Seasonal variation of Fasciola hepatica antibodies in dairy herds in Northern Ireland measured by bulk tank milk ELISA
Bovine fasciolosis, caused by the infection of the trematode parasite Fasciola hepatica, remains a problem in dairy herds causing significant production losses. In this study, bulk milk tank samples were utilised to generate a comprehensive survey of the variation in liver fluke exposure over the four seasons of 2016 in Northern Ireland (NI). Samples were tested using an antibody ELISA test; within-herd prevalence levels were categorised relative to sample-to-positive ratio (S/P%). Overall, 1494 herds (~ 50% of all active dairy farms in NI) were sampled. In total, 5750 samples were tested with 91% of herds having a sample result for each season. The proportion of herds with evidence of liver fluke exposure was very high across the year, with 93.03% of all bulk milk samples having some indication of liver fluke antibody presence. A high proportion of samples (2187/5750; 38.03%) fell within the highest infection class (indicating high within-herd prevalence). There was significant seasonal variation in the mean S/P%. A multivariable random effect ordinal logit model suggested that the greatest probability of being in a higher infection class was in winter, whilst the lowest was recorded during summer. There was a significant negative association between increasing herd liver fluke infection class and herd size. Furthermore, there was significant variation in infection levels across regions of Northern Ireland, with higher infection levels in northern administrative areas. This study demonstrates the very high liver fluke exposure in this region of Europe, and that risk is not equally distributed spatially or across seasons in dairy herds.
KeywordsBovine fascioliasis Dairy farming Trematode infection Parasite control Geographic risk
The authors would like to thank the Brucella laboratory team in DSIB, AFBI, for kind assistance with this project, especially Sharon Cassidy-Collins. We would also like to acknowledge cooperation of the dairies with the project.
Funding was received as part of a broader project on endemic diseases in Northern Ireland and co-infection of bovine tuberculosis (grant no. 15/3/10) by the Department of Agriculture, Environment and Rural Development.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- AFBI (2016a) Autumn and winter liver fluke forecast for Northern Ireland 2014–2015. In: Agri-Food Biosci. Inst. https://www.afbini.gov.uk/news/autumn-and-winter-liver-fluke-forecast-northern-ireland-2014-2015. Accessed 9 Aug 2017
- AFBI (2016b) Autumn and winter fluke forecast high for Northern Ireland. In: Farmers Wkly. http://www.fwi.co.uk/livestock/autumn-and-winter-fluke-forecast-high-for-nothern-ireland.htm. Accessed 9 Aug 2017
- AHI (2011) Liver fluke—the facts. Animal Health Ireland, Parasite control leaflet series, Leitrim, IrelandGoogle Scholar
- Bennema S, Vercruysse J, Claerebout E, Schnieder T, Strube C, Ducheyne E, Hendrickx G, Charlier J (2009) The use of bulk-tank milk ELISAs to assess the spatial distribution of Fasciola hepatica, Ostertagia ostertagi and Dictyocaulus viviparus in dairy cattle in Flanders (Belgium). Vet Parasitol 165:51–57. https://doi.org/10.1016/j.vetpar.2009.07.006 CrossRefPubMedGoogle Scholar
- Bennema SC, Ducheyne E, Vercruysse J, Claerebout E, Hendrickx G, 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. Int J Parasitol 41:225–233. https://doi.org/10.1016/j.ijpara.2010.09.003 CrossRefPubMedGoogle Scholar
- Bloemhoff Y, Forbes A, Danaher M, Good B, Morgan E, Mulcahy G, Sekiya M, Sayers R (2015) Determining the prevalence and seasonality of Fasciola hepatica in pasture-based dairy herds in Ireland using a bulk tank milk ELISA. Ir Vet J 68:16. https://doi.org/10.1186/s13620-015-0042-5 CrossRefPubMedPubMedCentralGoogle Scholar
- Byrne AW, McBride S, Lahuerta-Marin A, Guelbenzu M, McNair J, Skuce RA, McDowell SWJ (2016) Liver fluke (Fasciola hepatica) infection in cattle in Northern Ireland: a large-scale epidemiological investigation utilising surveillance data. Parasit Vectors 9:209. https://doi.org/10.1186/s13071-016-1489-2 CrossRefPubMedPubMedCentralGoogle Scholar
- Duscher R, Duscher G, Hofer J, Tichy A, Prosl H, 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. Vet Parasitol 178:273–278. https://doi.org/10.1016/j.vetpar.2011.01.040 CrossRefPubMedGoogle Scholar
- Höglund J, Dahlström F, Engström A, Hessle A, Jakubek EB, Schnieder T, Strube C, 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. Vet Parasitol 171:293–299CrossRefPubMedGoogle Scholar
- Hutchinson GW, Macarthur E (2003) Validation of French antibody ELISA for liver fluke. On farm, Meat and Livestock AustraliaGoogle Scholar
- Innocent GT, Gilbert L, Jones EO, McLeod JE, Gunn G, McKendrick IJ, Albon SD (2017) Combining slaughterhouse surveillance data with cattle tracing scheme and environmental data to quantify environmental risk factors for liver fluke in cattle. Front Vet Sci 4:65CrossRefPubMedPubMedCentralGoogle Scholar
- Lahuerta-Marin A, Gallagher M, McBride S, Skuce R, Menzies F, McNair J, McDowell SWJ, Byrne AW (2015) Should they stay, or should they go? Relative future risk of bovine tuberculosis for interferon-gamma test-positive cattle left on farms. Vet Res 46:90. https://doi.org/10.1186/s13567-015-0242-8 CrossRefPubMedPubMedCentralGoogle Scholar
- Mazeri S, Sargison N, Kelly RF, Bronsvoort BMC, Handel I (2016) Evaluation of the performance of five diagnostic tests for Fasciola hepatica infection in naturally infected cattle using a bayesian no gold standard approach. PLoS One 11:e0161621. https://doi.org/10.1371/journal.pone.0161621 CrossRefPubMedPubMedCentralGoogle Scholar
- MET Office (2016) Northern Ireland: climate. In: Met Off. http://www.metoffice.gov.uk/climate/uk/regional-climates/ni. Accessed 10 Aug 2017
- Molloy JB, Anderson GR, Fletcher TI, Landmann J, Knight BC (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. Vet Parasitol 130:207–212CrossRefPubMedGoogle Scholar
- Munita MP, Rea R, Bloemhoff Y, Byrne N, Martinez-Ibeas AM, Sayers RG (2016) Six-year longitudinal study of Fasciola hepatica bulk milk antibody ELISA in the dairy dense region of the Republic Ireland. Prev Vet Med 134:16–25. https://doi.org/10.1016/j.prevetmed.2016.09.024 CrossRefPubMedGoogle Scholar
- Rapsch C, Dahinden T, Heinzmann D, Torgerson PR, Braun U, Deplazes P, Hurni L, Bär H, Knubben-Schweizer G (2008) An interactive map to assess the potential spread of Lymnaea truncatula and the free-living stages of Fasciola hepatica in Switzerland. Vet Parasitol 154:242–249. https://doi.org/10.1016/j.vetpar.2008.03.030 CrossRefPubMedGoogle Scholar
- Selemetas N, Phelan P, O’Kiely P, de Waal T (2015) The effects of farm management practices on liver fluke prevalence and the current internal parasite control measures employed on Irish dairy farms. Vet Parasitol 207:228–240. https://doi.org/10.1016/j.vetpar.2014.12.010 CrossRefPubMedGoogle Scholar
- Skuce PJ, Zadoks RN (2013) Liver fluke: a growing threat to UK livestock production. Cattle Pr 21:138–149Google Scholar
- Taylor MA, Coop RL, Wall RL (2016) Veterinary parasitology, third. Wiley, ChichesterGoogle Scholar
- Williams R (2006) Generalized ordered logit/partial proportional odds models for ordinal dependent variables. Stata J 6:58–82Google Scholar