What has the animal rights movement done for animal welfare? Are we about to see a relaxation of the “strictest regulation in the world” over the use of animals in biomedical research in the UK? Scientists may welcome this and animal rights campaigners may not, but more importantly, what effect could this have on the welfare of animals used, and therefore on the quality of science in our laboratories? Sarah Wolfensohn1 Matthew Maguire2 Veterinary Services, University of Oxford, and 2University College London Medical School, UK 1

Title image. A mouse heart undergoes tests in a medical research laboratory. Photo: ©Bill Parry 22

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urveys show that public acceptance of use of animals in research has improved in the last decade and about three quarters of people accept such research is necessary to make medical progress (www.understandinganimalresearch. org.uk). However, animal welfare remains high on the political agenda and ministers recognise the spread and depth of public engagement on animal welfare issues. Complacency about that improved level of acceptability cannot be used as an excuse to allow any drop in standards. The revision of the EU Directive that con-

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trols the use of animals in biomedical research is currently being debated in the European Parliament and the Council of Europe and has been circulated widely for consultation (http:// scienceandresearch.homeoffice.gov.uk/animalresearch/legislation/Revision_of_EC_86-609. pdf). Add to this process the Better Regulation agenda (http://scienceandresearch. homeoffice.gov.uk/animal-research/legislation/ better-regulation) following the Hampton and Davidson reviews, and a new slimmed down application form for experimental projects about to be launched by the Home Office, and

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we have the opportunity for streamlined regulation. But is this an area where less process results in better outcomes? Animal use in bioscience Animal rights campaigners have, over time, helped to create an environment in which animal welfare is at the forefront of thinking about research using animals. Animals have been used in experiments at least as far back as the 3rd century BC, to Eristratus and Herophilus, and to Galen in the 2nd century AD. The birth of modern laboratory science can be attributed to William Harvey, who in 1628 discovered the circulation of the blood using live animals. As the use of animals in research increased, so did opposition to vivisection and in 1789 Utilitarian philosopher Jeremy Bentham asked a fundamental question on the use of animals in science: “The question is not can they reason, nor can they talk, but can they suffer?” The acceptability, or otherwise, of causing animals to suffer in the name of scientific progress is at the heart of the debate. The central question was, and still is, whether the harm to the animals caused by the research can be justified by the benefits to humans and animals that the research brings. This ‘utility versus morality’ question is essentially embedded in the modern Ethical Review Process, which is there to analyse every new research proposal and which looks at the benefit of the research (utility) versus the harm or suffering to the animal (morality). All new experimental work proposals undergo this evaluation by a panel of scientific experts, laypersons and animal welfare specialists based on a harm-benefit analysis, and was established in the UK in 1999. Yet the success of its implementation in individual research establishments depends very much on the prevailing culture of care and the authority of the ethical review committee; and numerous factors have been identified which can impede the progress of refinement (Lloyd et al, 2008). Historically, there have been some attempts at self-regulation by the scientific community. In 1831, Marshall Hall tried to establish his ‘Five Principles’ for experimental research and in 1871 the British Association for the Advancement of Science (BAAS) published a moral code of practice for use when working with experimental animals. Sadly neither was adopted by researchers. In 1875 Frances Power Cobbe founded the ‘Victoria Street Society for the Protection of Animals Liable to Vivisection’, which campaigned for the abolition of experiments using live animals and played an important part in

pressing for legislation and control over such experiments – in 1876, the Cruelty to Animals Act was passed by Parliament concerning the use of animals in research. The society divided in 1898 into the National Anti-Vivisection Society (NAVS) and the British Union for the Abolition of Vivisection (BUAV) and these two separate societies are still active today, both campaigning for abolition of the use of animals. The 1876 Act was a compromise between the abolitionists and the scientific community which left neither side happy: the welfare lobby felt let down as experiments were still permitted, while the scientists were outraged that their authority on matters of science was being challenged by non-scientists. The arguments were not simply about animal welfare but were influenced by wider social issues. Science is interconnected with the society in which it exists; attitudes and behaviour toward it are deeply embedded in the social, intellectual, cultural and political history of the period (French, 1975). The nineteenth century was a period of mass social upheaval, largely associated with the industrial revolution. As families flocked to the centre of towns seeking employment, society moved away from the countryside and the humananimal relationship was altered, animals becoming accepted as companions rather than livestock. This changed experience of the daily interactions with animals altered the public perception of how animals should be treated. The anthropomorphic literature that was published at the time exemplifies this: the ‘Beatrix Potter’ books read by children and families highlight the new perceptions of animals as friends, rather than a source of food (Figure 1). Figure 1. Rabbit – laboratory, pet, wild or food source? The animal’s quality of life and the perception of its welfare are not affected by the reason for its life or the cause of its suffering (Wolfensohn and Honess, 2007).

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Public perceptions In the face of increasing concern for animal welfare, the scientific community did little to reassure the public that their reasons for animal experimentation were ultimately humane and directed toward discovering cures that could benefit the general public. As science considered itself autonomous, a certain arrogance characterised the scientists of the day, who not only thought themselves above answering to the layperson, but believed the public could not understand science, as a doctor suggested in The Lancet in 1902: “Physiology is not a subject that can be made intelligible to the public at any time.” By becoming ‘scientific’, medicine was able to distance itself from quackery and gain recognition as a respectable profession. It was this battle about cultural authority and a fear among the clergy and aristocracy that science was becoming too powerful (Rupke 1990) that was at the root of the debate, rather than a primary concern for the welfare of animals. The scientific community’s limited efforts to engage the general public on the matter of experimentation, coupled with the belief that it should be free from interference from those attempting to regulate their profession, continued until the Association for the Advancement of Medical Research (AAMR) was founded in 1882, and became the Research Defence Society (RDS) in 1908. However, these efforts ceased as scientists moved from outrage at being interfered with, to dismissal. The RDS Quarterly Journal of 1915 claimed: “We cannot argue with them, for it is a waste of time, for they will not admit when they are wrong.” The matter had reached an impasse: there was no longer any real effort from the scientific community to see the debate from the point of view of the welfare lobby, which they dismissed as too stupid or too unreasonable; the abolitionists in turn dismissed scientists along the same lines and made no effort to reach a compromise. The anti-vivisection movement became synonymous with ‘animal rights’, and reemerged in the 1960s, gathering momentum once more. This was a period of cultural and social revolution with different social contexts from the previous century. Modern disease control meant that society was not as exposed to human pain and suffering as it was in the nineteenth or even early twentieth centuries (Paton, 1993), so it became more sensitive to visions of pain and suffering in animals. The 1960s also saw the birth of ‘investigative’ journalism, which provided a means of producing ‘shocking’ images of animals being used in research. 24

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The images and accounts of animals suffering in research, made available to a more sensitive general public, gave rise to a rebirth of the anti-vivisection sentiment and animal welfare groups gained increased support. In the absence of any image projected by scientists beyond a ‘closed door’, the public created its own, and the image of the ‘mad scientist’ vied for public attention with the likes of ‘Peter Rabbit’. The term ‘vivisection’ is still in use as a pejorative despite its definition as “the practice of operating on living animals in order to gain knowledge”. In the 19th century, the development of anaesthesia was in its infancy and much of the research involved surgical procedures (Figure 2). In the 21st century, only a small fraction of animals used in research undergo surgery, and all such operations use sophisticated modern anaesthetic techniques. In the UK in 2008, 38% of procedures were the breeding of geneticallyaltered rodents (http://scienceandresearch. homeoffice.gov.uk/animal-research/publications-and-reference/statistics) and did not involve surgery (Figure 3). After several years of campaigning, the rise of modern concern for animal welfare achieved new legislation, the Animals (Scientific Procedures) Act of 1986, and a new era of “the most comprehensive regulations covering laboratory animal welfare” began. The RDS was revitalised and a number of new ‘pro-research’ societies formed which included representatives from charities and patients grateful to medical research. The aim of these groups was to explain and defend the actions of the scientific community. Scientists no longer presented themselves as superior to the general public, but rather as working with them for their benefit. There has been an increased effort to educate the public on the central role of animal welfare in science but modern scientists face a number of challenges in communicating with the general public. The rapid advances in, and specialisation of, science is a barrier to sound public understanding of the debate, as are a decline in the level of scientific understanding amongst the public and the increased complexity of molecular biology, genetics, immunology and proteomics. Even if scientists do make time outside research, teaching and administration for public outreach, it is an activity which gets little recognition since academic success tends to be judged only on research performance criteria. There are disincentives in a system that emphasises published and peer-reviewed work over development of policy and advice.

Animal welfare

Since only 10% of MPs have a scientific background, it is particularly important that this engagement is carried out, in order to support those who are responsible for policy making. As John Denham, then Secretary of State for Innovation, Universities and Skills, said in 2008: “Public engagement, whether outreach work, media appearances or advising government, should be included as a key performance indicator” (www.dius.gov.uk/ news_and_speeches/speeches/past_ministers/ john_denham_160108.pdf). Animal welfare Perhaps more critical than forcing the scientific community to communicate about animal research is the effect the campaigners have had on animal welfare itself. It is certainly the case that over time they have drawn attention to some inexcusable treatments of animals. William Sharpey remarked in 1875 on an experiment performed by Magendie, “who made incisions into the skin of rabbits to show that the skin is sensitive. Now surely all the world knows the skin is sensitive, no experiment painful or without pain is needed for that” (Sykes, 2001). In 1985 the Royal College of Surgeons was fined £250 after a breeding monkey was found unconscious and dehydrated at their animal research unit (Samstag, 1985). Animal cruelty has taken place and the anti-vivisectionists have rightly called attention to it. The research community has the duty to get, and keep, its house in order. Campaigners have played a vital role in bringing about legislation to control animal research. The 1822 Martin’s Act against cattle cruelty, the 1876 Cruelty to Animals Act, and the 1986 Animals (Scientific Procedures) Act all owed an enormous amount to campaigners bringing the issues into the public arena and raising awareness. Since 1994, anyone wishing to hold a licence permitting experiments on animals has had to participate in accredited training programmes. The establishment in 1999 of the Ethical Review Process owes much to the awareness of, and importance placed on, animal welfare and the ethics of animal research. The introduction of these two elements has also helped to reinforce and improve awareness within the scientific community. Training reinforces self-regulation: it helps participants understand that, given the context of public debate, one aberration from accepted practice has consequences not just for the individual but for the whole research community. There is now a certain degree of peer pressure in many establishments to ensure that the welfare of animals is a paramount concern,

Figure 2. Vivisection. Painting by Emile-Edouard Mouchy of the dissection of a living dog (1832) (The Wellcome Institute Library, London).

both from a genuine concern for the welfare of the animals and also from an awareness of the wider consequences for public support and opinion. However, in the latter part of the 20th and the start of the 21st century animal rights campaigners have contributed less to the improved welfare of animals. Indeed many campaigns of the past 20 years have worked against animal welfare and there are numerous examples. Fear of attack has created anxiety within the scientific community, restricted the number prepared to speak out on the merits of animal experimentation and slowed progress within the scientific community in improving conditions; but all without reducing suffering to animals. Many perfectly good breeding centres for research animals have been targeted by direct action and closed (Toomey, 2005). The consequence is that some animals now have to travel many miles by air, sea or road to reach the research laboratories, causing stress which is separate from, but additional to, the actual experimental procedure; thus leading to greater potential total suffering. Although the anti-animalresearch movement originally helped to drive improvements, the effect of the campaigns of the second half of the 20th century has been bad for animal welfare (Smith, 2006). Direct action has profoundly reduced the effective sharing of best practice within the scientific community. The implementation of strict security reduces the ability to meet colleagues and exchange information that may improve animal welfare and scientific quality. Any genuine occurrences of animal suffering are not discussed openly for fear of retribution Biologist Vol 57 No 1 February 2010

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Figure 3. Modern use of animals in research. Most of today’s research is carried out on rodents (77%) and involves the study of genetic effects, not surgery.

by animal rights extremists, or even action by the regulatory authorities. Opportunities to learn from the mistakes of others or to publicly condemn any negligent incidents cannot be taken because of genuine security fears and there is a lack of open debate. Problems are not solved, but may be swept under the carpet and solutions neither sought nor implemented. There has been a debate in the scientific community (Wurbel, 2007) about the inclusion of sufficient information in the methods sections of papers. Many journals wish to keep word counts down and as a result only publish either scant methods sections or publish them separately online. Inevitably, where words are tight, it is the welfare aspects of methods that get left out. An additional consequence of animal rights campaigns is the possibility of animal research moving abroad. Globalisation has been called the “most powerful force for social good in the world today” (Bhagwati, 2007), pharmaceutical companies operate internationally and academia also finds value in establishing collaborations with international institutions. Yet, experiments may then be conducted in countries which have a more relaxed interpretation of the EU Directive, or which are outside the EU’s jurisdiction – and this holds the potential for an alternative level of animal welfare. There are also issues over loss of control, intellectual property, and confidentiality that have to be addressed with the outsourcing partners. However, by focusing on negative aspects of globalisation, we may be missing the opportunity to focus on accelerating its achievements; since, with appropriate precautions, there exists an opportunity to significantly improve the welfare of research animals around the world. 26

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Campaigns against animal research can feel like a modern phenomenon (Figure 4), but they have existed since the end of the 18th century and, while there are differences, there is also much common ground between that period and the modern period of campaigning. There has been: a characterisation by campaigners, with elements of truth, of scientists as remote and arrogant; a slow but real effort by the scientific community to explain their work better in response; challenges for scientists in trying to explain specialist knowledge to laypeople; and a focus on the ‘harm-benefit’ balance of animal research as the core of the ethical debate with the accompanying desire to reduce harm by improving animal welfare. In both periods, there were broader social undertones to the debate, though these contrast markedly: in the 19th century those against animal research were mainly the clergy and aristocracy keen to preserve their social power in the face of the march of science, whereas in modern times campaigners have tended not to hold positions of power. Probably the most significant difference between the campaigns of the two periods was the emergence in the 20th century of ‘direct action’, including action (often outside the law) intended to cause fear, intimidation and economic or even personal damage. It was primarily the emergence of direct action that changed the animal rights campaign in the late 20th century into one that no longer effected improvements in animal welfare; indeed one that actually hampers progress. The modern research community generally puts the ethics of animal experimentation at the heart of all its work, and the aim for the future must be not only to maintain this high standard of animal welfare but to continue to seek improvement. The revision of EU Directive 86/609 currently passing through the debating chambers encompasses many of these principles. That and the implementation of the Better Regulation agenda are both opportunities to embed the improvements in the regulations that control and facilitate this work. Yet, we cannot treat this as an opportunity for the research community to relax and return to its previous ways. Some argue that past failures show that self-regulation does not work in the environment of animal research; however, the changes emanating from Better Regulation mean that the role of animal welfare campaigners must be to work with the research community, not against them. This will require an openness and accountability that is simply not possible with current security levels.

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There must be freedom to report and discuss problems and ‘near misses’. ‘Near miss’ reporting is now accepted practice in air traffic control where problems are considered as the starting point for improving future performance. It is necessary to take an honest look at performance and use problems as an opportunity to learn. The only sustainable and effective way forward is for animal welfare lobbyists and the scientific community to understand each others’ point of view in a framework which depends on a strong ethical base and regulatory constraints that are light touch but rigorously enforced when necessary. In this way the current fortress mentality becomes unnecessary. This is the only attitude that can genuinely improve the welfare of animals in the years to come and benefit everyone through the scientific and medical advances for which research using animals is currently still essential. References Bhagwati J (2007) In Defense of Globalization. Oxford University Press French R D (1975) Anti-vivisection and Medical Science in Victorian Society Princeton University Press Lloyd M H, Foden B W and Wolfensohn S E (2008) Refinement: promoting the 3Rs in practice Laboratory Animals 42, 284-293 Paton W (1993) Man and Mouse: Animals in Medical Research. Oxford University Press Rupke N A (1990) Vivisection in Historical Perspective. Pro-vivisection in England in the Early 1880s: Arguments and Motives. Routledge London Samstag T (1985) Vivisection not an Issue, court told. The Times July 2 Smith K (2006) Caught in the Middle Nature 444 p 14 Sykes A (2001) Sharpey’s Fibres; the life of William Sharpey the Father of modern physiology in England. Sessions of York 2001 Toomey C (2005) Fierce Creatures. The Times April 24 2005 Wolfensohn S and Honess P (2007) Laboratory animal, pet animal, farm animal, wild animal: Who gets the best deal?

Figure 4. Demonstrators in Oxford protesting recently against the construction of a new biomedical research facility. UFAW Symposium: Quality of Life: The Heart of the Matter. Animal Welfare 16 supplement 1 117-123 Wurbel H (2007) Publications should include an animal welfare section Nature 446 p257

Sarah Wolfensohn (corresponding author) spent a number of years in general practice. She was appointed Head of Veterinary Services at the University of Oxford in 1991. She is a diplomate of the European College of Laboratory Animal Medicine, and a Royal College of Veterinary Surgeons Recognised Specialist in Laboratory Animal Science. She was a member of the implementation group for the Government’s Animal Health and Welfare Strategy for England and is a member of the Animal Procedures Committee. Email: sarah.wolfensohn@vet. ox.ac.uk. Matthew Maguire is a medical student at University College London. In his intercalated BSc in Medical Science with the History of Medicine, his dissertation focused on the changing attitudes towards animal experimentation.

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