Results and submissions : REF 2021

Improved policy and practice reduce antimicrobial use across the UK veterinary profession ...

Submitting institution: University of Bristol
Unit of assessment: 6 - Agriculture, Food and Veterinary Sciences
Summary impact type: Environmental
Is this case study continued from a case study submitted in 2014?: No

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1. Summary of the impact

Reducing animal and human exposure to antibiotics is integral to reducing the worldwide challenge of antimicrobial resistance. The Antimicrobial Resistance Force (AMR Force) at the University of Bristol has led the UK veterinary and farming sectors to reduce and refine the use of antimicrobials in livestock. Providing the evidence and means to modify and accurately monitor AMU has shaped industry policy and changed professional practice. AMR Force has:

influenced new Red Tractor certification guidance, contributing to 87% and 96% decreases in critically important antimicrobial (CIA) use in dairy and beef cattle, respectively;
developed a responsible antimicrobial use (AMU) policy for Waitrose’s milk producers, driving further reductions in AMU through changes in farmer behaviour;
worked with a large veterinary business to change veterinarian behaviour and reduce sales of CIAs by 75% within one year across 100 dairy farms;
developed software for the British dairy industry to accurately monitor and encourage responsible AMU in dairy cattle (accessible by 40% of GB’s milk pool in 2020, and used by 15%).

2. Underpinning research

The rapid emergence and spread of AMR is a critical public health issue worldwide. It has profound implications not just for human health, but also for veterinary medicine, farming and global food security with pressures to reduce AMU in agriculture. The need to cut and monitor AMU was formally recognised by the UK Government in its 2016 response to a “Review on AMR” commissioned by the UK Prime Minister in 2014. The Review argued for a significant increase in regulatory oversight of veterinary antimicrobials worldwide. The Government’s response set an AMU target for UK livestock and recognised the need to improve surveillance data on AMR and antimicrobial prescribing in farmed animals.

The University of Bristol (UoB) Veterinary School’s AMR Force – led by Dr Kristen Reyher – are regarded as pioneers of research into AMU and AMR in the livestock sectors, publishing empirical evidence in preeminent international journals. This interdisciplinary team of epidemiologists, microbiologists, social scientists and veterinarians had already begun conceiving and pioneering initiatives to reduce AMU in livestock long before the 2016 AMR review. As an integral part of a cross-Faculty interdisciplinary approach to AMR spearheaded by UoB, the team work alongside human clinicians, physical scientists and others to share best practice, data and innovation across the AMR sphere, reflecting the WHO’s ‘One Health’ approach to attaining optimal health outcomes for people, animals and the environment. Their evidence-based, participatory approach combines their own practical experience of antimicrobial monitoring and reductions across Bristol Veterinary School’s client farms with wider investigations in the field. Their work has engaged multiple industry partners, clinicians, farmers and academics from various disciplines and institutions at all stages of the research process. While the specific effect of AMU in farmed animals on global AMR remains unclear, AMR Force’s research, detailed below, has advanced understanding of: i) current AMU and AMR in UK agriculture, ii) effective interventions to improve responsible AMU in livestock veterinary practice and on farms and iii) accurate measurement of AMU to improve responsible reporting by the UK farming industries.

Defra AMU study. In 2015, the Department for Environment, Food & Rural Affairs (Defra) commissioned AMR Force, together with social scientists from Exeter University, to conduct a quantitative synthesis of evidence and generate empirical evidence to elucidate how and why antimicrobials were used in contemporary livestock systems [1]. This report demonstrated that AMU was prevalent across national and international livestock systems, yet little research and few interventions had addressed inappropriate use. Furthermore, although farmers and veterinarians were aware of AMR, this awareness did not lead to AMU behaviour change.

Waitrose milk producers study. Due to their reputation and expertise, AMR Force were approached in 2016 by Waitrose’s nationwide milk producers to conduct research to develop a responsible AMU policy [2]. The project actively engaged and opened a dialogue with multiple stakeholders (producers, veterinarians, industry and researchers) to develop practical recommendations for sustainable and responsible AMU. It was the first reported instance of participatory methodology in the livestock sectors to involve farmers from the outset. This work demonstrated that most of the 97 dairy farmers involved were aware of the AMR crisis and, while many were already stringent with AMU, they could envisage making further changes to improve responsible use on their farms, which they did following this work.

Successful interventions to reduce AMU. AMR Force identified interventions to reduce the use of CIAs, of special importance because bacteria that develop resistance to these antimicrobials present a particular problem for human health. Interventions included more targeted AMU and preventative measures (e.g. vaccination and improved hygiene, such as greater cleanliness and better ventilation). Their research found that interventions made it possible for veterinarians to discontinue the use of CIAs in livestock on participating farms without negative effects on animal health, productivity or welfare [3]. AMR Force research also demonstrated that participatory, farmer-led action groups showed great success in encouraging antimicrobial stewardship [5].

AMU monitoring. An accurate measurement of on-farm AMU improves understanding of how antimicrobials are administered and whether usage is truly increasing or decreasing. Due to differences in measurements used to calculate AMU by different groups, however, changes to AMU in livestock are difficult to compare across research outputs and official reports. AMR Force illustrated [4] that both over- and under-reporting of AMU result from the variety of AMU measurements in use, leading, in turn, to inconsistent interpretations of the same data. Further, they showed that farmers demonstrate preferences for certain metrics, taking ownership and using them to drive responsible use with benchmarking [5]. National approaches to responsible AMU measurement, however, do not accurately capture antimicrobials administered and stored locally on farms; standard approaches rely on farmers self-reporting usage and storage. An AMR Force study of a sample of dairy farms developed more accurate figures of usage and storage and found that over 85% of farms stored at least one CIA [6]. Furthermore, their research found that veterinary prescription records closely matched on-the-ground figures and could, therefore, be used as a proxy for AMU.

4. Details of the impact

Globally, AMR is estimated to cause over 700,000 human deaths and cost GBP66 trillion annually. Deaths from AMR are predicted to increase to 10 million by 2050, with use of antimicrobials in humans and animals also predicted to rise globally. Leading research from AMR Force has addressed this critical issue by advancing the understanding of AMU in livestock agriculture. Moreover, their research has inspired and initiated policy and behavioural change towards more responsible AMU. These achievements have been reached through high-quality research collaborations and commissions [1,2], serving on industry, charity and government committees and speaking at national and international meetings to provide evidence and influence decisions made at the highest levels.

The impact of AMR Force’s research is highly regarded. Their paper [3] on AMR interventions was the “clear winner” in the Veterinary Record’s 2019 Impact Awards. Explaining their decision, the publication commented that the paper “ gives a vision that these changes could be scaled up around the globe to greatly reduce the use of antimicrobials in farming” [A]. AMR Force have twice received prestigious Antibiotic Guardian Awards (a Public Health England initiative, in collaboration with Defra): in 2018 for engaging agricultural stakeholders to reduce AMU, and in 2019 for their farmer-led, peer-to-peer learning approach to antimicrobial stewardship [A].

1. Impacts on UK public policy

New industry association and certification scheme guidance on CIAs. AMR Force’s successful intervention to reduce CIAs in livestock – already well known within the industry before academic publication [3] – was a key reference in the not-for-profit British Cattle Veterinary Association’s (BCVA) 2016 AMU statement recommending the reduction of CIAs in cattle practice. “ The robust research conducted by… AMR Force … enabled us to formulate BCVA policy and make a case for our statement about highest-priority critically important (HPCIA) antimicrobials … the research provided robust evidence to support the advice that the reduction and even cessation of HPCIAs did not impact negatively on herd health.” [B]. In turn, BCVA’s 2016 CIA statement influenced Red Tractor – the UK’s largest Farm Assurance and food standards certification body – to issue guidelines in 2018 to restrict the administration of CIAs among farm animals: “ As a result [BCVA’s] statement was later reflected in the Red Tractor Assurance Scheme standards” (BCVA) [B]. Red Tractor’s updated guidance instructs certificate-holders to only use CIAs “ when all other treatment options have been exhausted” and as “ a last resort, under veterinary direction, backed up by … diagnostic testing” [B]. This guidance is compulsory for farms to maintain accreditation and has been adopted by Red Tractor’s 11,000 UK dairy members (responsible for ~93% of UK-produced milk) and around 24,000 beef and lamb members across England (80% of finished beef and 60% of finished lamb). This change is also reflected in government statistics: the Veterinary Antimicrobial Resistance and Sales Surveillance report (VARSS, 2020) relays an 87% and 96% drop in CIA use in dairy and beef cattle, respectively, since 2017 (p31) [B].

Industry and government groups commit to better monitoring and storage. Based on AMR Force’s research, UK government and industry bodies have set standards for collection, measurement and recording of AMU. For example, the Cattle Health and Welfare Group (CHaWG) drew on AMR Force research [4] in a final consultation paper (2019) on AMU monitoring [C]. This paper publishes metrics that illustrate achievements in meeting AMU targets as set by the non-profit Responsible Use of Medicines in Agriculture Alliance (RUMA). RUMA’s targets provide the foundation for the Veterinary Medicines Directorate’s (an executive agency of Defra) approach to tackling antibiotic resistance (as acknowledged in VARSS 2017, p5) [C]. In VARSS 2017 CHaWG states “ the dairy and beef sectors are committed to increasing the amount, quality and representativeness of the data for both antibiotic usage monitoring and benchmarking” (p38) [C]. In the VARSS 2020 report, CHaWG describe the benefits of the metrics, as set out their 2019 consultation paper as allowing: “farms to understand their antibiotic use, and how this is changing over time and relative to the industry, as well as help guide the veterinarian-farmer discussions around disease prevention and responsible antibiotic use.” (p46) [C]. Further, in 2019 the BCVA partnered with RUMA and the British Veterinary Association (BVA) to encourage veterinarians to work more closely with farmers on medicine usage, storage and collection of out-of-date medicines from farms, based on AMR Force’s work [6]. This is reflected in two key industry targets set by the RUMA Targets Task Force 2020 – on-farm benchmarking of AMU and the creation of a ‘Farm Vet Champions’ network (p30). Additionally, RUMA cite AMR Force work (a thesis which developed into [5]) to build their rationale for AMU targets (2021-24) for the UK livestock sector (p20, p29) [C].

1. Impacts on the UK dairy industry: new medicine monitoring software

Since 2018, AMR Force have been collaborating with National Milk Laboratories (NML), who receive samples from 98% of GB dairy farms, to develop ‘FarmAssist’. This database, managed and run by NML on behalf of milk buyers, provides a robust record of medicine use and antibiotic testing on dairy farms to support industry efforts to improve antimicrobial stewardship. AMR Force provided NML with advice on accurate data collection methods and metrics which provide meaningful measurements that are repeatable and consistent over time [4]. FarmAssist has influenced “ how [NML] relay potentially complex information in a way that supports vet-farmer discussion for positive behaviour change … Already we can report usage figures that describe the range of use across GB herds, and notably a reduction in use of HPCIA [highest priority CIA] products. These benchmarking figures are important to both support active vet-farmer health planning discussion on-farm, and to show the dairy sector’s continued progress with antimicrobial stewardship.” (Veterinary Advisor, National Milk Records (NMR)) [D]. At the end of 2020, two major milk buyers, representing 40% of the national milk pool, had contracts with NML to use FarmAssist. Over 1300 dairy farms (of around 8300 in GB) served by these buyers, and over 180 veterinary practices, have submitted data to the online platform. This equates to more than sixfold growth in fewer than two years, with the potential for this software to be scalable to 100% of GB’s dairy population [D].

1. Impacts on professional services: training & behaviour of veterinarians & farmers

AMR Force’s AMU interventions, which emphasise farmer-veterinarian collaborations for auditing antimicrobial prescribing and actively engaging farmers in education and herd health planning to reduce CIA use [3], were first piloted in UoB’s livestock veterinary practice and actively taught to veterinary students. This evidence base has been translated into practice by graduates of the Bristol Veterinary School and taken up across the profession. For instance, in 2016, these interventions were implemented by a large commercial livestock veterinary practice – Friars Moor Farm Vets (FMFV; including a UoB graduate who had studied under AMR Force researchers). As early adopters, FMFV developed a campaign that reduced CIA sales by 75% within a 12-month period from 2015-2016 across 100 dairy farms and approximately 30,000 dairy cows. This provided evidence that AMR Force interventions could be applied widely and successfully, giving confidence to the veterinary profession across the UK and beyond, as seen in the BCVA and Red Tractor guidelines. To develop this campaign, FMFV consulted AMR Force on their experience of eliminating CIAs from their own university farm practice, giving the practice “ confidence that we might achieve our aims” (FMFV veterinarians) [E].

In AMR Force’s work with Waitrose’s milk producers [2], 70 of 72 dairy farms in the producer pool attended policy development workshops and designed an impressive and challenging policy for reducing reliance on antimicrobials [E]. Six months after the policy was launched, 70% of veterinarians and farmers (many of whom were already farming organically and therefore using very few antimicrobials) indicated they had reduced AMU even further [E]. In response to farmers’ appetite for more information about antimicrobials, these producer pools also designed an online training tool for their farmers which became the bedrock for the National Office for Animal Health’s online course supporting the livestock industries in training farmers in better antimicrobial stewardship. As of end-2020, 529 farmers have completed this course [E].

1. Impacts on awareness and understanding of AMU

AMR Force have increased awareness of AMU issues among policymakers (both agricultural and health), the veterinary profession, the agricultural industries and the broader public.

Policy events: The UK Chief Medical and Veterinary Officers invited Dr Reyher to present research evidence at a national policy meeting on Promoting One Health and Taking Effective Action to Combat AMR in May 2017. Reyher was one of only a few academic speakers at the event, attended by 50 delegates comprising veterinary association representatives and policymakers from both animal health and human health organisations such as Defra, NHS bodies and Public Health England [F]. AMR Force have also presented evidence to and engaged Welsh Government (2017) and the National Farmers Union (2017 and 2018) [F].

Media coverage and public events: Working alongside colleagues from the Bristol Medical School and Biomedical Sciences, AMR Force has also raised awareness of AMR among farmers and the general public by discussing their research through regular TV appearances, public talks and activity on social media [F]. These activities include:

Appearances on national and regional TV and radio news programmes, including BBC Breakfast, BBC R4 Farming Today [reaching >1 million], BBC Points West.
Wide coverage in written press, including in national, farming and veterinary press (The Guardian [reaching 35.2 million], Scotsman [reaching 5.8 million], Farmers Weekly [reaching >40,000 households], Farmers Guardian [reaching ~30,000 households], Farming UK [reaching >100,000]).
A presentation on AMR Force’s audit of a sample of dairy farms [6] was given to ~70 dairy farmers in at the Agricultural and Horticultural Development Board (the national agricultural levy board) roadshow in 2018.
Two AMR Force projects are presented as shared learning resources on the Antibiotic Guardian website, “show[ing] the public how agriculturalists work towards global [AMU/AMR] targets and are proactive”.
Leading and participating in annual World Antimicrobial Awareness Week lectures and panel discussions (November 2015, 2016 and 2018 at Royal Society for Medicine).
Acting as an expert panellist at Science Media Centre briefing to journalists (including from the BBC, Daily Mail and The Sun, 2017).

AMR Force interventions for reducing CIA use [3] have also been integral to video content produced by the Food and Agriculture Organisation of the United Nations and hosted on their YouTube channel (100,000 subscribers). Their 2018 video showcases UK farmers and vets working together under the AMR Force approach and has almost 3,000 views to date. Another video, launched in 2017, with 4,500 viewers to date, explains the One Health approach to AMR and highlights AMR Force as a successful example of how to work towards One Health goals.

Improved welfare at slaughter of commercially farmed fish worldwide

Submitting institution: University of Bristol
Unit of assessment: 6 - Agriculture, Food and Veterinary Sciences
Summary impact type: Environmental
Is this case study continued from a case study submitted in 2014?: No

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1. Summary of the impact

As a result of University of Bristol (UoB) research, billions of farmed fish annually worldwide have improved welfare at slaughter. UoB was the first to identify and measure welfare problems with slaughter by asphyxiation in air or on ice, or gill cutting and bleed-out while still conscious; they proceeded to develop proven humane stunning techniques. Their collaborative research with industry has pioneered commercial stunning equipment now used worldwide for salmon and trout and enabled humane mass slaughter with improved productivity and fish quality. Concurrently, the research has led to significant changes in policy worldwide, including the World Organisation for Animal Health (OIE) guidelines, RSPCA welfare standards, the Soil Association’s and Naturland’s international organic standards. Affecting a wide range of fish species, these policies all follow UoB’s research by recommending stunning before slaughter.

2. Underpinning research

Pioneering research at the University of Bristol (UoB) has led the way in evaluating the welfare of farmed salmon and trout at the time of slaughter. Studies support the view that fish are sentient animals that can feel pain. It has been shown, for instance, that given the choice, fish will access analgesics to alleviate pain. To be considered humane, a killing method must render the fish immediately unconscious, unaware of any pain, and that this condition should persist until death.

Research by the UoB group in the early 2000s, led by Dr Kestin, was the first to establish that there was a welfare problem with the then prevalent methods of fish slaughter [1]. By monitoring the electrical activity of fish brains, they established that fish take a long time to die with the commercial methods of handling and slaughter used at the time. These included leaving fish to die a slow, painful death in air or in ice slurry, or gill cutting without stunning, which results in fish remaining conscious whilst slowly dying from blood loss [2].

The UoB team developed protocols for assessing welfare of fish at the time of slaughter [3], focussing on indicators of consciousness, such as respiration, eyes responding to light, checking whether the eyes move with movement of fish (conscious fish maintain their eyes horizontal when the body is turned, termed ‘righting mechanism’) and twitching in response to pinching. In experimental work, electroencephalograms provided the gold standard against which to benchmark these methods of assessing consciousness, which are easier to use in a commercial situation. Using these welfare protocols, the researchers found percussive or electrical stunning to be the principal humane methods of slaughter. Electrical stunning also has the potential to reduce handling of conscious fish. From a welfare perspective, electrocution (which may both stun and kill a fish instantaneously) is ideal, but there are potential commercial disadvantages in that it can affect flesh quality by causing, for example, blood spots and broken bones.

Thus, the body of work not only compared different methods of welfare assessment, handling and slaughter, but also investigated the consequences for the whole fish, its flesh quality and shelf life to ensure acceptability to the aquaculture industry. It was necessary to determine which electrical parameters of the equipment used to electrically stun fish would be effective in terms of fish welfare but without commercial downsides. Systematic experimental studies determined that the duration of stun application, plus the frequency and magnitude of the current, were important for how long trout remained stunned and whether or not they were humanely killed [4]. Further work on salmon [5] led to a better understanding of the electrical parameters needed to produce unconsciousness (animals that lose consciousness quickly are unaware of subsequent procedures used to kill them and do not feel pain: hence this is deemed humane). Follow-on research on electrical stunning specifically investigated flesh quality, including new species, such as turbot [6] and sea bass [7]. LINK-funded research [iii] by UoB and Silsoe Livestock Systems Ltd with industrial partners The Co-operative Group (CWS) Ltd, Waitrose Ltd, Ace Aquatec, Kames Fish Farming Ltd, Shetland Halibut Co. Ltd, together with the Humane Slaughter Association and funding from Defra, moved from stunning in fresh water to electrical stunning in sea water of farmed halibut, extending both species and water type.

This body of research, along with research conducted in development with a commercial partner, laid the foundation for practical, welfare-friendly methods of killing the billions of fish (more than all other food animals) farmed globally.

3. References to the research

Robb DHF, Kestin SC. (2002). Methods used to kill fish: Field observations and literature reviewed. Animal Welfare, 11(3), 269-282. https://www.ingentaconnect.com/content/ufaw/aw/2002/00000011/00000003/art00001
Robb DHF, Wotton SB, McKinstry JL, Sorensen NK, Kestin SC. (2000). Commercial slaughter methods used on Atlantic salmon: determination of the onset of brain failure by electroencephalography. Veterinary Record, 147(11), 298-303. doi:10.1136/vr.147.11.298
Kestin SC, van de Vis JW, Robb DHF. (2002). Protocol for assessing brain function in fish and the effectiveness of methods used to stun and kill them. Veterinary Record, 150(10), 302-307. doi:10.1136/vr.150.10.302
Robb DHF, O'Callaghan M, Lines JA, Kestin SC. (2002). Electrical stunning of rainbow trout ( Oncorhynchus mykiss): factors that affect stun duration. Aquaculture, 205(3-4), 359-371. doi:10.1016/s0044-8486(01)00677-9
Robb DHF, Roth B. (2003). Brain activity of Atlantic salmon ( Salmo salar) following electrical stunning using various field strengths and pulse durations. Aquaculture, 216, 363-369. doi:10.1016/S0044-8486(02)00494-5
Knowles TG, Brown SN, Warriss PD, Lines J, Tinarwo A, Sendon M. (2008). Effect of electrical stunning at slaughter on the quality of farmed turbot ( Psetta maxima). Aquaculture Research, 39, 1731-1738. doi:10.1111/j.1365-2109.2008.02049.x
Knowles TG, Brown SN, Warriss PD, Lines J, Tinarwo A, Bravo A, Carvalho H, Gonçalves A. (2007). Effect of electrical stunning at slaughter on the carcass, flesh and eating quality of farmed sea bass ( Dicentrarchus labrax). Aquaculture Research, 38 (16) , 1732 - 1741. doi:10.1111/j.1365-2109.2007.01846.x

Grant Funding

Kestin SC. Optimisation of harvest procedures of farmed fish with respect to quality and welfare. EU programme FAIR-CT97-3127, 1997-2000, EUR273,000
Knowles TG. StunFishFirst - Development of prototype equipment for humane slaughter of farmed fish in industry. EU – CRAFT (Coop-CT-2004-512991), 2005-2006, EUR755,894
Lines J. Humane electric stunning of farmed sea-fish (Link Collaborative Research). Defra, 2005-2006, GBP121,072

4. Details of the impact

Production of the six top species groups of farmed fish was estimated at 48.5 million tonnes in 2018 (Food and Agriculture Organisation (FAO))Footnote:

http://www.fao.org/3/ca9383en/ca9383en.pdf , representing many billions of individuals. These species are grouped as: carps and barbels; tilapias; catfish; salmons, trouts and smelts; freshwater fishes; and marine perch-like species, which include sea bass and sea bream. Total global production of farmed Atlantic salmon alone, the focus of initial UoB research, is estimated to comprise 200,000,000 fish (2.5 million tonnes in 2018, ( FAO)).

Research at UoB (2000 – 2020) alerted animal welfare charities, government agencies and fish producers to problems with existing slaughter practices within aquaculture fish production. Moreover, the work [4-7] identified practicable solutions to achieving an instantaneous loss of consciousness via electrical stunning which represents a more humane method of slaughter than those previously used. Thanks to the evidence base provided by this work, electrical stunners are now used around the world on salmon, trout, turbot and sea bass [2-7]. The use of stunners on pangasius (catfish), sea bream, yellowtail, carp and barramundi is currently under investigation by UoB with industrial partners in an Humane Slaughter Association project (see below), thus the work has successfully reached species from five of the six top groups of farmed fish, and beyond. Thanks to the specification of the new humane methods of stunning at slaughter by international standards, awareness of the methods is global, even if they are not always implemented (e.g. where farms are too small in scale for the equipment to be practical). Further, the UoB research team has collaborated with a commercial partner, Ace Aquatec, to develop stunning equipment. This, in turn, has opened up new markets and increased staff (recently doubling in number) and sales from European, Australian and South American regional offices for Ace Aquatec [I].

Impacts on national and international policy: food and animal welfare standards

To reassure consumers, most food derived from animals, including fish, complies with standards that ensure high standards of hygiene and animal health and welfare. The UK is the EU’s biggest producer of farmed salmon, the focus of earlier UoB research [2,5], and is responsible for 163 thousand tonnes of salmon each year (~15 million fish), 90% by volume of total EU production and 8% of the global market. Over 70% of UK salmon producers adopt RSPCA Assured welfare standards, which require certificate holders to ensure good welfare practices at slaughter. These practices reflect the UoB team’s research; Kestin of the UoB group contributed to the RSPCA’s guidelines on fish welfare at slaughter for farmed Atlantic salmon, which were updated in 2018 [A] and are still informed by UoB work. The UoB team further influenced retailer standards, opening up the use of electrical stunning to more species investigated by UoB, including trout [4] and sea bass [7]. For example, Waitrose, the retailer with the greatest market share of fish in the UK (1.9 million fish/year), requires that “ All our farmed salmon, sea farmed rainbow trout, rainbow trout, brown trout, sea bass, sea bream and halibut are stunned prior to slaughter.” [Bi]. Both Waitrose and the Co-op were partners in Link-funded research [iii] which extended the range of species that could be effectively and practicably stunned, given the widely differing responses between species to stunning, and also investigated stunning in sea water (Waitrose was also a partner in [ii]). The Co-op standards also require that fish are stunned before slaughter [Bii].

The Farm Animal Welfare Committee (FAWC), the expert committee to Defra and the Devolved Administrations in Scotland and Wales, and which informs UK legislation and practice, produced a report in 2014, ‘Opinion on the Welfare of Farmed Fish at the Time of Killing’ [C]. The report is based predominantly on UoB’s research: 13 of its 20 references come from their work. The 2018 Humane Slaughter Association (HSA, the UK charity concerned exclusively with promoting humane treatment of all food animals worldwide) report ‘Humane Slaughter of Farmed Finfish around the world’ [D] acknowledges the leading work at UoB, “ Two common methods of stunning fish, currently considered to be the most humane and globally acceptable for food safety, are electrical and percussive stunning. Both methods are already in-use in the rainbow trout and Atlantic salmon industries, respectively, and the stunning parameters are based on scientific recommendations (e.g. Robb et al, 2002b [4] *)*”. The report notes how methodologies for welfare assessment, humane stunning and stun-kill are continually being refined and extended to include other fish species [D].

UoB research continues to inform EU practice and is widely cited (seven references) in a 2017 review [E] funded by the European Commission. This report also notes that “ The OIE and EFSA’s Scientific Opinions (2009) on the key fish species, provide a useful point of reference” (Executive Summary). The EFSA 2009 report on salmon cites nine UoB papers whilst its trout report seven key papers from UoB research (including [1-6]). Other international food standards that insist on humane slaughter (stunning before kill) include the Global Aquaculture Alliance’s Best Aquaculture Practices (GAABAP, 2017) [Fii], which base their stunning and killing on a review citing seven papers from UoB research (including [1,3,5]), and the Soil Association’s Aquaculture standards [Fiii], which are underpinned by the UoB-informed FAWC guidelines [C]. A 2009 report published by the Research Institute of Organic Agriculture (FiBL), ‘Stunning and slaughter methods for edible fish’, cites 13 UoB papers and forms an important part of the evidence base used by Naturland’s Standards for Organic Aquaculture (latest version 2020) [Fv]; Naturland is a major international association for organic agriculture.

An increasing number of worldwide standards are adopting guidelines for stunning before slaughter, not only of salmonids (salmon and trout), but also of other farmed fish species. The scientific evidence base for these policy changes includes the pioneering studies by UoB. For example, the World Organisation for Animal Health (OIE) publishes an Aquatic Animal Health Code for its 181 member countries, which states: " farmed fish should be stunned before killing, and the stunning method should ensure immediate and irreversible loss of consciousness” and recommends electrical stunning for “ carp, eel, salmonids” (OIE, 2019) [G]. A review undertaken for the OIE by Lines (of UoB) and Spence (2014) [H] provided the evidence base for the Aquatic Animal Health Code and cites 11 references from the UoB team, including [1-6]. A 2017 assessment of uptake of OIE guidelines, produced for the European Commission by the IBF Consortium (cited in the HSA report [D]), estimated that “ best practices are mostly achieved, with a few exceptions” for Atlantic salmon produced in the European Economic Area.

Economic impacts: industry collaboration and commercialisation of fish stunning equipment

Having developed validated methods for measuring fish welfare at slaughter and defined the principal factors to achieve effective stun with fish in the laboratory, the next step for the UoB group was to upscale the stunning method for commercial settings. Robust and effective stunning equipment was needed to cope with large numbers and rapid processing of fish (line speed in major UK farmed salmon processing factories may be 4,000 per hour, with fish weighing 10-12kg each). This was achieved through Kestin, Knowles and Lines’ research collaboration from 2001 with Ace Aquatec Ltd (AA), producers of aquaculture and marine technologies. Kestin introduced AA to the concept of electrical stunning at an industry meeting and, together, UoB and AA went on to develop and test the first prototype in-line electrical stun systems for the humane commercial killing of farmed salmon and trout [I].

Development work between AA and UoB is ongoing, both in-house and via externally funded research, including GBP721,580 awarded in 2019 by the charity the Humane Slaughter Association to implement in-water electrical stunning in aquaculture of Nile tilapia, Pangasius (catfish), gilthead sea bream, yellowtail and possibly carp [I].

As a result of contributions from UoB, AA is now an award-winning and major provider of humane fish slaughter equipment; in 2019, its Humane Stunner Universal (HSU) technology won a Queen’s award to industry for Enterprise Innovation, while in 2017 it was awarded the Innovation Award at Aqua Nor, the world’s largest aquaculture industry fair. HSU is now in use on farms around the world, including in Chile, New Zealand, Japan, Germany, Greece, USA and Canada [Ii]. Before UoB involvement, AA’s core business was seal deterrents for salmon farms. The company has experienced significant growth as a result of introducing the humane slaughter equipment into its product line. AA’s CEO sums up the considerable commercial impacts of the stunning equipment as including: “ new regional offices in Chile, Norway, and Australia; investment … this year totalling over £4m; doubling of staff from 10 to 20 employees in six months; addition of new species to our stunning capabilities, including bream, tilapia, and prawns … The company has grown from a family run business in 2008 with a handful of deterrents sold each year, to an international business with recurring rental revenue of £2m, with an aim to double each year.” [Ii]. AA has increased its net assets from GBP299,904 in 2015 to GBP3,545,347 in December 2019 [Iii], with sales of its humane slaughter equipment making a major contribution. AA also report that the electrical stunning equipment brings sustainability benefits, having “ reduced waste going to landfill and provided an income to farmers/suppliers where otherwise there was an expense for removal and destruction. These products are now supplying high end restaurants and pet food where before the use of anaesthetic required them to go to landfill.” [Ii].

Welfare outcome measures and enhanced management have improved farm animal welfare ...

Submitting institution: University of Bristol
Unit of assessment: 6 - Agriculture, Food and Veterinary Sciences
Summary impact type: Environmental
Is this case study continued from a case study submitted in 2014?: No

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1. Summary of the impact

University of Bristol (UoB) research has improved the welfare of over 84 million farm animals. We achieved this by developing new, quantifiable animal observations (outcome assessments) to evaluate the effects of environment and management on welfare. In collaboration with national farm assurance schemes, outcome assessments have been implemented on 16,400 UK farms. The UoB-led AssureWel project has improved farmer and veterinary practice, benefiting the welfare of six of the main terrestrial livestock types. Welfare outcome assessments and management strategies are integrated into Defra and RSPCA guidance, have informed UK government policy on beak trimming, are incorporated into UK food retailer supply chain, and have informed farm assurance schemes and official welfare guidelines in Europe and North America.

2. Underpinning research

Welfare outcome measures are quantifiable indicators that provide a direct measure of the welfare of the animals assessed. Previous assessments focussed on factors that influence welfare (inputs), such as environment and housing, rather than the effect (outcome) on the animals. University of Bristol (UoB) research has developed protocols for on-farm outcome assessments of health, physical condition and behaviour, for use in farm assurance schemes.

Research funded by the British Pig Executive (BPEX) [i] focused on optimising the validity, repeatability and feasibility of outcome assessments for farm assurance schemes. Farmers use these outcome assessments to focus their management in the most effective way to improve animal welfare. These studies on pig husbandry within the UK, included the first experimental evaluation of the impact of sampling strategy on the estimated prevalence of welfare outcome measures [1], revealed the influence of time of day on assessment results [2], and investigated repeatability of assessments [3]. This body of work generated specific recommendations for the implementation of welfare outcome measures into farm assurance schemes including a defined list of five measures, which need to be assessed every quarter by an attending veterinary surgeon. These recommendations were incorporated into the ‘Real Welfare’ scheme for farms/farmers during the final stage of pig rearing/production (finishing). Following a period of preparation by the industry, including training of all pig veterinary surgeons, the recommendations were implemented in full by Red Tractor and BPEX from April 2013.

Alongside research in pigs, a major grant from the Tubney Charitable Trust [iii] enabled UoB, in collaboration with RSPCA and the Soil Association, to establish bespoke welfare outcome assessments for five other key terrestrial livestock types (laying hens, broiler [meat] chickens, dairy cattle, beef cattle and sheep), and accelerate the implementation of outcome measures within farm assurance schemes – The AssureWel Project.

In laying hens, one of the five outcome measures identified was feather cover [4], an indicator of injurious pecking (IP). IP includes gentle and severe feather pecking (pecking at the tips of feathers, and pecking, pulling and removal of the feathers of other hens, respectively) and vent and cannibalistic pecking (pecking at the skin and underlying tissues of other hens). IP has significant implications for bird welfare, health, mortality and productivity [5]. IP is routinely managed by beak trimming; beak trimmed flocks show less severe feather pecking and have lower mortality at 40 weeks [5]. Beak trimming is considered a mutilation, and consequently is prohibited by EU legislation, with a derogation to allow the procedure to prevent injurious pecking. The UK government is committed to regularly reviewing the need for this derogation, with the intention of implementing a ban on beak trimming if IP can be successfully managed via other means.

A systematic review of the literature (funded by the Tubney Charitable Trust [ii]) identified potential management strategies, which were used to develop bespoke management packages. The data, gathered across 100 flocks on 63 farms, showed that employing a bespoke management package (53 flocks) was associated with 12% lower plumage scores and 24% fewer severe feather pecks compared with control flocks (no management package, 47 flocks) and that the more strategies employed, the lower the levels of IP [5]. This evidence [5] was used to produce the FeatherWel guide, freely available to stakeholders, to inform and disseminate best practice management strategies for commercial flocks and was later incorporated into the AssureWel project and manual. A Defra-commissioned study carried out by UoB [6] supported farmers with non-beak trimmed flocks to employ strategies from the FeatherWel guide to manage IP. These strategies were found to be generally beneficial; however, rates of IP were very variable, and where IP did occur damage was rapid and severe.

3. References to the research

1) Mullan S, Browne WJ, Edwards S, Butterworth A, Whay HR, Main DCJ. (2009). The effect of sampling strategy on the estimated prevalence of welfare outcome measures on finishing pig farms. Applied Animal Behaviour Science, 119:39-48. DOI: 10.1016/j.applanim.2009.03.008

2) Mullan S, Edwards SA, Butterworth A, Whay HR, Main DCJ. (2009). Interdependence of welfare outcome measures and potential confounding factors on finishing pig farms. Applied Animal Behaviour Science, 121(1): 25-31. DOI: 10.1016/j.applanim.2009.07.002

3) Mullan S, Edwards SA, Butterworth A, Whay HR, Main DCJ. (2011). Inter-observer reliability testing of pig welfare outcome measures proposed for inclusion within farm assurance schemes. The Veterinary Journal, 190(2):e100-109. DOI: 10.1016/j.tvjl.2011.01.012

4) Main DCJ, Mullan S, Atkinson C, Bond A, Cooper M, Fraser A, Browne WJ. (2012). Welfare outcomes assessment in laying hen farm assurance schemes. Animal Welfare, 21, 389–396. DOI: 10.7120/09627286.21.3.389

5) Lambton S, Nicol CJ, Friel M, Main DCJ, McKinstry JL, Sherwin CM, Walton J, Weeks CA. (2013). A bespoke management package can reduce levels of injurious pecking in loose-housed laying hen flocks. Vet Record, 172: 423 429. DOI: 10.1136/vr.101067

6) University of Bristol, School of Veterinary Science (2015). Defra Project AW1145: A study to test the effectiveness of management strategies in reducing injurious pecking of laying hens with intact beaks in non-cage systems

Grant Funding:

i) Main DCJ. Adding value to farm assurance: On-farm evaluation of health and welfare outcomes, British Pig Executive (BPEX), 2006 – 2009, GBP247,067

ii) Sherwin CM, Main DCJ, Nicol CJ, Weeks CA. Reducing injurious pecking by implementing existing knowledge, Tubney Charitable Trust, 2008 – 2011, GBP886,294

iii) RSPCA, Soil Association and UoB, AssureWel project, Tubney Charitable Trust, 2010 - 2016, GBP2.7 million

iv) Nicol CJ. A study to test the effectiveness of management strategies in reducing injurious pecking of laying hens with intact beaks in non-cage systems, Defra, 2012-2015, GBP464,055

4. Details of the impact

National implementation of welfare outcome assessments

From 2011 to 2017, welfare outcome assessments [1-3, 5] were implemented within farm assurance schemes across the UK. The AssureWel project developed freely available, scheme-specific protocols and implemented welfare outcome assessments into the UK ‘Red Tractor Assurance’, ‘RSPCA Assured’ and ‘Soil Association Certification’ schemes. Guidance and best practice were distilled in the final AssureWel Manual, which is available to download or as a printed copy; it is used across the farming, supply chain and food retail industries to improve animal welfare. From 2013 to 2020, over 200 farm assurance assessors from the UK, Europe and the USA were trained on farms and via the AssureWel webtool. This was the only major new national initiative at the time to focus on these outcome measures and helped farmers to seek support from other sources. UoB researchers provided expert consultancy on welfare outcome assessment to NGOs including Compassion in World Farming and World Animal Protection.

Data from AssureWel associated schemes shows that, for pigs, dairy cows and non-cage laying hens, >95% of all farms in the UK are incorporated in the schemes (Table 1) [A].

Table 1 – Summary of welfare outcome assessment implementation (2019).

### Species (Schemes: ### a=Red Tractor, b=RSPCA, c=Soil Association)	### No. (%) UK farms within schemes	### No. animals on those farms	### No. animals assessed per cycle
Laying hens (b,c)	1,400 (>95% of non-cage farms)	20,000,000	70,000
Pigs (a,b,c)	1,600 (>95%)	5,000,000	1,600,000
Dairy cows (a,b,c)	11,000 (>95%)	1,800,000	110,000
Beef cattle (b,c)	1,100 (5%)	65,000	22,000
Sheep (b,c)	1,000 (2%)	400,000	20,000
Broilers (b,c)	300 (5%)	57,000,000	2,500,000
Total	16,400 (18%)	84,265,000	4,322,000

Improved animal welfare

Pigs – Data collected via the ‘Real Welfare’ scheme shows ongoing improvements in pig husbandry and welfare [Bi]. The UK Chief Veterinary Officer welcomed the Real Welfare report [Bii], describing it as ‘a practical way of monitoring changes and promoting welfare improvements over time, as well as supporting the industry in demonstrating welfare standards to consumers and retailers’ [Biii].

Laying Hens – Peer-reviewed analysis of welfare outcome assessments in non-caged laying hens reveals that feather loss, an indicator of injurious pecking, has reduced by 35% on the head/neck region and additionally 31% over the back/vent [C]. Updated data suggests that this welfare benefit for approximately 1,800,000 birds is being maintained over time (Figure 1) [A].

Cattle – Compared with 2014 baseline data, in 2018, 45,000 fewer cows were lame (28% reduction), 18,000 fewer were fat (38% reduction), 72,000 fewer suffered from hair loss lesions or swellings (HLS) (45% reduction), and 135,000 fewer were dirty (64% reduction) (Figure 2) [A]. Not only is lameness painful and requires treatment, it also leads to production losses estimated at GBP248 per case or GBP11,200,000 per year to the UK industry.

Figure 1 – Proportion of laying hens recorded with slight (blue) and severe (orange) feather loss on two body areas over time (mean: 766 farms and 38,300 birds assessed per year).

Figure 2 – Proportion of cattle recorded as lame, thin, fat, with hair loss, lesion or swelling (HLS), or dirty over 5 years (Sep 2013 – Aug 2018) (mean: 7,000 farms and 70,000 cows assessed per year).

Informed national regulatory policy

Based on the evidence from the Defra commissioned study into beak trimming [6] and advice from the Beak Trimming Action Group (BTAG) [Di] of which Professor Nicol was a member, in 2015 the UK government decided not to ban beak trimming [Dii]. The then Secretary of State for Environment, Food and Rural Affairs added that ‘the BTAG report also identified improved management techniques that could reduce feather pecking. The Government expects to see these techniques introduced across the laying hen sector’ [Dii]. The majority of mainstream laying hen flocks are beak trimmed (cage and non-cage housed; >40 million birds); all of these flocks have a reduced risk of severe outbreaks of cannibalism as a result of the UK government’s decision not to ban beak trimming.

Codes of practice for farm animal welfare developed by Defra under the Animal Welfare Act (2006) have a regulatory role to help establish or disprove a person’s liability if a case reaches prosecution. The codes of practice for Laying Hens and Pullets [Ei], Meat Chickens and Meat Breeding Chickens [Eii] and Pigs [Eiii], all promote welfare outcome assessments to monitor welfare and direct users to the UoB-led AssureWel and FeatherWel projects for guidance on measuring welfare outcomes.

The Lion code, which applies to approximately 95% of UK egg production, requires producers to implement at least six management strategies from the FeatherWel guide [Fii]. In addition, the RSPCA Welfare Standards for Laying Hens (2017) [Gii] require that all of their farms (housing more than 20 million hens) have a copy of the FeatherWel guide, are familiar with the contents and implement the recommendations as appropriate. Moreover, many of the welfare standards for pullets and laying hens in the RSPCA Assured scheme include ‘requirements and guidance based on research and work by The University of Bristol’ [Gi]. Implementation of strategies from this guide benefits the welfare of the majority of loose-housed laying hens in the UK (more than 20 million hens annually).

Informing international farming practice

AssureWel International is a group of stakeholders including representatives from farm assurance schemes in the USA, Germany, Austria, Netherlands and Serbia who have implemented welfare outcome assessment and maintain an online training and knowledge hub. Dr Mullan also leads the Global Animal Welfare Assurance (GAWA) initiative, an international alliance of higher welfare schemes, which requires monitoring of welfare outcomes by members.

In 2018, UoB were contracted to develop welfare outcome measures for the Belgian Pig Assurance Scheme (Belpork) covering 2,500 farms representing 50% of national production [H]. Dr Mullan led stakeholder workshops, pilot testing of measures and training of assessors enabling the scheme to begin formal monitoring of welfare outcomes in February 2020.

Hennovation, an EU-funded Horizon 2020 project (UoB-led) used the laying hen industry as an example of initiating change through farmer led innovation. The project produced Feather Pecking Guidelines’ [I] educating stakeholders with regard to the management of feather pecking. These guidelines [I] were co-authored by Dr Weeks, referred to the FeatherWel website, and have been translated into Dutch, Spanish and Czech.

Change in practice by UK food retailers

Major UK food retailers have included welfare outcome measures within their supply chain requirements and acknowledge direct support of UoB in the process through provision of training to employees (Marks & Spencer: ‘Operationally, we’re supported by our suppliers and expert organisations such as Bristol University. All our agriculture managers are externally trained in animal welfare by Bristol University’, Sainsbury’s: ‘We ensure that all relevant internal colleagues receive training on our health and welfare policies to guarantee their effective implementation. Recent examples include University of Bristol animal welfare courses’ and The Co-operative:

‘We are working with….The University of Bristol to trial a new method of measuring chicken welfare called Qualitative Behavioural Assessment (QBA).’), with the importance of this process being highlighted publicly in the drive to improve welfare by these and other retailers (Morrisons, Tesco and Waitrose) [J].

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Table 1 – Summary of welfare outcome assessment implementation (2019).

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