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Implications of extreme weather events for risk of fluke infection Philip Skuce, Jan van Dijk, Daniel Smith and Eric Morgan In spite of a promising summer at the time of writing (July 2014), we have had more than our share of wet weather in the UK in recent years, including record rainfall and damaging floods in the winter of 2013/2014. How could all that rain be influencing risks to animal health, especially from diseases such as fasciolosis, which are associated with wet conditions? It is long established that liver fluke infection risk is largely driven by the prevailing climatic conditions – particularly temperature and rainfall. The past 10 to 15 years in the UK have seen increasing fluke prevalence in livestock (and other animals including alpacas, horses and deer), as well as altered geographical distribution and seasonality of the disease. These changes have been mainly attributed to changing climatic conditions, specifically warmer and wetter springs and summers and milder winters (for example, Kenyon and others 2009, van Dijk and others 2010). Assuming that the dominant seasonal patterns of fluke

Philip Skuce, BSc, PhD, Moredun Research Institute, Pentlands Science Park, Edinburgh EH26 0PZ, UK e-mail: [email protected] Jan van Dijk,DVM, PhD, MRCVS, Daniel Smith, BSc, MSc, Institute of Infection and Global Health, Department of Epidemiology and Population Health, University of Liverpool, Leahurst, Cheshire CH64 7TE, UK Eric Morgan, MA, VetMB, PhD, DipEVPC, MRCVS, School of Veterinary Sciences and Cabot Institute, University of Bristol, Bristol BS40 5DU, UK

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transmission remain as they have in the past, unprecedented levels of fluke risk have been predicted for the coming decades (Fox and others 2011). However, the dynamics of fluke populations in animals at pasture may change altogether. This is currently being explored by ourselves, using mathematical models of liver fluke epidemiology, as part of the EU-GLOWORM project. Superimposed on these warming, wetting trends, recent climate projections predict an increase in the frequency and intensity of extreme weather events, for example, summer droughts, heatwaves and winter flooding (IPCC 2013). The extensive flooding of farmland on the Somerset Levels last winter may be a distant memory to some now, but in southwest England, January 2014 was the wettest on record since 1910 (Fig 1). Statistics also showed that this was one of (if not the) most exceptional periods of winter rainfall across England and Wales for almost 250 years (data from UK Met Office). In this article, we explore the implications of such extreme events for liver fluke epidemiology and speculate about what this might mean for liver fluke risk this year. Fasciolosis risk is not just determined by within-year climatic conditions but also by fluke abundance in previous years. Indeed, levels of infection in livestock have been shown to be strongly correlated with temperature and rainfall patterns over the preceding five years (McCann and others 2010). An example of this would be the succession of wet summers from 2007 to 2012, which inevitably led to the ‘perfect storm’ that was the 2012/2013 fluke

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Research Image: UK Met Office

England, and the Somerset Levels season. The summer of 2012 was in particular, were under water exceptionally wet, with more than for weeks on end (Fig 2). What 200 per cent of normal rainfall impact is this winter flooding over most of the UK from June likely to have on fluke risk this to August (data from the UK Met year? The infectious metacercarial Office). This led to extremely cysts are likely to remain viable high fluke burdens on pasture underwater; indeed, that is how and resulted in unprecedented they are routinely maintained in levels of acute fluke disease in the laboratory. Where flooding may sheep in the last quarter of 2012, actually help reduce infection risk accounting for about one-third of is in physically preventing stock all diagnosable submissions (data from gaining access to infected from the AHVLA). This situation pasture, although, as stated above, was compounded by a very mild the infection risk this year may winter, with livestock still at risk be relatively low. Serious flooding of ingesting overwintering fluke would also be expected to accelerate cysts while grazing outdoors. This the dying off of existing vegetation was then followed by an extremely and delay the onset of spring late and cold spring, the second growth so, in this context, should coldest on record (UK Met Office), be beneficial as well. Severe flooding with hard frost and deep snow in might also be expected to decimate many places from March to April. the rabbit population, historically Pregnant animals, especially sheep, a key wildlife reservoir of infection were in relatively poor condition at but unquantified in recent years. lambing and there were significant Alternatively, or perhaps losses due to chronic fluke at that concurrently, severe flooding may time. There was also relatively little FIG 1: UK Met Office rainfall anomaly map for January 2014 displace the rabbit population and grass growth, so newborn lambs showing the distribution of rainfall as a percentage of the spread infection further. As for snails, became infected with fluke almost long-term average from 1981 to 2010 the fluke’s favoured intermediate as soon as they started grazing. host species, Galba truncatula, is considered This chain of events led to fluke becoming of parasites and snails at pasture has, thus to be the least aquatic of all the lymnaeids. an animal health and welfare crisis for the far, been poorly quantified. Recent work G truncatula is a genuine mud snail, requiring livestock industry in spring 2013, as widely has shown that unembryonated fluke eggs access to the air, and typically it does not reported in the farming and veterinary press. are able to survive temperate winters very survive well in standing water. Other Traditionally, in the UK, fluke risk well (Daniel Smith, unpublished data). lymnaeid snails, which are usually larger, for has been associated with the summer The precise levels of overwinter survival example, Lymnaea stagnalis, Radix auricularia, infection of snails, with cercariae emerging of infected snails, and metacercarial cysts, Radix peregra, Lymnaea palustris and Galba from late summer onwards to drive acute however, require further investigation. glabra are all more at home in larger bodies fasciolosis in the autumn and chronic disease So, what of the fluke risk for the rest of semi-permanent water. At least some of thereafter. The influence of weather on of 2014? At the time of writing, it is too these can act as intermediate hosts for liver this process was elegantly captured back in early in the year to quantify risk in the fluke (Relf and others 2009), but they are the 1950s in the Ollerenshaw Index – an autumn; however, we may speculate on the typically less common than G truncatula on indicator of fluke risk over the course of a influences of recent UK ‘extreme weather farmland. Prolonged deep flooding would, typical grazing season. This model takes events’ on fluke abundance. Thankfully, the therefore, be expected to kill off the mud account of the climatic conditions around summer of 2013 was unusually hot and dry snail in its natural habitat. However, this the main period of fluke egg development over most of the country. This would be snail is not able to adhere to its substratum as and infection of snails (that is, spring and expected either to desiccate the snails or drive well as some of the larger species in flowing summer) and predicts the autumn infection them underground to aestivate. This would water, so it may well be dispersed on flood risk associated with that (Ollerenshaw and reduce the probability of hatching miracidia margins. When the flood water recedes, Rowlands 1959). The model provided the contacting suitable host snails and would also it is possible that this new habitat will be first ever liver fluke forecast for the farming retard parasite development in snails already less suitable for its survival, although there community, and is still used today in the infected. As a consequence, we would is always the possibility that a few snails regional liver fluke forecasts produced by anticipate relatively few cercariae encysting may end up in a potentially favourable place the National Animal Disease Information on herbage in the autumn. That said, the and establish new snail colonies. Being Service (www.nadis.org.uk). There is, fine summer of 2013 was followed by an hermaphrodite, the snails do not need a however, also a component of fluke risk extremely wet and mild winter, so conditions mate to breed and can successfully colonise associated with infected snails surviving at for in-snail survival are likely to have been an area in a matter of weeks. Overall pasture over winter. Survival of such snails good, even if the numbers were relatively then, prolonged winter flooding would be is likely to be greater during milder winters low to start with. Within-snail development expected to reduce snail numbers and provide and this could potentially lead to disease of the parasite would have been completed a respite from fluke infection in grazing during months in which it is least expected in the early summer, with individual animals. However, ‘overspill’ flooding may (for example, June). Unfortunately, changes snails capable of shedding hundreds, if not facilitate snail dispersal into new habitats, in population and grazing dynamics are thousands of cercariae. It is therefore possible with fluke potentially emerging on farms not captured by the Ollerenshaw Index and that some chronic, or even acute, fasciolosis where it was not present before. therefore new models that are able to predict may occur unseasonably early this year. In conclusion, we do not wish to new risk periods generated by fundamental What about too much water when downplay the risk of liver fluke this year. shifts in parasite seasonality and host factors temperatures are low? This spring, large It is not possible to accurately predict how may be needed. The overwinter survival parts of the UK, especially the southwest of August 30, 2014 | Veterinary Record | 199

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Research David Davies/PA Archive/Press Association Images

wet this summer will be, so it is under the EUFP7 GLOWORM important to be on guard. The project, grant agreement number fluke risk this year is likely to 288975CP-TP-KBBE.2011.1.3-04. be lower, certainly compared References to 2012/2013, but it will not Bates P. (2014) Flood crisis: dredging is a have gone away, even after a simplistic response to a complex problem. ‘good’ summer. Circumstances The Guardian February 12, 2014. www. such as these could represent an theguardian.com/environment/2014/ feb/12/flood-crisis-dredging-climate-change. ideal opportunity for farmers to Accessed July 16, 2014 ‘kick fluke while it’s down’, for Fox, N. J., White, P. C. L., McClean, example, treating stock in the C. J., Marion, G., Evans, A. & Hutchings, M. R. (2011) Predicting early summer or at turnout with FIG 2: Sheep ‘grazing’ on flooded fields. Decreased land area impacts of climate change on Fasciola hepatica an effective flukicide. Although intensifies effective stocking density – but is the higher land less risk. PLOS One 6, e16126 too late for an article in August, likely to harbour fluke, and do snails drown when submerged? IPCC (2013) Summary for Policymakers. In Climate Change 2013: The Physical Science this message has been promoted Basis. Contribution of Working Group I to the Fifth support of environmental stewardship by Sustainable Control of Parasites Assessment Report of the Intergovernmental Panel on and reduced nitrate-phosphate pollution of in Sheep (SCOPS), Control of Cattle Climate Change. Cambridge University Press. surface waters. This could increase the extent Parasites Sustainably (COWS) and other Kenyon, F., Sargison, N. D., Skuce, P. J. & Jackson, F. (2009) Sheep helminth disease in south of favourable snail and hence fluke habitat organisations earlier in the year. Targeting eastern Scotland arising as a possible consequence of to historical levels, just as climate drives the adults at this time will reduce shedding climate change. Veterinary Parasitology 163, 293-297 higher and less predictable disease risk, and of eggs at pasture, hence also infection levels McCann, C. M., Baylis, M. & Williams, D. J. L. (2010) The development of linear regression models the tools available for control are diminished in snails, and thereby decrease fluke risk using environmental variables to explain the spatial by drug resistance. The days of ‘sour’ land in autumn. It is also perhaps worth taking distribution of Fasciola hepatica infection in dairy herds unsuitable for grazing might then be upon a few diagnostic samples (blood or faeces) in England and Wales. International Journal for Parasitology, us once more, at a time when productivity from presumed fluke-naive animals (for 40, 1021-1028 Ollerenshaw, C. B. & Rowlands, W. T. (1959) is at a premium to underpin food security. example, lambs and calves) over the course A method of forecasting the incidence of fascioliasis in Ironically, the greatest consequences of of the summer to help assess the dynamics Anglesey. Veterinary Record 71, 591-598 recent and high profile flooding, while of fluke infection this year, in particular the Relf, V., Good, B., McCarthy, E. & de Waal, T. (2009) Evidence of Fasciola hepatica infection in Radix perreducing direct disease risk through effects start of transmission and the time at which egra and a mollusc of the family Succineidae in Ireland. on fluke biology, could lead to a long-term treatments might first be needed. More Veterinary Parasitology 163, 152-155 legacy of increased risk through land use monitoring in general is a useful defence van Dijk, J., Sargison, N. D., Kenyon, F. & change. Parasites live in a complex world Skuce, P. J. (2010) Climate change and infectious disagainst unpredictable shifts in seasonal ease: helminthological challenges to farmed ruminants of interacting forces, and direct effects of patterns as a result of increasing variation in in temperate regions. Animal 4, 377-392 climate on their biology are modified by climate. many other factors, including land use Finally, practical farm management doi: 10.1136/vr.g5377 7 77 and politics. Epidemiological models that practices, such as improving drainage of lowintegrate these wider factors are needed if lying ground, rolling previously poached predictions of the effects of climate change areas, removing reeds and rushes (that is, on animal disease are to improve on the anything to reduce potential snail habitats speculation to which we are currently and interaction between snails and livestock) limited. will help to improve the pasture and reduce the overall fluke burden. However, excessively quick runoff from intensively Acknowledgements grazed, compacted grassland soils was The authors are indebted to C. B. widely cited as an important contributory Ollerenshaw (Central Veterinary factor to last winter’s floods in Somerset Laboratory, retired) for helpful discussions (Bates 2014). It is likely that farmers will and insightful comments on the manuscript. increasingly be expected to boost the water The authors would also like to thank Becky storage capacity of their land in areas prone Stirk, UK Met Office, for providing relevant to flooding, and also to slow drainage in weather records. Daniel Smith is funded

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Implications of extreme weather events for risk of fluke infection Philip Skuce, Jan van Dijk, Daniel Smith and Eric Morgan Veterinary Record 2014 175: 198-200

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