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Dictyocaulus Viviparus in Great Britain

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Dictyocaulus Viviparus in Great Britain Predicting the Unpredictable: the Changing Epidemiology of Dictyocaulus viviparus in Great Britain. Catherine Anne McCarthy Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor in Philosophy. September 2018 Predicting the unpredictable: the changing epidemiology of Dictyocaulus viviparus in Great Britain. Catherine Anne McCarthy Abstract Disease caused by the bovine lungworm, Dictyocaulus viviparus, is a cause of significant morbidity and mortality in dairy herds across the world. Subclinical infections are associated with reduced milk production in dairy cattle and growth rate deviations in beef calves whereas clinical outbreaks can be unpredictable and expensive. Current estimates for lungworm prevalence across Great Britain are unknown but have risen significantly since the 1970s. This has been associated with more cases in adult cattle and the disease emerging into more northern regions of England and Scotland. The objectives of this thesis were to quantify and understand changes in lungworm epidemiology which have occurred over the past 40 years, understand the relative role that farm management factors and climate (change) have had on the changing prevalence of the disease and to predict future changes which may occur under climate change conditions. Chapter 2 investigates the spatiotemporal distribution of lungworm cases reported to the Veterinary Investigation and Diagnosis Analysis (VIDA) database from 1974 – 2014. There has been a significant increase in the diagnostic rate of lungworm across Great Britain from 0.97 cases per 1,000 submissions in 1980 to 4.04 cases per 1,000 submissions in 2014, with a dramatically increased rate in Scotland. Moreover, the number of cases in adult cattle has increased since the 1980s. Chapter 3 describes the novel use of an existing D.viviparus ELISA in dairy herds, with an improved test sensitivity of 66.7% and specificity of 95.5% under field conditions. Chapter 4 subsequently made use of this test in a cross - sectional survey of UK dairy farmers, which improved our understanding of farm management practices associated with an increased risk of D.viviparus presence. Chapter 5 quantifies the influence of climatic conditions, building a mathematical model, which predicts the development, survival and migration of infective D.viviparus larvae on pasture. It was validated using a longitudinal study and showed that pasture infectivity occurred 46 days prior to a peak in antibody response (95% confidence intervals 38 – 52 days). The model demonstrated that the climate was conducive to increased D.viviparus transmission in Scotland from 1995 onwards. Under future climate change predictions, by 2055, the majority of England is predicted to have a climate not conducive to D.viviparus transmission. Exceptions to this are in Scotland and the southwest of England, which are predicted to remain hotspots for the disease until at least 2095. In the past, researchers have largely attempted to explain the changes observed in lungworm epidemiology from farm management factors. However, the findings presented here suggest that climate (change) can account for most of the changes observed and may have already had a significant impact on the epidemiology of D.viviparus across Great Britain. Future global changes in livestock farming will continue to threaten the stability of the disease landscape. Mathematical models such as the one described here, can forecast heightened disease risk periods and will be useful in the design of sustainable control measures for lungworm disease. ii Acknowledgements This PhD has been funded by the Biotechnology and Biological Sciences Research Council (BBSRC) Doctoral Training Partnership programme, without which, I would not have been able to undertake this work. I am sincerely grateful to my supervisors Dr. Jan van Dijk and Professor Rob Christley for their insight, guidance and support throughout the project. Special gratitude goes to Jan for being the driving force throughout this PhD from the start, for never letting me lose interest in the subject and for supporting me through numerous personal challenges throughout the past five years. I will miss our long discussions over a beer in Leahurst, Mold, Bristol and Uppsala. I would like to acknowledge Professor Diana Williams who stepped in at a later stage of the PhD and provided guidance, stability and insight in an unofficial capacity during the past twelve months. I would like to thank Professor Johan Höglund, for providing useful insight during the development of the diagnostic test in Chapter 3. Also Dr Inna Kozlova and Dr Mikael Juremalm at Svanova, Boehringer – Ingelheim for providing the ELISA kits which were used throughout the PhD and for being incredible hosts during our time in Uppsala. I would like to acknowledge Professor Rob Smith for providing useful contacts within the Tesco Sustainable Dairy Group (TSDG) during the cross – sectional study. I would like to thank all the farmers and veterinarians involved in this project. I would like to thank all the staff at National Milk Records for patiently gathering milk samples for me on a very regular basis. Your help during this time was greatly achieved. I hope the chocolates were good enough! My gratitude goes to Helen Gartner at APHA, Weybridge for providing the data used in Chapter 2. My particular thanks goes to Ben Strugnell at Farm iii Post Mortems Ltd for sending me regular updates on lungworm cases that he had seen, providing fantastic post – mortem photos and being a regular supply of infected cattle faeces for the laboratory studies in Chapter 5. “Trial – by – thesis” was a phrase used by a good friend of mine when she was doing her PhD, and I think this is apt. However, I have not done this alone and I have never felt more supported than I have done over the past 12 months. My utmost gratitude goes out to my friends at Leahurst (particularly Sarah, Tamzin, Cajsa, Jay and John) and friends that I have made since my masters (particularly Tasha, Luke, Jimmie and Marisol) for keeping my head above water and always giving me a reason to smile. Particular thanks goes to Sarah for being like a sister to me over the past 12 months. Your kindness, patience and good sense of humour have been a source of constant joy, without which, I do not know that I would have finished this PhD on time. I hope I can return the favour soon. To Tetley and Kenco who are always entertaining but really cannot see what all the fuss is about when the real world is “out there”. My thanks go to my brother, Mike, and sister, Rachel, for always being by my side and for providing support when things got tough. To my Mum and Dad. I would not be where I am in life today without your love and patience. To my Mum for providing limitless support, hugs and a shoulder to lean on. To my Dad for teaching me that there is always something to laugh about no matter how bad your day may seem. To my “bootiful” Gran who would have been very proud and whom I blame for my own sense of humour, without which, I would be a very different person. To my Grandma and Grandad for inspiring in me my love of science. As Grandad said the day that I got into vet school, “God helps those who help themselves”. I think you might have been right there, but I have not done this alone. Thank you all. iv Dedication This thesis is dedicated to my Gran, Dot Laughing until the end. v Table of Contents Abstract ....................................................................................................................... ii Acknowledgements ..................................................................................................... iii Dedication ................................................................................................................... v Table of Contents ........................................................................................................ vi List of Figures .............................................................................................................. ix List of Tables .............................................................................................................. xiii Chapter 1: Introduction ........................................................................................... 1 1.1 Food security and the role of helminth infections in farmed ruminants .............. 1 1.1.1 Current challenges in Veterinary parasitology ..................................................... 1 1.1.2 Attempts to overcome the negative consequences of global change.................. 4 1.1.3 Knowledge gaps in the control of helminths under global change ...................... 6 1.2 The impact and epidemiology of Dictyocaulus viviparus in farmed cattle ............ 8 1.2.1 Historical account of the disease .......................................................................... 8 1.2.2 Economic impact of Dictyocaulus viviparus infection ........................................... 8 1.2.3 The parasite lifecycle ............................................................................................ 9 1.2.4 Dictyocaulosis in non-cattle species ................................................................... 14 1.2.5 Host stages and the development of immunity ................................................. 16 1.2.6 Transmission on pasture ..................................................................................... 20 1.2.7 Current diagnostic options for Dictyocaulus viviparus
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