Rumen fluke in cattle and sheep: measuring impacts and improving diagnosis

Lead Research Organisation: Queen's University Belfast
Department Name: Sch of Biological Sciences

Abstract

Helminth (worm) parasites cause around 55% of all farm animal diseases. These parasites impact hugely on livestock productivity by affecting growth rates, fertility, meat quality, wool or milk production, and sometimes cause death. One of the most important parasites to impact animal production in the UK/Ireland (and throughout the EU) is the liver fluke, Fasciola hepatica. It infects more than 300 million cattle and 250 million sheep worldwide resulting in losses of over $3 billion to global agriculture through lost productivity. In the UK it costs the cattle farming industry alone around £23 million each year as a result of poor animal condition and a significant reduction of milk and meat yields. Worryingly, resistance to the frontline chemical treatment for liver fluke (a drug called triclabendazole) has become widespread leaving farmers with little to combat the disease. Until recently, infections by similar parasites called paramphistomes, or rumen fluke, were regarded as being of minor importance. However, over the last few years increasing reports of production losses from farmers in Great Britain and Ireland have been ascribed to infection by rumen fluke. It is now believed that rumen fluke has become a bigger problem than liver fluke in many areas. In order to meet the growing threat to food security posed by rumen fluke infection it is imperative that we act now. In this project we will answer some basic questions about its biology, its impact on animal health and productivity and will develop new tests that will allow more rapid and specific diagnosis than currently possible.

Specifically, we will address three main questions:

1) What is the extent of the rumen fluke problem in the UK?
2) What is the impact of rumen fluke on animal performance, health & welfare?
3) Can we develop a rapid and specific diagnostic test for rumen fluke?

Our approach is timely and will determine the extent of the problem in the UK and for the first time determine a measurable impact of infection on animal production in both cattle and sheep. Furthermore we will have produced rapid and specific diagnostic tests that will allow appropriate control measures to be put in place. These important findings will allow more effective management practices to be put in place early and give us a realistic chance of avoiding the problems of drug resistance currently seen with liver fluke.

Technical Summary

The overall objective of the project is to address the emerging threat to animal health, welfare and livestock sustainability posed by rumen fluke in sheep and cattle. Specifically, we will address three main questions:

1) What is the extent of the rumen fluke problem in the UK?
The true extent of the rumen fluke problem in the UK has not yet been investigated. Using data collated from our industry partners we will determine its incidence and geographical range in the UK and use a multiplex PCR on intermediate hosts (snails) to investigate the likelihood of co-infection with liver fluke. We will conduct a UK-wide survey of farmers to gauge their awareness of the problem and set up knowledge transfer events to help them manage the infection more effectively.

2) What is the impact of rumen fluke on animal performance, health & welfare?
Despite considerable anecdotal evidence that diarrhea and production loss are caused by chronic rumen fluke infection it is still unclear to what extent infection impair animal welfare and translate into measurable production losses. We will conduct field studies on four experimental husbandry farms to measure the impact of rumen fluke infection on diarrhoea score, bodyweight and welfare assessment of grazing dairy heifers. Metabolic studies using state-of-the-art calorimetric chambers will also be conducted to determine the impact of rumen fluke on feed intake and digestibility in sheep.

3) Can we develop a rapid and specific diagnostic test for rumen fluke?
Current diagnosis of rumen fluke relies on labour-intensive methods such as examination of animals at post-mortem or faecal egg counts. Using proteomics we will characterize the secretome of rumen fluke and use selected antigens to develop ELISAs for detection of rumen fluke in faecal samples and bulk milk.

Planned Impact

This project, aimed at investigating the impacts of rumen fluke in sheep and cattle in the UK and improving its diagnosis will have important societal and economic impacts.

[1] The livestock industry, such as cattle and sheep managers, and veterinarians, will benefit from having access to early warning signs of rumen fluke infection through animal-based (welfare) indicators and the development of tools for rapid and correct diagnosis. At present diagnosis is based on faecal egg counts in living animals making it difficult to distinguish clearly between rumen fluke and liver fluke, and relying on abattoir data for diagnosis is not practical for dairy cattle and breeding ewes nor for rapid response. Increasing scientific knowledge of early signs of the disease and developing tools for its rapid and correct diagnosis will enable effective therapeutic intervention before the onset of pathology. This in turn will enable producers to rear livestock to higher standards of health and welfare and ensure cost-effective control.

Furthermore, to what extent acute and chronic rumen fluke infection translate into measurable production losses or predispose animals to other diseases is unknown. Knowledge gained from this project will help to quantify the true impact on productivity and inform management decisions needed to avoid livestock and economic losses due to rumen fluke infection. It will promote livestock performance by avoiding the failure to thrive associated with chronic rumen fluke infection. Lower levels of infection will reduce pasture contamination and thus reduce the incidence of infection in subsequent years. In addition, selective use of anthelmintics with proven efficacy will improve livestock productivity, prevent the selection of anthelmintic resistant rumen fluke populations and thus maintain our ability to limit the spread and incidence of infection.

The development of tests for the early diagnosis of infections will improve targeting and economic use of therapeutics, thus limiting the unnecessary contamination of pasture with anthelmintic residues which may harm invertebrate eco-systems. By limiting the exposure of livestock to fluke infection this project aims to maximize weight gain and feed use efficiency in stock animals and minimize anthelmintic usage. This will reduce the presence of anthelmintic residues in the export product. Overall this project will enable the livestock industry to rear livestock to higher standards of health and welfare and to achieve economic competitiveness.

[2] Agricultural industry stakeholders such as meat plants, food processors and retailers will benefit in at least two ways. Firstly, this research will help to ensure that improving animal welfare should remain a priority for them, thus guaranteeing higher standards of health and welfare of the animals. A second important benefit is the reduced presence of anthelmintic residues in the export product. Both these benefits have important economic consequences for the food industry, as they can use this when marketing their products.

[3] Policy makers (Governments, EU, NGOs, etc) will benefit from having access to a scientific knowledge base quantifying i) to what extent rumen fluke infections, chronic or pathogenic, affect animal welfare and animal performance and ii) the potential for co-infection with liver fluke. This will enable them to make sound, evidence-based decisions and inform on strategies for improving the conditions and management of farmed animals. Furthermore, this project is in line with the aims of the "One Health" approach taken by policy makers as it will facilitate a more targeted use of therapeutics and the uptake of management practices minimizing anthelmintic usage.

[4] Consumers will benefit from knowing that something is being actively done to improve the health and welfare of farmed animals, and that products from farm to fork are welfare-friendly and free of unnecessary drug residues.

Publications

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Cwiklinski K (2019) The cathepsin-like cysteine peptidases of trematodes of the genus Fasciola. in Advances in parasitology

 
Description We have established conditions that permit excystment (or activation) of the infective juvenile stage of rumen fluke and generated significant transcriptomics and proteomics datasets to help us understand parasite development and how they infect and cause disease (and avoid the immune response) in their host animals. We have developed the first coproantigen-based ELISA for detection of rumen fluke infection and are currently validating these using field samples. All primary data from this project has been published in peer-reviewed journals. Further manuscripts are in preparation detailing the effects of rumen fluke on health/productivity in dairy heifers and feed conversion efficiency in sheep.
Exploitation Route Our findings are far-reaching for rumen fluke biology and animal health. Our new method for fluke excystment will allow in vitro experiments to be performed on how this parasite causes disease in sheep/cattle. The new diagnostic tools will allow rapid detection of rumen fluke infection (and allow appropriate treatments to be given quickly - a major advance for animal health and welfare) and could also be used in epidemiological studies to monitor the spread of infection in the UK and beyond. Our transcriptome/proteome studies have identified several new candidates for further diagnostic tests but also vaccine candidates which were lacking for this species.
Sectors Agriculture, Food and Drink,Pharmaceuticals and Medical Biotechnology

URL https://pubmed.ncbi.nlm.nih.gov/33581320/
 
Description The project has raised awareness of rumen fluke in the UK and Ireland, particularly amongst farmers/producers who are concerned about this infection. Planned pathway to impact activities in conjunction with our industrial partners (Agrisearch and AHDB) aimed at dissemination of project findings/wider education to such end users were delayed whilst research findings were published (and partly due to COVID-19). However, the aspects of the project with most obvious impact for the farming community (i.e. impact of rumen fluke on animal productivity and health) were published in 2022 and will be the subject of educational resources delivered via our industry partners.
First Year Of Impact 2018
Sector Agriculture, Food and Drink
Impact Types Policy & public services

 
Description Dr Mark Robinson joined teachnical working group of Animal Health Ireland
Geographic Reach National 
Policy Influence Type Membership of a guideline committee
URL http://animalhealthireland.ie/?page_id=411
 
Description DEL PhD studentship
Amount £60,000 (GBP)
Organisation Government of Northern Ireland 
Department Department for Employment and Learning Northern Ireland (DELNI)
Sector Public
Country United Kingdom
Start 10/2016 
End 09/2019
 
Title Generating transcriptome resources for the rumen fluke, Calicophoron daubneyi. 
Description Infections by parasitic flatworms are an important animal health and production concern for livestock producers worldwide. In recent years there has been a sharp increase in both the incidence and severity of rumen fluke (the paramphistome Calicophoron daubneyi) infections in both sheep and cattle in Western Europe. This is a major concern since outbreaks of clinical (and fatal) paramphistomosis are on the rise in the UK/Ireland. Despite their prevalence, our current knowledge of basic rumen fluke biology, and how they interact with their hosts, is remarkably limited. To begin to address this, we have generated significant transcriptome datasets for C. daubneyi via long read PacBio sequencing which served as a reference map for differential expression analysis (Illumina RNAseq) of 4 intra-mammalian life-cycle stages: newly excysted juveniles, immature worms recovered from the small intestine, newly-migrated flukes and adults, both recovered from the rumen. It is envisaged that these resources will aid discovery of novel vaccine candidates and diagnostic antigens for this emerging parasite infection. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
Impact A resource for the research community - will aid drug target and diagnostic antigen discovery for rumen fluke. 
URL https://www.ebi.ac.uk/ena/browser/view/PRJEB28150?show=reads
 
Description AHDB Beef & Lamb 
Organisation Agricultural and Horticulture Development Board
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution Supply of research data of importance to the partner and levy payers.
Collaborator Contribution Aid with dissemination of research findings to end users (e.g. farmers groups/vets) through factsheets/webinars etc. Our research will contribute to future policy development.
Impact Pending (activities delayed by COVID-19).
Start Year 2017
 
Description Agrisearch 
Organisation Agrisearch
Country United Kingdom 
Sector Private 
PI Contribution Supply of research data of importance to the partner and levy payers.
Collaborator Contribution Aid with dissemination of research findings to end users (e.g. farmers groups/vets) through factsheets/webinars etc. Our research will contribute to future policy development.
Impact Pending (activities delayed by COVID-19)
Start Year 2017
 
Description Oral presentation 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Oral presentation " Transcriptome and secretome analysis of intra-mammalian life-stages of the rumen fluke Calicophoron daubneyi provides new insight into host interactions and informs a novel coproantigen test" at the WAAVP 2021 Dublin meeting.
Year(s) Of Engagement Activity 2021
URL http://www.waavp2021.com/
 
Description PDRA presentation at BSP conference 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Research presentation made by a PDRA Dr Kathryn Huson at the British Society for Parasitology meeting in Aberystwyth 2018.

HUSON, K.M, OLIVER, N. & ROBINSON, M.W. (2018). Novel eggshell biochemistry of rumen flukes.

It reached a broad audience (>250 in attendance) with collaboration requests from academics.
Year(s) Of Engagement Activity 2018
URL http://bsp.uk.net/bsp-spring-meeting-2018-aberystwyth-abstract-book-3/
 
Description Poster and parasite demonstration at AFBI Hillsborough 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact My team and I attended an open day at AFBI Hillsborough entitled "Dairy Innovation - Profiting from AFBI research" on 6th June 2018. We brought specimens of fixed parasites and microscopes etc in order to promote our BSRC-funded work and education farmers/general public about parasitic infections and control options.
Year(s) Of Engagement Activity 2018
URL https://www.afbini.gov.uk/dairy-open-day-2018
 
Description Presentation at Helminth meeting - Thailand 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact GRCF funded workshop entitled "A One Health Approach to Helminth Control in South East Asia" held at Mahidol University, Bangkok, Thailand, 19th 22nd June 2017. Intention was to network with potential collaborators from across south-east Asia with a view to submitting future collaborative grant applications.
Year(s) Of Engagement Activity 2017
 
Description Presentation at workshop in Shanghai, China 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Third sector organisations
Results and Impact GRCF/British council funded workshop entitled "Neglected helminth diseases of China and the impact of urbanisation" held at Fudan University, Shanghai, China, 29th-31st January 2018. Intention was to network with potential collaborators from across China with a view to submitting future collaborative grant applications.
Year(s) Of Engagement Activity 2018
 
Description UK Veterinary Vaccinology Conference 2017 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact I was part of the organising committee for the BBSRC UK Veterinary Vaccinology Conference (16th-17th January 2017, Riddel Hall, Queens University, Belfast). The event was a great success and attracted 140 delegates to see a strong line up of internationally-recognised speakers at Queens.
Year(s) Of Engagement Activity 2017
URL http://www.vetvaccnet.ac.uk/veterinary-vaccinology-network-conference-2017