi sp. nov. from cattle and its snail host in the Kenya Highlands. Parasitology 52, 143151.Google Scholar
Dreyfuss, G, Abrous, A, Vignoles, P and Rondelaud, D (2004) Fasciola hepatica and Paramphistomum daubneyi: vertical distribution of metacercariae on plants under natural conditions. Parasitology Research 94, 7073.Google Scholar
Dreyfuss, G, Vignoles, P, Rondelaud, D and Cabaret, J (2015) The Mud Snail (Galba truncatula) Ecology, Parasitism and Control. Saarbruecken, Germany: Lambert Academic Publishing, pp. 97123.Google Scholar
Fuertes, M, Pérez, V, Benavides, J, González-Lanza, MC, Mezo, M, González-Warleta, M, Giráldez, FJ, Fernández, M, Manga-González, MY and Ferreras, MC (2015) Pathological changes in cattle naturally infected by Calicophoron daubneyi adult flukes. Veterinary Parasitology 209, 188196.Google Scholar
González-Warleta, M, Lladosa, S, Castro-Hermida, JA, Martínez-Ibeas, AM, Conesa, D, Muñoz, F, López-Quílez, A, Manga-González, Y and Mezo, M (2013) Bovine paramphistomosis in Galicia (Spain): prevalence, intensity, aetiology and geospatial distribution of the infection. Veterinary Parasitology 191, 252263.Google Scholar
Gordon, DK, Roberts, LCP, Lean, N, Zadoks, RN, Sargison, ND and Skuce, PJ (2013) Identification of the rumen fluke, Calicophoron daubneyi, in GB livestock: possible implications for liver fluke diagnosis. Veterinary Parasitology 195, 6571.Google Scholar
Horak, IG (1971) Paramphistomiasis of domestic ruminants. Advances in Parasitolgoy 9, 3372.Google Scholar
Iglesias-Piñeiro, J, González-Warleta, M, Castro-Hermida, JA, Córdoba, M, González-lanza, C, Manga-González, Y and Mezo, M (2016) Transmission of Calicophoron daubneyi and Fasciola hepatica in Galicia (Spain): temporal follow-up in the intermediate and definitive hosts. Parasites & Vectors 9, 610.CrossRefGoogle ScholarPubMed
Jones, RA, Williams, HW, Dalesman, S and Brophy, PM (2015) Confirmation of Galba truncatula as an intermediate host snail for Calicophoron daubneyi in Great Britain, with evidence of alternative snail species hosting Fasciola hepatica. Parasites & Vectors 8, 656.Google Scholar
Jones, RA, Brophy, PM, Mitchell, ES and Williams, HWYN (2017a) Rumen fluke (Calicophoron daubneyi) on Welsh farms: prevalence, risk factors and observations on co-infection with Fasciola hepatica. Parasitology 144, 237247.Google Scholar
Jones, RA, Dalesman, S, Ayodeji, S, Thomas, RK and Brophy, PM (2017b) The prevalence and development of digenean parasites within their intermediate snail host, Galba truncatula, in a geographic area where the presence of Calicophoron daubneyi has recently been confirmed. Veterinary Parasitology 240, 6874.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.Google Scholar
Macan, T (1960) A Key to the British Fresh and Brackish Water Gastropods: With Notes on Their Ecology. Iver, Buckinghamshire, UK: Freshwater Biological Association, Scientific Publication, 13.Google Scholar
Mage, C, Bourgne, H, Toullieu, J-M, Rondelaud, D and Dreyfuss, G (2002) Fasciola hepatica and Paramphistomum daubneyi: changes in prevalences of natural infections in cattle and in Lymnaea truncatula from central France over the past 12 years. Veterinary Research 33, 439447.Google Scholar
Malrait, K, Verschave, S, Skuce, P, Van Loo, H, Vercruysse, J and Charlier, J (2015) Novel insights into the pathogenic importance, diagnosis and treatment of the rumen fluke (Calicophoron daubneyi) in cattle. Veterinary Parasitology 207, 134139.Google Scholar
Martínez-Ibeas, AM, González-Warleta, M, Martínez-Valladares, M, Castro-Hermida, JA, González-Lanza, C and Mi, B (2013) Rumen fluke in Irish sheep: prevalence, risk factors and molecular identification of two paramphistome species. BMC Veterinary Research 12, 143.Google Scholar
Martinez-Ibeas, AM, Munita, MP, Lawlor, K, Sekiya, M, Mulcahy, G and Sayers, R (2016) Development and validation of a mtDNA multiplex PCR for identification and discrimination of Calicophoron daubneyi and Fasciola hepatica in the Galba truncatula snail. Veterinary Parasitology 195, 5764.Google Scholar
Mason, C, Stevenson, H, Cox, A and Dick, I (2012) Sheep health: disease associated with immature paramphistome infection in sheep. Veterinary Record 170, 343344.Google Scholar
Millar, M, Colloff, A and Scholes, S (2012) Bovine health: disease associated with immature paramphistome infection. Veterinary Record 171, 509510.Google Scholar
Ministry of Agriculture, Fisheries and Food (MAFF) (1986). Manual of Veterinary Parasitological Laboratory Techniques. Reference book 418. London, UK: Her Majesty's Stationary Office.Google Scholar
Murphy, TM, Power, EP, Sanchez-Miguel, C, Casey, MJ, Toolan, DP and Fagan, JG (2008) Paramphistomosis in Irish cattle. Veterinary Record 162, 831.Google Scholar
National Research Council (NRC) (2001). Nutrient Requirements of Dairy Cattle, 7th edn. Washington: NAS.Google Scholar
Rondelaud, D, Vignoles, P and Dreyfuss, G (2007) Parasite development and visceral pathology in Galba truncatula co-infected with Fasciola hepatica and Paramphistomum daubneyi. Parasitology 81, 317322.Google Scholar
Rondelaud, D, Vignoles, P and Dreyfuss, G (2016) Larval trematode infections in Galba truncatula (Gastropoda, Lymnaeidae) from the Brenne Regional Natural Park, central France. Journal of Helminthology 90, 256261.CrossRefGoogle ScholarPubMed
SAC (2016) Immature rumen fluke cause deaths of ewes. Veterinary Record 179, 538543.Google Scholar
Taylor, E (1939) Technique for the estimation of pasture infestation by strongyloid larvae. Parasitology 31, 473478.Google Scholar
Toolan, DP, Mitchell, G, Searle, K, Sheehan, M, Skuce, PJ and Zadoks, RN (2015) Bovine and ovine rumen fluke in Ireland – prevalence, risk factors and species identity based on passive veterinary surveillance and abattoir findings. Veterinary Parasitology 212, 168174.Google Scholar
Toole, AO, Browne, JA, Hogan, S, Bassière, T, Dewaal, T, Mulcahy, G and Zintl, A (2014) Identity of rumen fluke in deer. Parasitology Research 113, 40974103.Google Scholar
Zintl, A, Garcia-Campos, A, Trudgett, A, Chryssafidis, AL, Talavera-Arce, S, Fu, Y, Egan, S, Lawlor, A, Negredo, C, Brennan, G, Hanna, RE, De Waal, T and Mulcahy, G (2014) Bovine paramphistomes in Ireland. Veterinary Parasitology 204, 199208.Google Scholar