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. 2020 Jun 19;15(6):e0234922. doi: 10.1371/journal.pone.0234922

A semi-structured questionnaire survey of laboratory animal rehoming practice across 41 UK animal research facilities

Tess Skidmore 1,*, Emma Roe 1
Editor: I Anna S Olsson2
PMCID: PMC7304590  PMID: 32559221

Abstract

If a laboratory animal survives an experiment without lasting compromised welfare, its future must be negotiated. Rehoming may be a consideration. This paper reports on research findings that provide an indication of the uptake of animal rehoming by UK facilities and the associated moral, ethical, practical and regulatory considerations that inform decisions to rehome or not. This research addresses a widely acknowledged gap in the literature to understand both the numbers, and types of animals rehomed from UK research facilities, as well as the main motivations for engaging in the practice, and the barriers for those facilities not currently rehoming. From the ~160 UK research facilities in the UK, 41 facilities completed the questionnaire, giving a response rate of approximately 25%. Results suggest rehoming occurs routinely, yet the numbers are small; just 2322 animals are known to have been rehomed between 2015–2017. At least 1 in 10 facilities are rehoming. There exists a clear preference for the rehoming of some species (mainly cats, dogs and horses) over others (rodents, agricultural animals and primates). Indeed, although 94.15% of species kept in laboratories are rodents, they make up under a fifth (19.14%) of all animals known to be rehomed between 2015–2017. The primary motivation for rehoming is to boost staff morale and promote a positive ethical profile for the facility. Barriers include concern for the animal’s welfare following rehoming, high scientific demand for animals that leaves few to be rehomed, and, finally, certain animals (mainly those genetically modified) are simply unsuited to rehoming. The findings of this research will support facilities choosing to rehome, as well as those that are not currently engaging in the practice. By promoting the practice, the benefits to rehoming in terms of improving laboratory animal’s quality of life, helping facility staff to overcome the moral stress of killing, and addressing public concern regarding the fate of laboratory animals, can be attained. It is only once an understanding of rehoming from the perspective of UK research facilities has been ascertained, that appropriate policy and support can be provided.

Introduction

Rehoming is defined by the UK Home Office (pg. 10) as “the movement of a relevant protected animal from an establishment to any other place that is not an establishment under A(SP)A.” The “place” referenced is most commonly a farm, aquarium, zoo or private home [1]. Directive 2010/63/EU states that animals can be rehomed if: “the state of the health of the animal allows it”, “there is no danger to public health, animal health, or the environment”, and if “appropriate measures have been taken to safeguard the well-being of the animal”[2]. The Directive makes explicit that those animals whose welfare would be compromised if rehomed should be killed at the end of experiments [2].

The practice of rehoming is guided by the notion that animals are sentient beings and worthy not only of avoiding suffering, but also of experiencing a good quality of life [3]. Despite laboratory animals’ role in important medical advances, the use of animals in scientific research remains a controversial issue [4]. Rehoming addresses the arguably unnecessary killing of some animals after being used in a scientific procedure. The killing of research animals is undertaken for three primary reasons– 1) as a scientific requirement, 2) to prevent avoidable suffering (euthanasia), or 3) for financial/logistical reasons [5]. As will be discussed, the main opportunity for rehoming lies where humane killing would otherwise take place for financial or logistical reasons.

‘Surplus’ or “bred but not used” [6] animals are often cited as the most appropriate candidates for rehoming [5] for the following reasons. Firstly, surplus animals have not been subject to research, and thus long-term health implications (often cited as a barrier to rehoming) are less likely to represent a risk [7]. Secondly, rehoming these animals typically presents a lower risk of disease transmission [5]. Thirdly, the “moral stress” [8] experienced by those associated with the killing of these animals tends to be higher for surplus animals because of a cultural awareness of ideas of waste. Killing these animals can be perceived as “wrong”—especially when the animal could be placed in a potential home [5, 9]. Thus, rehoming laboratory animals may benefit staff morale [10].

The reasons to consider rehoming are not only proposed by those working inside the laboratory; public opinion should also be taken into account. Killing, even when undertaken humanely, can evoke strong negative emotions in the public [11]. Some may view it as an infringement on the right to life, underrating its inherent value [5]. Euthanasia may have more positive connotations in the veterinary clinic setting when companion animals are relieved of suffering, but in the animal laboratory, issues with routine killing are compounded within a setting where animals are systemically harmed for human benefit. Thus, research should seek to address societal concerns and reflect these concerns appropriately within policy guiding animal research.

Indeed, despite the widely recognised benefits to rehoming, and concerns surrounding the routine nature of killing within animal research facilities, no literature quantifies how many animals are rehomed from UK laboratories. However, existing research speculates that it is likely to be undertaken with very small numbers of animals [5], and thus currently constitutes the exception rather than the rule. There is a lack of research that explores the extent of laboratory animal rehoming practices at a national level, nor is there much detail regarding the process of laboratory animal rehoming when it does occur.

Rehoming and animal welfare

Attaining high standards of animal welfare in the farm, zoo, laboratory, and for companion animals is an important societal concern [12]. Animal welfare typically includes a consideration of animal’s affective state (pain), biological functioning (injuries), and sometimes also a consideration of naturalness (such as pasture access) [13]. Novel and innovative approaches for achieving good animal welfare are increasingly considered. The rehoming of laboratory animals represents one way in which attempts could be realised, as the registers of ethical concern about practising good animal welfare shift towards the case for more rehoming. This section will examine how rehoming represents both an opportunity to improve, but equally compromise, animal welfare.

The Farm Animal Welfare Committee (FAWC) proposed the notion of “a life worth living” [14]. A life worth living means that the balance between negative and positive experiences is favourable, and is achieved by complying with minimum welfare standards coupled with the promotion of positive experiences [15]. It includes the degree to which the animal is provided with its needs and wants, resulting in good health and happiness, and also longevity [16]. Longevity in the context of rehoming is important, as the practice could help to extend animal lives as well as promoting positive life experiences. If an animal would have a life worth living, then death is contrary to the animal’s individual interests, as it involves the absence of positive states [17]. Rehoming represents a way to enhance quality of life, and extend life. Hence, research should examine the processes by which it occurs in order to understand best practice, improve policy and promote rehoming as an option once research is concluded. The voice of researchers is valuable here: “Don’t we, as researchers, owe our animals a different life after they have completed their contributions to science?” (pg. 506) [18].

However, it is also crucial to acknowledge that rehoming is not always in the best interests of the animal, and may instead serve to compromise welfare. Current UK regulatory guidance, such as the Animals in Scientific Procedures Act (1986), or A(SP)A, helps to ensure standards of welfare are maintained in the laboratory, yet once rehomed this legislation is no longer in place to protect the animal in question. It is thus the responsibility of the facility to ensure that rehoming will in no way compromise welfare [19]. This must remain an absolute priority. Factors that can affect welfare during the rehoming process are the animal’s state of health, the duration and condition of transport to the new home, and the social and/or physical environment the animal will be moved to [7]. Research notes that potential compromises to welfare can be minimised or eradicated with careful and thorough planning of key processes such as transport [7] and socialisation [9, 19] to lower animal stress.

Existing research on laboratory animal rehoming

There is a lack of academic literature focusing specifically on the politics, ethics and practices of laboratory animal rehoming, and that which has been undertaken focuses on the success of rehoming practice. This includes research on the rehoming of cats [20], dogs [19, 21, 22], ferrets [23] and primates [7, 18]. Research shows beagles have a high adaptive capacity, fit in well with families and thus make good companion animals [21]. Within 6–12 weeks of rehoming, behaviour tests on the dogs reflected relaxed body language, as well as reduced heart rates, signifying calm behaviour once settled in the home environment [21]. Research also found cats were successfully rehomed from a research facility, with a retention rate of 93.5% [20]. Of those rehomed, 80.4% were considered a valued family member, and behavioural problems were reported in just 11.3% of the cats within 6 months of adoption [20]. Finally, a study revealed that Cornell University have developed a successful direct adoption scheme, and that the University of California, San Francisco employs an indirect scheme, whereby animals are transported to a third party shelter before rehoming [9]. Both schemes were judged to be successful, with “hundreds” of animals placed in adoptive homes [9]. These case studies convey hope that rehoming as a practice could be successfully institutionalised and adapted to specific facility needs, across a range of sentient species.

However, the overwhelming focus on large mammal species does not provide a comprehensive understanding of all rehoming practice across species. Although companion animals are more commonly considered for rehoming, the practice occurs across many species—including rabbits, rats, guinea pigs and even mice [18]. In fact, the “small size, easy and affordable maintenance and short longevity” (pg. 197) of these animals may reduce the level of commitment needed from potential adopters [5]. Despite this, there has been little work undertaken focusing on rodents, fish or agricultural animals (all of which are commonly used in animal research), and consequently there is a need to expand understandings of rehoming frequency for these species, as well as the channels by which this occurs. This is especially true as the majority of facilities keep rodents [2426], so providing information to support them could increase rehoming prevalence.

Purpose and significance of study

Although existing work evaluates rehoming in specific circumstances, no research has been undertaken to gauge the current situation regarding the numbers rehomed from UK laboratories, and which species are more commonly considered. Existing literature notes this as an essential next step in understanding the rehoming process [9, 27]. This is necessary to enhance animal welfare by following correct rehoming procedures which can help to ensure animal welfare after rehoming, as stipulated by law, and promote the rehoming of laboratory animals where viable. Most of the existing literature is based upon case studies, and focuses on larger mammal species. Finally, although research has identified motivations to rehome and reasons why facilities are not engaging in the practice, no work has quantified which motivations and barriers are considered to be the most important by the research facilities themselves. This is necessary to adapt existing policy accordingly, and support facilities if they choose to rehome their animals in the future.

As such, the key research questions are:

  • How many UK facilities are known to be rehoming?

  • How many animals, and what species, are being rehomed?

  • What are the motivations for rehoming, and the barriers for those not currently participating in the practice?

  • What range of activities does the rehoming process typically involve?

  • What are the main reasons facilities identify for not being able to rehome?

Methodology

Engagement in, and perceptions of, rehoming were measured using a specially designed questionnaire. Reponses were collected between July 2018 –January 2019. The questionnaire was designed using the University of Southampton’s software, iSurvey, a survey generation tool allowing the dispersion of online surveys. The questionnaire was split into 6 sections: 1) Role and background both of the respondent and the facility they represented, 2) The facilities’ rehoming policy, 3) Barriers to rehoming, 4) Opportunities presented by rehoming, 5) The rehoming process, and 6) Reasons for choosing not to rehome animals (S1 Appendix). Logic questions were applied, so the survey format varied between participants, and respondents were only presented with questions relevant to them based upon their previous answers. The survey included both closed and open questions, but comprised mostly of checkbox options, allowing it to be completed quickly and easily. In the case a suggested option was not relevant, participants were able to select an ‘other’ box and manually add in their response. Enabling the survey to be completed online increased convenience for the participant, as well as enabling more efficient distribution. The majority of participants completed the questionnaire within 10 minutes.

Given the sensitive nature of the research and difficulty in contacting participants (staff working at animal research facilities), they were approached indirectly through the auspices of the Animals in Science Committee and the AWERB (Animal Welfare Ethical Review Body) Hub network. It was important that respondents were able to participate on behalf of their facility, because the questions were assessing views at the facility rather than the personal level. Thus, any employee could complete the survey if they had the necessary data/knowledge. Reminder emails were circulated twice to increase participation. 41 facilities out of the ~160 UK research facilities currently operating in the UK completed the survey—giving a response rate of approximately 25%. Incomplete surveys were not counted. Nvivo12 was used to analyse the qualitative responses, Microsoft Excel (2016) to analyse quantitative findings and assist in numerical analysis (including calculating numbers of animals rehomed), and SigmaPlot (Version 13) to enable graph production.

In order to calculate the numbers of animals kept in UK research facilities to enable a comparison to the numbers rehomed, the “total animals used for the first time in experimental procedures”[26] was used. As GA (genetically altered) animals cannot be legally rehomed, the “creation & breeding of GA animals not used in experimental procedures” was omitted from the analysis. To calculate the numbers of surplus animals—which research reports are the most common rehoming candidates—the Home Office document titled “Additional statistics on breeding and genotyping of animals for scientific procedures, Great Britain 2017” was used. This is because it includes, for the first time since reporting began, non-GA animals that were bred for scientific procedures but were killed or died without being used in such procedures. However, it only states the number not used (1.81 million animals) and attributes 80% of the figure to mice, 11% rats and 7% fish. In order to calculate the remaining 2% of ‘other’ animals, we employed a weighting system whereby the same ratios of animals used for the first time in procedures were applied to the remaining 2% of animals (here cats, dogs other than beagles, beagles, primates, horses, rabbits, guinea pigs, gerbils, hamsters, ferrets, birds, quail, goats, sheep, cattle, pigs and amphibians). As these figures are not available for the years 2015 and 2016, we multiplied the figure by 3 in order to get an average across the 2015–2017 reporting years.

Analysing data from the open questions involved a structured inductive thematic analysis. This helped to identify common topics, ideas, concepts and patterns arising from the qualitative, open answer data. In order to do this, we used Nvivo12 to code the data and to generate themes from it. Using Nvivo12, the thematic analysis also entailed a frequency count, whereby it was possible to see the number of times each identified theme was referenced across all participants.

The questionnaire was considered and approved by the University of Southampton’s Ethics Committee. All those who responded to the questionnaire were provided with a participant information sheet, and were given the opportunity to ask questions about the study. Participants provided their consent to participate in the research before completing the questionnaire. Other than protection of personal data and the anonymisation of results, the research was not considered to raise significant ethical issues.

Results and discussion

Context

Participants represented a variety of roles, including but not limited to: Establishment Licence Holders (ELHs), Named Veterinary Surgeons (NVSs), AWERB chairs, Named Animal Care and Welfare Officers (NACWOs), and Named Information Officers (NIOs). In terms of the species kept at facilities, the questionnaire results reflect accurately the wider landscape of UK research institutions [2426]. The majority of facilities that completed the questionnaire had mice (36 facilities), rats (29 facilities), and fish (23 facilities). A small number of facilities kept dogs (6 facilities), primates (4 facilities), horses (4 facilities) and cats (2 facilities). The types of research undertaken at the facilities also varied, including but not limited to; conservation, human medicine development, teaching, and animal behaviour, welfare and nutrition. Both public and private facilities completed the questionnaire.

Number of facilities participating in rehoming

As there are ~160 UK animal research facilities, the 19 facilities that the survey found to be rehoming constitutes approximately 11% of the total number of UK research establishments (Fig 1). It is possible to say with certainty that at least 11.9% of UK facilities are rehoming, and that at least 13.8% have not engaged in the practice from the 2015–2017 period, but scaling up to give speculative figures for the whole sector is not possible. The questionnaire indicates that rehoming is considered as a possibility in UK research facilities. The fact rehoming is often a consideration in UK research facilities is also demonstrated by only one facility of the 41 facilities (which kept solely fish) suggesting that they were “unaware that rehoming was possible” from the closed answer questions.

Fig 1. UK research facilities that have rehomed in 2015–2017 period and completed the questionnaire as a percentage of all UK research facilities.

Fig 1

Comparing numbers of animals kept to those rehomed

Numbers rehomed across the 19 facilities from the years 2015–2017 are very low—just 2322 animals were rehomed (Table 1). Both consideration for rehoming and the numbers rehomed appears to depend heavily upon the species in question. Those species kept in larger numbers (such as mice, rats and fish) are less likely to be rehomed, whilst those kept in smaller numbers, such as cats and dogs, are more likely to be considered (goats and quail provide notable exceptions). Birds are also rehomed in large numbers, although they are also kept in higher numbers within facilities. Despite 10,141 primates being used in research, none of the four facilities that completed the survey and kept primates had rehomed them in the last 3 years. However, it should be noted that primates can be retired from research, whilst still living at the facility.

Table 1. A comparison of numbers of animals kept (using Home Office statistics) from 2015–2017, and numbers known to be rehomed (from 41 facilities that completed the survey).

The colour coding helps to show which animal groups are kept in higher numbers within facilities, and which are rehomed in higher numbers. Higher numbers are represented in more saturated colours.

Numbers kept (first time use in procedure and bred but not used) 2015–2017 across all UK facilities Numbers rehomed of those that completed the questionnaire (n = 41 of the ~160 UK facilities) (2015–2017)
Cats 448 171
Dogs other than beagles 447 71
Horses 1406 69
Gerbils 943 19
Cattle 10580 64
Beagles 10456 44
Hamsters 4742 16
Ferrets 1746 4
Amphibians 14706 31
Fish 1266584 1277
Birds 495889 383
Rabbits 41080 18
Pigs 17211 5
Guinea pigs 83886 18
Rats 1317886 103
Sheep 141941 7
Mice 7912669 22
Goats 726 0
Primates 8196 0
Quail 37 0

There is academic, public and policy acknowledgment of higher levels of sentience in primates [28], and in America, chimpanzees are legally entitled to retirement [29]. Research advocates that, in the US, chimpanzees should be retired as a moral imperative which acknowledges claims for redress against “histories of displacement, confinement and experimentation” (pg. 619) [29], yet in the UK context there exist worries regarding the welfare of rehomed primates. For example, one facility explained they did not currently engage in rehoming due to the difficulty in maintaining primate social groups established in the laboratory, and consequently the negative welfare implications of separation when undertaking rehoming.

Although 94.15% of species kept in laboratories are rodents, they make up under a fifth (19.14%) of all animals known to be rehomed between 2015–2017. Conversely, birds, cats, dogs, horses, amphibians and agricultural animals constitute 80.86% of total species rehomed, despite making up just 5.84% of those kept (see Table 1 for more details). This is based on the following grouping: dogs (beagles and all other dog breeds), small mammals (rats, mice, gerbils, rabbits, hamsters, ferrets, guinea pigs), birds (common quail and all other birds), agricultural animals (cattle, sheep, pigs and goats), and cats, horses, amphibians and primates. Fish were excluded from this analysis due to one outlier facility having rehomed over 1200. There thus exists a preference for the rehoming of some species over others.

The rehoming process

Preparation of the animal

This section reports on qualitative (semi-structured questions) and quantitative (closed questions) findings from the survey. Selecting the most suitable animals for rehoming was deemed an important and thorough process by the participants, commonly undertaken following facility-wide rehoming policy (14 of the 19 facilities that rehomed followed their own rehoming policy). The survey revealed that various factors were considered to be significant when assessing the suitability of an animal for rehoming. These included the animal’s health, their age, breed, species and temperament, as well as the procedures they had undergone which would dictate their long-term health. Table 2 (below) provides a frequency count of these aspects as referenced across all participants.

Table 2. Animal suitability for rehoming frequency count (n = 19).
Factors to consider as raised by participants Number of times referenced
Health 14
Temperament 8
Age 3
Breed 1
Species 1

The majority of respondents (14 of the 19 facilities that rehomed) referenced the importance of the Named Veterinary Surgeon (NVS) and relevant heath checks in this process, who is typically in charge of judging and enabling a comprehensive assessment of overall welfare and quality of life post-rehoming. The responses collected suggest that the most important factor to consider is the health of the animal, and if that cannot be guaranteed, then rehoming should not be attempted. As one respondent, a Named Information Officer at a facility that kept amphibians, birds and rodents, wrote: the “NVS and the NACWO must confirm that the condition of the animal and its health allows for rehoming.

In terms of preparation for rehoming, larger mammal species typically required greater effort from laboratory staff (in terms of time and resources) to rehome. This commonly included establishing and completing comprehensive and effective socialisation and training schemes, ensuring exposure to new environments, and undertaking necessary medical procedures (such as neutering). All four stages of preparation were noted to be necessary both for rodents, and for cats and dogs. These were not considered necessary with livestock (only socialisation deemed appropriate) and no preparation was required for the rehoming of fish and amphibians. Despite the fact it would seem that rehoming larger mammals required greater effort in terms of time and cost, this does not appear to hinder efforts to rehome them, and rehomed numbers are still much higher in these species.

Finding the right home

The majority of animals were rehomed to staff, or their friends and family (18 facilities out of the 19 that rehomed employed this pathway to find homes). This route was more commonly sought out when rehoming smaller numbers of rodents. Rehoming this way was beneficial in that owner preparation was unnecessary as those rehoming the animals were facility employees (commonly animal technicians) who already had experience with the species in question. Eight facilities used word of mouth to find homes, suggesting there is an acceptance of rehoming to the public, but that this is not generally advertised openly. Two facilities transferred their animals to third party rehoming organisations that undertook the rehoming process on their behalf, signifying that effective partnerships can be forged between facilities and rehoming organisations. Rehoming did not necessarily entail rehoming to private family homes; homes were also found in bird breeders, animal sanctuaries, schools, farms, and petting zoos.

Evaluating owner capability was judged very important in the rehoming process– 16 of the 19 facilities that rehomed required the prospective owner to meet certain criteria. An evaluation of owner capability is also important in animal shelters; owner questionnaires, interviews with shelter staff, and home visits to establish levels of knowledge regarding pet behaviour and physiology are recommended [30, 31]. This is important as owner lifestyle and circumstances greatly affects the quality of life of companion animals [32, 33]. In this research, much emphasis was placed not only on finding a home, but also on ensuring it was the ‘right’ home for the animal. This form of matching is not specific to laboratory animals; literature in the animal shelter context finds it equally important [34]. Criteria included that the prospective owner must be able to demonstrate that they have previous species experience, suitable housing, and handling ability (Table 3). In addition to this, and mainly for species such as horses, cats and dogs, the NVS may visit/inspect the proposed home to ensure its suitability. The potential new owner may have to complete a questionnaire (two facilities required this of new owners), which includes questions investigating the motivations to rehome the animal, previous experience of owning an animal of the same species, as well as an enquiry into the personal situation (other animals or children in the home, rural/urban environment, current employment).

Table 3. Owner criteria frequency count (n = 19).
Factors to consider as raised by participants Number of times referenced
Prior species experience 11
Suitable housing 3
Owner questionnaire completion 2
Home inspection 2
Demonstrate handling ability 1

As well as having selection criteria, once the new owner had been identified questionnaire responses suggested that preparing the new owner was also important (12 facilities out of the 19 that rehomed undertook some form of owner preparation). This preparation was wide ranging (Table 4), and included that contact with the NVS should be sought if any medical issues arise in the future. Some facilities noted that the owner is provided with appropriate housing and initial food for the rehomed animal(s). For example, the manager of one facility explained how “The animals are always released with items from their home cages and some diet. We inform the new owners it will take them quite a while to acclimatise and for the initial few days just to place their hands in the cage and let the animals come to them. Some offered what the NACWO of one facility (which kept a variety of species including horses and beagles) termed a “going home pack” which included a bag of the current diet, treats and a vaccination record. One facility mentioned the importance of ensuring the owner is made fully aware of their responsibility for animal wellbeing, and their legal responsibility as a pet owner. As the participant explained, new owners are “asked to sign a document to confirm they will be responsible for the care and health of the animal(s) and seek veterinary attention should it be required”. This suggests that facilities are aware of the risks in rehoming in terms of liability, and have policy to ensure that owners are legally responsible for their new pet and that transfer of ownership is properly enacted. Three facilities explained that new owners are invited to the facility to view and potentially interact with the animal before rehoming, although again it should be noted that this was mainly for larger companion species such as horses, dogs and cats. In contrast to animal research facilities, which are typically inaccessible to the public, animal shelters tend to welcome visitors, where research finds social interaction to be influential in whether animal are chosen for rehoming [35, 36].

Table 4. Owner preparation frequency count (n = 19).
Factors to consider as raised by participants Number of times referenced
Rehoming packs 7
NVS support 5
Prospective owners invited into facility 3
Socialisation advice 2
Legal responsibility 1

Existing research suggests finding the right sanctuary and environment for the laboratory animal post-rehoming is critical [7, 37]. Further, people who take their newly adopted animal companion to a veterinarian early on are more likely to keep the animal for life [38]—so early and maintained contact with the NVS, which many facilities made an integral part of the rehoming process, is likely to be beneficial.

Another possibility is to rehome the animal with the help of a rehoming organisation (two facilities completing the survey collaborated with external rehoming organisations). This offers advantages; the organisation finds and vets the new owners, provides them with necessary information and remains available as a point of contact. Using such an organisation can be “safe and anonymous” (pg. 2) for the research institution [9]. Indeed, many facilities have already formed good working relationships with such organisations [9]. However, some of those that work at rehoming organisations are volunteers—and literature notes that these volunteers are not always taught the required skills to adequately train and socialise animals [39] In fact, only 12% of animal shelter employees across the United States rated volunteers as well trained “to a great extent” [40]. Research also finds an irregular schedule of social contact with animals from volunteers and frequent changes in active volunteers [41, 42].

From the findings, it is possible to outline the ‘typical’ 5-stage rehoming process (Fig 2). Participant responses suggested rehoming schemes are catered to the individual animal, and so do divert in some ways from this broad framework. For example, rodents were commonly rehomed with housing, and companion species such as dogs and cats were more likely to be rehomed through third party rehoming organisations, and only after an NVS home visit. However, this diagram broadly conveys the consistent themes that feature in the rehoming process.

Fig 2. The 5-stage rehoming process as understood by those UK facilities currently engaging in rehoming.

Fig 2

This flowchart provides an overview of all potential rehoming processes and policies, and not all will be relevant for all research animals.

The typical 5-stage rehoming process

Difficulties encountered by those facilities rehoming

The majority (58%) of facilities that had rehomed from 2015–2017 reported that they encountered no problems (Fig 3). However, eight facilities that had rehomed stated that the process was time consuming; one NVS suggested there was a “delay in Home Office approval”, whilst another facility director suggested there was an extensive “level of documentation required”. This implies that rehoming is generally considered easy to undertake, but can be time consuming due to the need to navigate complex regulatory boundaries in order to sign the animal off from A(SP)A regulation. Conversely, it is worth noting that very few facilities suggested rehoming was a costly process (2 facilities), that there was difficulty finding homes (1 facility), networking with relevant organisations (1 facility) or that rehoming attracted negative media attention (1 facility).

Fig 3. Graphs which show 1) the main difficulties experienced by UK research facilities that completed the questionnaire that have rehomed in the past 3 years (n = 19), 2) reasons cited by UK research facilities that completed the questionnaire for not engaging in rehoming in the past 3 years (n = 22), and 3) the perceived opportunities presented by rehoming as understood by all UK research facilities that completed the questionnaire (n = 41).

Fig 3

Resources needed to rehome

As there is an understanding that in order for rehoming to be successful it must be considered carefully and planned thoroughly [43], it is inherently resource intensive for the facility. In the survey, those facilities that had rehomed suggested the main difficulty experienced was that the process was time consuming. Research acknowledges that animals should be spayed prior to rehoming, and that if this is not standard procedure, it can be time-intensive in terms of set up, surgery and aftercare [9]. Working through a third-party rehoming organisation can help to counteract this as the organisation can undertake any medical attention needed, as well as the sourcing and screening of prospective owners. Interestingly, the longer time investment involved in the rehoming of larger animals typically kept as pets (dogs and cats) did not deter efforts to rehome, as these animals were more likely to be considered for rehoming (Table 1). Research recommends that the resources needed to successfully rehome should not be a deterrent and that it should still be “recommended for the sake of the dogs” (pg. 24) [19].

Opportunities presented by rehoming

The majority of facilities completing the questionnaire (58%) reflected that rehoming was “good for staff morale” (24 facilities). A similarly high number (23 facilities) believed it showed a positive ethical stance. The expectation of future well-being of animals played a significant, but slightly lesser role (19 facilities), while 13 facilities felt rehoming offered no opportunities (Fig 3). Interestingly, but perhaps unsurprisingly, those facilities not currently engaging in rehoming did not reflect that the process could benefit them. Conversely, those that had engaged in rehoming in the previous 3 years were more likely to suggest it contributed positively to animal welfare, staff morale and demonstrated a positive ethical stance.

Existing research reports that rehoming can benefit animal welfare, allowing a dignified and deserved retirement [44]. Rehoming helps to ‘uphold scientist’s ethical responsibilities’ [18]. Rehoming also has important ramifications for the wider facility and can help to develop and foster a “culture of care” and staff wellbeing [7, 43], as echoed in the questionnaire results (Fig 3). Staff morale may be improved further if the staff member is able to rehome the animals themselves, which the survey reflected was fairly common; 18 facilities rehomed their animals to staff members. Routine killing is emotionally challenging and stressful for facility staff [45], so any opportunity to allow animals to have a life outside of the laboratory will benefit employees, most of whom care deeply about the animals with which they work [46]. There thus exists a two-way process, whereby it is positive for staff to 1) circumvent the emotional stress of unnecessary killing (avoidance of negative states), and 2) provide the animal with an increased quality of life once rehomed (promotion of positive states). However, there are challenges that come with rehoming to staff—an NVS explained how the rodents could not be rehomed to employees as staff might “acquire rodents from other sources” that are “microbiologically dirty […] which could present a risk of inadvertent delivery of disease”. Microbiological contamination is thus considered a risk, and therefore some facility staff cannot keep rodents as pets, including those from the laboratory.

Reasons facilities are not currently engaged in rehoming

Amongst those facilities that had not rehomed in the previous 3 years, eight reported that the reason was concern for the animal’s health if it were to be rehomed. Eight stated that high demand means few are left to retire. Slightly fewer numbers felt rehoming would be too stressful for the animal (4 facilities), that it was difficult to predict long-term health implications (4 facilities) or that rehoming would result in a loss of control (4 facilities). Fear of unwanted or negative media attention (2 facilities), convenience (one facility) and being unaware that rehoming is possible (one facility) were rarely selected as reasons not to rehome (Fig 3). Reasons for not rehoming can thus be grouped into welfare concerns with regard to the animal’s health if rehomed, practical issues surrounding demand and the fact that research needs’ tend to leave few animals to retire, and external challenges including fear of negative media attention.

As well as the challenges recognised above (Fig 3), utilising the open answer box, participants articulated additional reasons for their lack of engagement in rehoming. These included that; 1) rehoming is impossible for some GA animals due to its illegal nature following A(SP)A policy [1] (if GA animals are rehomed, the environment and other animals may be exposed to infectious agents and consequently rehoming could have severe negative impacts that extend beyond the boundaries of the laboratory), 2) three facilities explained that they had never been approached to rehome, and therefore a lack of demand for rehoming was cited as a barrier, and finally 3) animals were not considered for rehoming at some facilities because of the research undertaken, much of which was of a terminal nature due to the tissues required. As one participant, an NACWO at an amphibian and rodent facility, explained, the “vast majority of projects involve terminal or non-recovery final procedures.” The survey responses thus reflect a conflict between the demands of the research and any possibility of rehoming.

Biosecurity

Despite it being scientifically unclear exactly how some GA animals might pose a biosecurity risk, the rehoming of GA animals was considered illegal by some who responded to the survey. One participant, a Director at a rodent facility, explained how their genetically altered rodents are “not permitted for rehoming”. Many UK facilities house genetically modified animals, and this number is increasing [2426]. The Home Office advice note on rehoming states that an animal should only be rehomed if it will not harm the environment, other animals, itself or people [1], but participants acknowledged the difficulties in guaranteeing this when rehoming genetically modified laboratory animals. As one participant, an AWERB Chair at a fish and rodent facility explained, “We are working almost exclusively with infectious pathogens so rehoming cannot be achieved from a human safety point of view”. Another, the AWERB chair at a rodent, fish and pig facility, discussed the “associated risks” involved with rehoming GA animals used in “infectious work”. Thus, health risks from exposure to animals outside of the laboratory limits rehoming practice. A case study of GA pig rehoming discusses how ‘EnviroPigs’ were not rehomed for fear of potential environmental and food safety risks, making transfer to a farm sanctuary irresponsible [27]. Indeed, there is uncertainty around allowing transgenic animals to be retired [9], as well as complex legal liability issues should animals escape [27]. Research advises that no genetically modified livestock be rehomed and enter the food chain [9]. It is also suggested that genetically modified animals should not be adopted, importantly whether they are neutered or intact, to any member of the public [9].

Perceptions of risk

Linking to this are issues of liability, risk and reputation for the research facility. Participants noted the importance of the legal transfer of ownership when rehoming—implying there exists a perceived risk for the facility otherwise. One participant, a NACWO, explained in response to an open answer in the questionnaire survey, “The new owner is made fully aware of their responsibility for the pony’s health and well-being. They are also made aware of their legal responsibility to change ownership details on the passport”. Ultimately, facilities cannot control how the rehoming process may reflect on them and their reputation [9]. This is also reflected in two facilities citing negative media attention as a barrier to rehoming (Fig 3). Research finds a major deterrent to rehoming is that sanctuaries/members of the public could discuss abnormal animal behaviour/physiology with the media and thus the facility be presented in a negative light [47]. This could result in them being unlikely to rehome again. To combat this, there is potential to introduce confidentiality agreements regarding the origins of the animal before considering rehoming [47].

Animal welfare concerns

Although also acting as a motivation to rehome, perceived future animal welfare also represented a barrier in terms of loss of control and potential reduced standards of care. There were worries regarding ensuring animal welfare once the animal had left the facility—one participant, a NACWO at a fish and rodent facility, explained how it was “too difficult to monitor animal welfare after re-homing has occurred”. There were also more specific concerns over the conditions in which animals will be kept; one participant, a manager at a mouse facility, outlined that the animals at their facility required “high standards of care not readily available”. Worries regarding the animals’ life post-rehoming are justified; there exists a high turnover rate of companion animals, and owners may lose interest and get rid of the animal [9]. Previous research has also outlined worries regarding rehoming psychologically distressed monkeys, who may not adapt well to a new environment [7]. The transportation of animals, especially primates who possess significant mental capacities [48], can also be very stressful [49]. Ultimately, participants eluded that the ethical legislation that exists in facilities does not extend to private homes/sanctuaries, and there were hence worries regarding ensuring animals were provided with a life worth living post-rehoming.

Study limitations

It should be noted that the collected responses may represent a selection bias, as those who rehome more regularly may also have been more likely to complete the survey. As it is a controversial issue, there may have been a social desirability bias in response to more subjective questions. Additionally, although over 25% of facilities in the UK completed the questionnaire, this remains a sub sample of the total population. Thus, caution should be exercised when attempting to generalise results to all UK research facilities. Finally, an extrapolation was made from 2017 Home Office data to the years 2015 and 2016 to calculate an approximate number of surplus animals across the 3 years. However, there is likely to be some variance in the proportions of surplus animals by species year by year that is not accounted for in this research.

Future research

Although this research demonstrates that some species are preferred over others for rehoming, future research should seek to understand the mechanisms by which this occurs. This is necessary to understand why particular animals are chosen for rehoming, and may promote the rehoming of animals not typically considered. Work should also be undertaken to evaluate the success of rehoming schemes with species including rodents and fish, not simply larger animals traditionally kept as pets or primates as has been undertaken previously. Despite the clear impossibility of finding homes for all of the rodents and fish currently kept in UK facilities, there would be merit in understanding the drivers and processes of rehoming even small numbers of these species. This would help to encourage and support facilities with species such as rats and mice in their efforts to rehome, as well as guiding them in developing relevant and useful facility-wide policy.

Conclusion

This research has demonstrated that rehoming occurs in just under 50% of the UK research facilities that participated in the study, but is usually in very small numbers (just 2322 animals are known to have been rehomed from 2015–2017). There exists a clear species preference for rehoming, whereby traditional companion animals (cats, dogs and horses) are more commonly considered. Rehoming appears to occur through two pathways: 1) in small numbers of rodents (typically gerbils, rats, guinea pigs and rabbits) rehomed to staff and their families and friends, and 2) in larger numbers of traditional companion animals through extensive public rehoming schemes. The main motivation for doing so is to boost staff morale and demonstrate a positive ethical profile. Expectation of future well-being of the animal also played a slightly lesser, but still noteworthy and connected role. These benefits were not realised by those facilities not engaging in rehoming.

The most significant barrier is the time taken to rehome, yet generally most facilities that rehomed in the previous 3 years found the process to be easy and few experienced substantial difficulties. This may be because the survey revealed that rehoming is generally a very well-planned process, with 14 out of the 19 facilities that had rehomed in the 2015–2017 period employing facility-wide rehoming policy which included choosing the appropriate animals, socialisation and training, and owner selection and preparation. This importantly differed through its tailoring to the animal in question.

The main reasons for choosing not to rehome include concern for the animal’s health if it were to be rehomed, high demand for research animals, and animals in the facility being unsuitable for rehoming (participants explained this was primarily genetically modified fish and mice).

The questionnaire revealed that rehoming is a known and considered pathway for laboratory animals, but is undertaken in relatively small numbers. Despite rehoming occurring in low numbers, the practice was interpreted by facilities that rehomed to be good for animal welfare, the staff and the wider facility, and as such should be considered where possible.

As part of a movement to enhance animal welfare and introduce measures which promote a ‘life worth living’ through the attainment of positive states in animals, rehoming from UK animal research facilities finds a place. Rehoming helps to support staff in overcoming issues related to moral stress, as well as address public concern regarding the current routine nature of animal killing in the laboratory. In order to promote the practice, it is imperative to enhance current understandings regarding both which facilities are participating in the practice, and how they do it, in order to disseminate the information to institutions not currently active in this area.

Supporting information

S1 Appendix

(DOCX)

Acknowledgments

We thank all participants for their generous time contribution, and to the reviewers for their valuable comments.

Data Availability

There are ethical restrictions on sharing the data gathered from the questionnaire. Data cannot be shared resulting from the impossibility of fully anonymising questionnaire results. To allow access to the data through sharing is in direct contradiction to the ethical agreement signed by participants, and approved by the University of Southampton’s ethical committee. The University of Southampton’s ethical committee (Head of Research Governance) can be contacted at: rgoinfo@soton.ac.uk.

Funding Statement

T.S and E.R 205393/D/16/Z Wellcome Trust https://wellcome.ac.uk/ The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Decision Letter 0

I Anna S Olsson

23 Jan 2020

PONE-D-20-01484

A quantitative investigation into the occurrence and processes of laboratory animal rehoming from UK animal research facilities

PLOS ONE

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PLoS One. 2020 Jun 19;15(6):e0234922. doi: 10.1371/journal.pone.0234922.r002

Author response to Decision Letter 0


17 Feb 2020

Additional revision:

1. Thank you for useful considerations regarding data restrictions. Unfortunately, I cannot share the data for ethical reasons as consent was on the basis that the information gathered from participants would not be shared beyond the authors of this paper. I proceeded in this way as it is difficult to fully anonymise data in a small field. I hope this provides a satisfactory explanation. Thank you again for your comments.

Attachment

Submitted filename: Response to reviewers.docx

Decision Letter 1

I Anna S Olsson

14 Apr 2020

PONE-D-20-01484R1

A semi-structured questionnaire survey of laboratory animal rehoming practice across 41 UK animal research facilities

PLOS ONE

Dear Ms Skidmore,

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Reviewer #2: No

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Reviewer #2: No

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Reviewer #1: The study has an important topic: The authors carried out a survey on the rehoming practice of 41 research facilities in the UK to find answers for the following questions: How often are animals rehomed, what attitudes exist in the facilities about this topic and which reasons prevent institutions from rehoming their laboratory animals.

I propose a major revision because the authors should present their results in a more comprehensive manner.

• Please present all results of your questionnaire in the manuscript. I miss specific data, for example: How many animals of which species are kept in the 41 facilities that answered? How many animals of which species they rehomed trough which pathway (staff, third party organization)? How often have animals been given to schools, farms etc.? In the chapter “The rehoming process” (lines 349-419) I miss specific data to follow up on the statements. Example: Line 359: “The majority of respondents…” - what number exactly?

The presentation of results is more comprehensible in the chapters in lines 431-504 (chapters “Difficulties encountered…” to ”Reasons facilities are not… ”).

• In my opinion it is misleading to present the number of the rehomed animals as a percentage of all animals kept in the UK. Please place the number of the rehomed animals in relation to the animals kept in the 41 facilities that responded.

• In the method chapter (for example lines 239-241) and in the results section the authors already included discussion aspects. Please separate these areas. PLOS One allows a combination of results and discussion, but this should be shown in the heading accordingly.

Further comments:

• Please include more data in the abstract.

• Please include the legal requirements in the UK into the introduction. Directive 2010/63/EU makes specific statements on what to do with animals at the end of procedures and on the rehoming of animals.

• Please explain abbreviations when you use them for the first time (e.g. GA in line 216)

• You can delete the sentence in lines 339-340 “The next section…”

• Please add the n-numbers to the figure captions for figures 7 and 8 (n = 22 facilities without rehoming…)

• I do not understand why the figures are referred to here: line 374 for figure 4 and line 541 for figure 8?

• Figure 1 is unnecessary as this information is expressed in figure 2.

• Table 2 contains very little information and is unnecessary since you can also insert the missing numbers in the text.

• How did you calculate the numbers in figure 4? Birds 36.65%?

• Line 344 and line 656: Rabbits and ferrets are not rodents! Replace with “small mammals”.

• In the illustrations, the font is sometimes too small and difficult to read, e.g. in figures 6 and 7.

• Discussion lines 644 ff. Do you have an idea how to find a new home for millions of fish, rats and mice? Is that realistic? Please discuss.

Reviewer #2: This paper aims to assess how many facilities in the UK rehome former research animals, which species, which numbers, for which reasons and by which process. The authors also look at barriers to rehoming. In itself, this is a very relevant and interesting theme to explore, as there are insufficient data to support the practical implementation of the rehoming stipulations in legislation.

However, I have some major concerns with this paper In summary, some parts of the paper lack focus (introduction, discussion), there is an issue with confusing the concepts of animal welfare and ethics in discussing arguments for rehoming, I have doubts about the way the numerical data are presented (known percentage of rehomed animals), the paper lacks critical use of references (there are references to books that are implicitly referred to as results from scientific research, which they aren’t) and the text as a whole does not read fluently. I lost track of the flow several times and had to go back and re-read.

I will begin with providing detailed comments on my major concerns.

ABSTRACT

The data about rehomed versus kept are misleading. See comment regarding major concern about the analysis.

INTRODUCTION

- I do not agree with the authors approach to refute "death of an animal does not constitute a welfare matter". The authors seem to confuse the concepts of animal welfare and animal ethics. Animal Welfare concerns the situation of the animal as the animal perceives it. In that respect, the fact that an animal dies is not an animal welfare matter, as we have no indication that animals are conscious of any future time that is lost by their death. HOW the dies (i.e. how much suffering does the concept induce) is an animal welfare matter. Animal ethics, on the contrary, is how we humans think animals should be treated. In that respect, giving an animal " a life worth living" after retirement from the research facility is an ethical matter, in which animal welfare aspects have to be taken into account. The authors should rethink their line of reasoning.

- The introduction lacks focus and is unbalanced, being very one-sided towards an obligation to rehome. This should be more balanced for a scientific paper in my view. I would propose to structure the introduction to make it very concise and clean, including: what is rehoming, what are animal welfare benefits and risks, what are ethical arguments for or against rehoming (if that is indeed something they will get back to based on the survey responses; if not, I think the authors should consider to stay away from philosophical/moral discussions).

METHODOLOGY

My one issue with the methodology is how the authors choose to calculate the known percentage of rehomed animals. The current way to calculate this (numbers rehomed across 41 facilities compared to all UK unused non-GA + first time procedure animals) provides a huge underestimation. The authors do state twice in the paper that they calculate the “minimum percentage” and yet, in the rest of the manuscript, they treat it as if it is the maximum. A more correct calculation would have been to use numbers of rehomed animals in relation to number of kept animals for the 41 facilities. As I look at the questionnaire, however, I see that the authors only have information about “animals kept at this time”, for which I don’t know which period this is. The only somewhat correct way to present the data then, would a comparison between species, using the proportion of each species that is being rehomed (based on 41 facilities) and proportion of each species as they are used throughout the UK, as an indication of the disproportion, but without comparing numbers kept to numbers rehomed.

RESULTS

Following my major concern in the methodology, the results section needs to be re-worked.

DISCUSSION

The discussion does not read easily, I think in part because a clear structure is generally lacking. It is difficult to see whether the authors use the same order as the one that was used to present the results, or whether they refer back to the research questions and deal with them in sequence. Perhaps a few subtitles could help.

Some elements of the discussion do not appear in the results section. For example Lines 532-533: the view of the respondents about which species are ‘unrehomeable’ was not asked directly of the particpants. This may have come out in the open questions, but then the results from a structured analysis on this must be presented in the results section. Another one is on line 546: biosecurity. This is the only time in the entire manuscript that biosecurity is mentioned as a significant barrier. This must be presented in the results section first.

I would not use single quotes to support statements if you have not presented a structured analysis of open questions in the results section. This makes the study look extremely subjective and anecdotal.

CONCLUSION

The conclusion is actually quite concise and clear. But its contents needs to be modified to reflect the requested changes.

Next, there are also some minor concerns.

ABSTRACT

Lines 30-32: the sentence "this paper reports on research findings that explain..." is too strong. The findings do not explain anything, they merely provide an indication.

Line 36 and beyond: the abstract should at least mention the number of facilities that participated and the response rate.

Line 36-37: This needs to be adapted to respond to my major comment in methodology section about the analysis

INTRODUCTION

Line 58: “The practice supports the notion that…”. I do not agree with “supports”. The practice of rehoming is guided by the notion that animals are sentient beings etc.

Lines 69-70: these arguments are worded too strong. They may be possible, but certainly not true for all cases. Please re-word.

Line 78-79: again too strong. In veterinary practice, euthanasia is also frowned upon many times. And routine euthanasia (which can happen e.g. in an overcrowded shelter) is never regarded as favourable.

Line 91 and beyond: I am concerned about the authors’ understanding of the concept of animal welfare, because of the references they use in this section. The fact that they refer to a philosophical paper to define animal welfare concerns me. There are good papers by animal welfare scientists, which should be preferred as a source. See for example: Broom 2011, Acta Biother, 59:121-137 or Weary and Robbins 2019, Anim Welf, 28:33-40.

Line 130-142: I find this paragraph confusing. The authors could elaborate a bit on the results from the outcome studies, to indicate good practices in rehoming already.

Line 133: “The overwhelming focus on these species is limiting”: I do not understand what the authors are trying to say.

Line 134-137: The references 5 and 20 are books. Very unlikely that these report original research. Can primary sources be used? Or are the authors of the books referring to anecdotal evidence? This needs to be made more clear, because the authors state “as research points out…”, so the supporting references should be research papers.

Line 148: “This is necessary to enhance animal welfare”: I find this quite a vague statement and would like to know what the authors mean. Is it about enhancing animal welfare by rehoming, or enhancing animal welfare by rehoming correctly (using proper procedures, which can help guarantee the welfare of the animals after rehoming, as demanded by law)?

METHODOLOGY

The methods section needs to mention when the survey was administered (months & year).

Line 178 and 242: “the university of XXXXX” – I assume the authors have blinded the university, but since this is not a blinded review, that is not necessary.

Line 179: “spilt” should be “split”

Line 192: AWERB should appear in full the first time it is used

Lines 192-195: this information should be presented at the beginning of the results section

Line 216 and 496 (for example): sometimes GA is used and sometimes GM, while I think the authors mean the same

Line 218: No need for this long sentence, just use the term that was introduced before: surplus animals

Lines 207-235: The data processing section is too long and fragmented. Also, crucial information is missing. Please create one or two paragraphs with data processing information, concisely reporting how the responses to the questions were processed (how were closed questions processed, what about open questions – was thematic analysis used?), which variables were calculated, why and how….

RESULTS

Lines 259-261: this is a bold statement that is insufficiently supported by the data that are presented. How does the variety in the survey relate to the variety in all other facilities?

Figure 1: I would delete figure 1. There is no added value there, as the numbers are already in the text.

Line 278-280: I find this an odd statement, given that, equally, it is very possible institutions that do not rehome did not complete the survey. Also, does this mean that incomplete surveys were not counted? This needs to be stated in the data processing part of the Methodology section.

Line 289: “If we assume that the ratio above extends” – to what?

Line 291: This is an example of how minimum percentage is not used throughout. Because it is a minimum, you can only state that “at least 0.02% of laboratory animals are known to be rehomed from 2015-2017”, but again, this figure to me is really misleading as it is a huge underestimation.

Line 300: keep in mind that primates may not be rehomed in the UK sense of the word, but they may be retired from research, while still living at the facility.

Table 1: again, misleading due to the “known percentage rehomed” calculation. Similar comment for the last column with the ration.

Figure 4: The left pie chart is difficult to read. I would turn this figure into a table comparing proportions of animals rehomed (41 institutions) and animals kept (UK total). This, in my opinion is the only valid numerical comparison that could be made (see my major concern about the calculation of “known percentage rehomed”).

Lines 349 and beyond: the presentation of results is very qualitative as it almost looks at individual responses from respondents. I feel a more structured analysis, like a thematic analysis with a frequency count, is appropriate.

Lines 487-489: The grouping of reasons for not rehoming does not adequately capture the responses. E.g. Fear of unwanted or negative media attention is not a practical issue. Please re-consider this.

DISCUSSION

Lines 526-527: “this is also demonstrated by only one facility of the 41 facilities”: it is not clear what is demonstrated

Line 545 and beyond: the authors seem to suggest that all GM models pose a biosecurity risk, which is not true.

Line 585: “this effect” – which effect? Please state clearly to what you are referring.

**********

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Reviewer #1: No

Reviewer #2: No

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PLoS One. 2020 Jun 19;15(6):e0234922. doi: 10.1371/journal.pone.0234922.r004

Author response to Decision Letter 1


7 May 2020

Thank you for your very helpful comments on the first draft of this paper. I have responded to them below.

Reviewer 1:

• Please present all results of your questionnaire in the manuscript. I miss specific data, for example: How many animals of which species are kept in the 41 facilities that answered? How many animals of which species they rehomed trough which pathway (staff, third party organization)? How often have animals been given to schools, farms etc.? Thank you for this contribution. Unfortunately, however, we cannot provide this information from the data collected. The data we have does not break down the different pathways used to rehome to an individual/species level. We only have data for the numbers of facilities that use different pathways to rehome. In the chapter “The rehoming process” (lines 349-419) I miss specific data to follow up on the statements. Example: Line 359: “The majority of respondents…” - what number exactly? This has now been changed in accordance with comments – we have added in the specific number of respondents. On reviewer 2’s suggestion, this has also been supplemented with a frequency count of particular themes arising from the qualitative open answer responses.

The presentation of results is more comprehensible in the chapters in lines 431-504 (chapters “Difficulties encountered…” to ”Reasons facilities are not… ”). Thank you, this has been noted.

• In my opinion it is misleading to present the number of the rehomed animals as a percentage of all animals kept in the UK. Please place the number of the rehomed animals in relation to the animals kept in the 41 facilities that responded. Unfortunately, we cannot place the number of animals rehomed in relation to the number of animals kept across the 41 facilities across the 3 years because the data we have is only for animals kept in the 41 facilities at that time. Thus, and in keeping with reviewer 2’s comments, we have removed the suggestion that the number of rehomed animals is a percentage of all animals kept, and instead presented the different data to allow a visual comparison (see tables 1 and 2).

• In the method chapter (for example lines 239-241) and in the results section the authors already included discussion aspects. Please separate these areas. PLOS One allows a combination of results and discussion, but this should be shown in the heading accordingly. Thank you for this advice, the results and the discussion sections have now been combined, and the headings adjusted accordingly.

Further comments:

• Please include more data in the abstract. We have now added in information regarding number of facilities that completed the survey and the response rate, number of animals known to be rehomed (2322 animals), and a species breakdown of numbers rehomed: “although 94.15% of species kept in laboratories are rodents, they make up under a fifth (19.14%) of all animals known to be rehomed between 2015-2017.”

• Please include the legal requirements in the UK into the introduction. Directive 2010/63/EU makes specific statements on what to do with animals at the end of procedures and on the rehoming of animals. Thank you, this is a very useful suggestion. The legal requirements regarding rehoming as laid out in Directive 2010/63/EU have now been added to the introduction.

• Please explain abbreviations when you use them for the first time (e.g. GA in line 216). Now corrected this by explaining the abbreviation.

• You can delete the sentence in lines 339-340 “The next section…” Thank you, this line has now been deleted.

• Please add the n-numbers to the figure captions for figures 7 and 8 (n = 22 facilities without rehoming…) We have updated figure captions to reflect the number included in the figure.

• I do not understand why the figures are referred to here: line 374 for figure 4 and line 541 for figure 8? The reference to these figures have now been removed.

• Figure 1 is unnecessary as this information is expressed in figure 2. Thank you. Figure 1 has been removed in line with the recommendation of both reviewers 1 and 2

• Table 2 contains very little information and is unnecessary since you can also insert the missing numbers in the text. Now removed in line with reviewer’s recommendation.

• How did you calculate the numbers in figure 4? Birds 36.65%? A more detailed description of how we calculated the numbers has now been included in the figure caption for figure 4. It reads as follows “The left column shows the percentage of animal groups (such as small mammals, birds, agricultural animals) currently kept in all UK facilities. This data is based on Home Office annual statistics of animals used in research. The right column shows an equal breakdown of animal groups rehomed across the 41 facilities that completed the survey to allow a comparison”.

• Line 344 and line 656: Rabbits and ferrets are not rodents! Replace with “small mammals”. Thank you – this has now been changed to small mammals.

• In the illustrations, the font is sometimes too small and difficult to read, e.g. in figures 6 and 7. The font size has now been made larger in these figures to ensure it is more readable.

• Discussion lines 644 ff. Do you have an idea how to find a new home for millions of fish, rats and mice? Is that realistic? Please discuss. Thank you for this consideration. We feel it is not realistic to try to rehome all of these species. However, it is important that, because of this, research does not neglect these species. Instead, research should be undertaken into the rehoming of these species, as well as the current focus on large mammals (dogs, cats, primates). We have now added in “This does not mean rehoming all those fish and rodents currently kept in UK facilities, as given the numbers this would be unrealistic, but instead understanding why and how efforts are made to rehome even small numbers of these species”.

Reviewer 2:

This paper aims to assess how many facilities in the UK rehome former research animals, which species, which numbers, for which reasons and by which process. The authors also look at barriers to rehoming. In itself, this is a very relevant and interesting theme to explore, as there are insufficient data to support the practical implementation of the rehoming stipulations in legislation.

However, I have some major concerns with this paper In summary, some parts of the paper lack focus (introduction, discussion), there is an issue with confusing the concepts of animal welfare and ethics in discussing arguments for rehoming, I have doubts about the way the numerical data are presented (known percentage of rehomed animals), the paper lacks critical use of references (there are references to books that are implicitly referred to as results from scientific research, which they aren’t) and the text as a whole does not read fluently. I lost track of the flow several times and had to go back and re-read.

I will begin with providing detailed comments on my major concerns.

ABSTRACT

The data about rehomed versus kept are misleading. See comment regarding major concern about the analysis. This has now been updated and does not discuss data about rehomed v. kept.

INTRODUCTION

- I do not agree with the authors approach to refute "death of an animal does not constitute a welfare matter". The authors seem to confuse the concepts of animal welfare and animal ethics. Animal Welfare concerns the situation of the animal as the animal perceives it. In that respect, the fact that an animal dies is not an animal welfare matter, as we have no indication that animals are conscious of any future time that is lost by their death. HOW the dies (i.e. how much suffering does the concept induce) is an animal welfare matter. Animal ethics, on the contrary, is how we humans think animals should be treated. In that respect, giving an animal " a life worth living" after retirement from the research facility is an ethical matter, in which animal welfare aspects have to be taken into account. The authors should rethink their line of reasoning. The discussion of death not constituting a welfare issue has been removed, and instead effort has been made to explain how rehoming may both improve animal welfare when following regulatory guidance, but also potentially also compromise it.

- The introduction lacks focus and is unbalanced, being very one-sided towards an obligation to rehome. This should be more balanced for a scientific paper in my view. I would propose to structure the introduction to make it very concise and clean, including: what is rehoming, what are animal welfare benefits and risks, what are ethical arguments for or against rehoming (if that is indeed something they will get back to based on the survey responses; if not, I think the authors should consider to stay away from philosophical/moral discussions).Thank you for this useful suggestion. The moral and ethical arguments for considering rehoming have now been removed. In order to balance out our arguments, we have added a discussion of how rehoming can also negatively impact welfare: “Of course, it is also crucial to acknowledge that rehoming is not always in the best interests of the animal, and may instead only serve to compromise welfare. Current UK regulatory guidance, such as the Animals in Scientific Procedures Act, or A(SP)A, helps to ensure welfare is maintained in the laboratory, yet once rehomed this legislation is no longer in place to protect the animal in question. It is thus the facility’s responsibility to ensure that rehoming will in no way compromise welfare [22]. This must remain an absolute priority. Factors that can affect welfare during the rehoming process are the animal’s state of health, duration and condition of transport to new home, and the social and/or physical environment the animal will be moved to [8]. Research notes that potential compromises to welfare can be minimised or eradicated with careful and thorough planning of key processes such as transport [8] and socialisation [10, 22] to lower animal stress.”

METHODOLOGY

My one issue with the methodology is how the authors choose to calculate the known percentage of rehomed animals. The current way to calculate this (numbers rehomed across 41 facilities compared to all UK unused non-GA + first time procedure animals) provides a huge underestimation. The authors do state twice in the paper that they calculate the “minimum percentage” and yet, in the rest of the manuscript, they treat it as if it is the maximum. A more correct calculation would have been to use numbers of rehomed animals in relation to number of kept animals for the 41 facilities. As I look at the questionnaire, however, I see that the authors only have information about “animals kept at this time”, for which I don’t know which period this is. The only somewhat correct way to present the data then, would a comparison between species, using the proportion of each species that is being rehomed (based on 41 facilities) and proportion of each species as they are used throughout the UK, as an indication of the disproportion, but without comparing numbers kept to numbers rehomed. Calculating the percentage of animals rehomed as a percentage of Home Office figures has now been removed, and instead a visual comparison has been enabled through tables 1 and 2, which show the number of animals kept (in all UK research facilities between 2015-2017) and those rehomed (out of the 41 facilities that completed the questionnaire).

RESULTS

Following my major concern in the methodology, the results section needs to be re-worked. Thank you – the results section has now been updated to reflect changes in the analysis.

DISCUSSION

The discussion does not read easily, I think in part because a clear structure is generally lacking. It is difficult to see whether the authors use the same order as the one that was used to present the results, or whether they refer back to the research questions and deal with them in sequence. Perhaps a few subtitles could help. Thanks, this is a very useful suggestion. The results and conclusions sections have now been merged, and extra subtitles have been added to aid with a clearer structure.

Some elements of the discussion do not appear in the results section. For example Lines 532-533: the view of the respondents about which species are ‘unrehomeable’ was not asked directly of the participants. This may have come out in the open questions, but then the results from a structured analysis on this must be presented in the results section. Another one is on line 546: biosecurity. This is the only time in the entire manuscript that biosecurity is mentioned as a significant barrier. This must be presented in the results section first. Thank you for this useful advice. A structured analysis has now been provided in the results and discussion section, and it has been made clearer that biosecurity risks as a barrier have come from the open question responses.

I would not use single quotes to support statements if you have not presented a structured analysis of open questions in the results section. This makes the study look extremely subjective and anecdotal. We have now provided a structured analysis of the open questions, including a frequency count. We have consequently left in the single quotes to support statements, as the structured analysis will make their use more objective and scientific.

CONCLUSION

The conclusion is actually quite concise and clear. But its contents needs to be modified to reflect the requested changes. Thank you for your positive comments. The conclusion has now been updated in line with wider changes to the paper.

Next, there are also some minor concerns.

ABSTRACT

Lines 30-32: the sentence "this paper reports on research findings that explain..." is too strong. The findings do not explain anything, they merely provide an indication. I have adapted this as suggested to: “This paper reports on research findings that provide an indication of the uptake of animal rehoming by UK facilities...”

Line 36 and beyond: the abstract should at least mention the number of facilities that participated and the response rate. Thank you. These figures have now been included in the abstract, along with more figures in line with reviewer 1 comments.

Line 36-37: This needs to be adapted to respond to my major comment in methodology section about the analysis. The suggestion of a percentage of animals rehomed from the wider numbers kept in UK facilities has been removed.

INTRODUCTION

Line 58: “The practice supports the notion that…”. I do not agree with “supports”. The practice of rehoming is guided by the notion that animals are sentient beings etc. Thank you, this has been modified accordingly.

Lines 69-70: these arguments are worded too strong. They may be possible, but certainly not true for all cases. Please re-word. Re-worded to “Firstly, surplus animals have not been subject to research, and thus long-term health implications (often cited as a barrier to rehoming) are less likely to represent a risk [8]. Secondly, rehoming these animals typically presents a lower risk of disease transmission.”

Line 78-79: again too strong. In veterinary practice, euthanasia is also frowned upon many times. And routine euthanasia (which can happen e.g. in an overcrowded shelter) is never regarded as favourable. Thank you for this thoughtful consideration. This has now been changed to “Euthanasia may have more positive connotations in the veterinary clinic setting when companion animals are relieved of suffering, but in the animal laboratory, issues with routine euthanasia are compounded within a setting where animals are systemically harmed for human benefit.”

Line 91 and beyond: I am concerned about the authors’ understanding of the concept of animal welfare, because of the references they use in this section. The fact that they refer to a philosophical paper to define animal welfare concerns me. There are good papers by animal welfare scientists, which should be preferred as a source. See for example: Broom 2011, Acta Biother, 59:121-137 or Weary and Robbins 2019, Anim Welf, 28:33-40. An updated definition of animal welfare has been included, based on Weary and Robbins (2019) – “Animal welfare typically includes a consideration of animal’s affective state (pain), biological functioning (injuries) and sometimes also a consideration of naturalness (such as pasture access).” The definition of animal welfare from a philosophical paper has been removed.

Line 130-142: I find this paragraph confusing. The authors could elaborate a bit on the results from the outcome studies, to indicate good practices in rehoming already. Thanks, this is a good suggestion. We have now also added data on the success of current rehoming schemes – “Research showed beagles have a high adaptive capacity, fit in well with families and thus make good companion animals [25]. Within 6-12 weeks of rehoming, behaviour tests on the dogs reflected relaxed body language, as well as reduced heart rates, signifying calm behaviour once settled in the home environment [25]. Research also found cats were successfully rehomed from a research facility, with a retention rate of 93.5% [23]. Of those rehomed, 80.4% were considered a valued family member, and behavioural problems were reported in just 11.3% of the cats within 6 months of adoption [23]. Research revealed that Cornell University developed a successful direct adoption scheme, and that the University of California, San Francisco employs an indirect scheme, whereby animals are transported to a third party shelter before rehoming [10]. Both schemes were judged to be successful, with “hundreds” of animals placed in adoptive homes [10]. These case studies convey hope that rehoming as a practice could be successfully institutionalised and adapted to specific facility needs, across a range of sentient species.”

Line 133: “The overwhelming focus on these species is limiting”: I do not understand what the authors are trying to say. We understand the confusion - the sentence has been adapted to be clearer – “However, the overwhelming focus on these species does not provide a comprehensive understanding of all rehoming practice across species”

Line 134-137: The references 5 and 20 are books. Very unlikely that these report original research. Can primary sources be used? Or are the authors of the books referring to anecdotal evidence? This needs to be made more clear, because the authors state “as research points out…”, so the supporting references should be research papers. Thank you for pointing this out. We have removed as ‘research points out’, as the authors of the book are referring to anecdotal evidence. However, we cannot find any primary sources of research that can be used in this context.

Line 148: “This is necessary to enhance animal welfare”: I find this quite a vague statement and would like to know what the authors mean. Is it about enhancing animal welfare by rehoming, or enhancing animal welfare by rehoming correctly (using proper procedures, which can help guarantee the welfare of the animals after rehoming, as demanded by law)? This has now been updated to reflect reviewer’s concerns to “This is necessary to enhance animal welfare by following correct rehoming procedures which can help to ensure animal welfare after rehoming, as stipulated by law, and promote the rehoming of laboratory animals where viable”

METHODOLOGY

The methods section needs to mention when the survey was administered (months & year). We have now provided information on when responses were collected: “Reponses were collected between July 2018 – January 2019.”

Line 178 and 242: “the university of XXXXX” – I assume the authors have blinded the university, but since this is not a blinded review, that is not necessary. Changed as suggested to include the University of Southampton.

Line 179: “spilt” should be “split”. Thank you! This has been corrected.

Line 192: AWERB should appear in full the first time it is used. Thank you – we have added in an explanation of the abbreviation.

Lines 192-195: this information should be presented at the beginning of the results section. The sentence “Participants represented a variety of roles, including but not limited to: Establishment Licence Holders (ELHs), Named Veterinary Surgeons (NVSs), AWERB (Animal Welfare and Ethical Review Body) chairs, Named Animal Care and Welfare Officers (NACWOs), and Named Information Officers (NIOs)” has been moved to beginning of results section.

Line 216 and 496 (for example): sometimes GA is used and sometimes GM, while I think the authors mean the same. We have now used GA (in accordance with Home Office policy guidance) throughout the paper.

Line 218: No need for this long sentence, just use the term that was introduced before: surplus animals. Thank you for the advice, we have removed the long sentence and used surplus.

Lines 207-235: The data processing section is too long and fragmented. Also, crucial information is missing. Please create one or two paragraphs with data processing information, concisely reporting how the responses to the questions were processed (how were closed questions processed, what about open questions – was thematic analysis used?), which variables were calculated, why and how….Thank you for this helpful advice. The data processing section has now been cut back to two shorter paragraphs. More data has been provided regarding the way in which the open question data was analysed: “Analysing data from the open questions involved a structured inductive thematic analysis. This helped to identify common topics, ideas, concepts and patterns from the data. In order to do this, we used Nvivo12 to code the data and to generate themes from it. Using Nvivo12, the thematic analysis also involved a frequency count, where it was possible to see the number of times each identified theme was referenced across all participants”. More detail has also been provided regarding how closed question responses were analysed: “Nvivo12 was used to analyse the qualitative responses, Microsoft Excel 2016 to analyse quantitative findings and assist in numerical analysis (including calculating numbers of animals rehomed), and SigmaPlot (Version 13) to assist in graph production”. As we looked at the sample (41 facilities) as a whole, no independent variables were included. Further, the questionnaire involves descriptive statistics, so there is no need to explain how independent variable were calculated.

RESULTS

Lines 259-261: this is a bold statement that is insufficiently supported by the data that are presented. How does the variety in the survey relate to the variety in all other facilities? Thank you for the advice – this statement has been removed.

Figure 1: I would delete figure 1. There is no added value there, as the numbers are already in the text. Thanks – Figure 1 has been deleted in line with reviewer comments.

Line 278-280: I find this an odd statement, given that, equally, it is very possible institutions that do not rehome did not complete the survey. Also, does this mean that incomplete surveys were not counted? This needs to be stated in the data processing part of the Methodology section. We have now deleted “It is possible that facilities currently engaged in rehoming did not complete the questionnaire, nevertheless 19 represents more than 1 in 10 research facilities.” We have also added into the methodology that incomplete surveys were not counted.

Line 289: “If we assume that the ratio above extends” – to what? This section of the sentence has been removed, as it was unclear.

Line 291: This is an example of how minimum percentage is not used throughout. Because it is a minimum, you can only state that “at least 0.02% of laboratory animals are known to be rehomed from 2015-2017”, but again, this figure to me is really misleading as it is a huge underestimation. Thank you - this figure has been removed throughout the paper in line with wider comments regarding the analysis.

Line 300: keep in mind that primates may not be rehomed in the UK sense of the word, but they may be retired from research, while still living at the facility. Thanks – we have added in this thoughtful contribution.

Table 1: again, misleading due to the “known percentage rehomed” calculation. Similar comment for the last column with the ration. This has been removed from the table.

Figure 4: The left pie chart is difficult to read. I would turn this figure into a table comparing proportions of animals rehomed (41 institutions) and animals kept (UK total). This, in my opinion is the only valid numerical comparison that could be made (see my major concern about the calculation of “known percentage rehomed”). Thank you for your advice, the pie chart has now been converted to a table.

Lines 349 and beyond: the presentation of results is very qualitative as it almost looks at individual responses from respondents. I feel a more structured analysis, like a thematic analysis with a frequency count, is appropriate. This is a very useful contribution, a structured analysis with a frequency count has now been included.

Lines 487-489: The grouping of reasons for not rehoming does not adequately capture the responses. E.g. Fear of unwanted or negative media attention is not a practical issue. Please re-consider this. We have amended this to include three groupings; “welfare concerns with regard to the animal’s health if rehomed, practical issues surrounding demand and the fact that research needs’ tend to leave few animals to retire, and external issues including fear of negative media attention”.

DISCUSSION

Lines 526-527: “this is also demonstrated by only one facility of the 41 facilities”: it is not clear what is demonstrated. This sentence has been made clearer – it is the fact rehoming is often a consideration in UK research facilities that is demonstrated.

Line 545 and beyond: the authors seem to suggest that all GM models pose a biosecurity risk, which is not true. Added in “Despite it being scientifically unclear exactly how some GA animals might pose a biosecurity risk, the rehoming of GA animals was considered illegal by some who responded to the survey.”

Line 585: “this effect” – which effect? Please state clearly to what you are referring. Thank you for your advice, this has now been made clearer – the effect referred to is the improvement in staff wellbeing through rehoming.

Attachment

Submitted filename: Response to reviewers.docx

Decision Letter 2

I Anna S Olsson

1 Jun 2020

PONE-D-20-01484R2

A semi-structured questionnaire survey of laboratory animal rehoming practice across 41 UK animal research facilities

PLOS ONE

Dear Dr. Skidmore,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

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We look forward to receiving your revised manuscript.

Kind regards,

I Anna S Olsson, Ph.D.

Academic Editor

PLOS ONE

Additional Editor Comments (if provided):

General: It is debatable whether the term euthanasia should be used when animals are killed in situations when it is not in their own interest. I recognize that the term euthanasia is predominant when referring to animals killed for research purposes, but I invite you to reflect on whether it is the best term in your paper. For example, you write "Euthanasia is undertaken for three primary reasons – 1) as a scientific  requirement, 2) to prevent avoidable suffering, or 3) for financial/logistical reasons". Critics would say that the term "euthanasia" only applies to 2) in the cited example. I understand that you are aware of the controversy and briefly mention it in the introduction with a reference to Kuře, J., Euthanasia: The" Good Death" Controversy in Humans and Animals. 2011: BoD–

652 Books on Demand. Please consider changing to "killing" and justify your choice.

Table 1 I really appreciate the use of colour coding - please add that higher numbers are represented in more saturated colours.

Line 379 the owner is provided with appropriate housing and feeding for the rehomed animal(s).

Line 155 Existing literature notes this as an essential next step in (or the essential)

Lines 474-476 "there are challenges that come with rehoming to staff – an NVS explained how the rodents could not be rehomed to employees as staff might “acquire rodents from other sources” that are “microbiologically dirty […] which could present a risk of inadvertent delivery of disease”. This statement is a little puzzling as there is no obvious relation between rehoming rodents to staff and the same staff acquiring rodents from other sources. I assume that the relation may be that because microbiological contamination is considered a risk, staff are not allowed to keep rodents as pets, and therefore can't receive rehomed rodents. Do you know if this is the case?

Lines 496-500 and section Biosecurity Please provide a reference for that rehoming GA animals is not in itself illegal in the UK.

Figures 3-5: Please consider merging the 3 sets of graphs into one figure with 3 panels.

Reference list: Reference manager generated lists require careful manual checking. For example, "Office, H."  is not the right way to refer to the Home Office! There are also inconsistencies in whether journal titles are capitalized or not (they should be).

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: N/A

**********

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Reviewer #1: Yes

Reviewer #2: No

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Thank you for this very careful revision. You have implemented the reviewers' comments well. Please capitalize the word "owner" in the captions of Tables 4 and 5.

Reviewer #2: The authors were able to significantly improve the manuscript.

There is a remaining major concern about the discussion for me, which requires some additional work and consists of the following:

- Although it is true that not many papers exist on rehoming of research animals, there are some. Particularly with relevance to the section "finding the right home", I feel that it is approporiate to compare the practices to the shelter literature and investigated approach / recommended good practices.

- The authors report on the involvement of third party rehoming organisations. However, they should at least consider that these consist of volunteers who mean well, but who are rarely trained professionally for the duties they perform. This should be briefly discussed in relation to available literature on animal welfare volunteers.

- The fact that an extrapolation was made from 2017 data to 2015 and 2016 (see lines 215-217 in the methods section) should be mentioned as a limitation to the study, as this is based on the assumption that numbers are similar in those three years (if there is a good reason to assume this, then it should be mentioned as well).

The remaining minor concerns:

Line 37: "this period" should be clarified

Line 104: "desire" is perhaps a bit inappropriately anthropomorphic. Perhaps better to say something like "includes the degree to which the animal is provided with what it needs as well as wants" (or use "needs and wants" as these are commonly used terms in animal welfare science)

Line 142: why use "sentient" here explicitly for companion animals? This implies that the subsequent species mentioned (rabbits, rats, guinea pigs and mice) are not sentient, which is not commonly accepted as they are vertrebrates as well.

Table 1 : mention the number of UK facilities in the column header of the second column. In the caption, explain the coding of the shading, i.e. darker shading indicates a higher number.

Lines 300 - 314: this feels repetitive (title is also almost identical to the one above). Why not introduce the percentages of animal groups in the text in the section above, and then refer to table 1 for details?

Tables 3 and 4: captions should mention the total number of respondents

Lines 378-379: did the institution provide all the housing and food that the animal needed or did they provide some of it? It would be useful to have a specific example of what is meant.

Lines 568-571: sentence not entirely clear, particularly the first part "this does not mean rehoming... kept in UK facilities".

**********

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Reviewer #2: No

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PLoS One. 2020 Jun 19;15(6):e0234922. doi: 10.1371/journal.pone.0234922.r006

Author response to Decision Letter 2


3 Jun 2020

Thank you all for your very helpful comments.

General: It is debatable whether the term euthanasia should be used when animals are killed in situations when it is not in their own interest. I recognize that the term euthanasia is predominant when referring to animals killed for research purposes, but I invite you to reflect on whether it is the best term in your paper. For example, you write "Euthanasia is undertaken for three primary reasons – 1) as a scientific requirement, 2) to prevent avoidable suffering, or 3) for financial/logistical reasons". Critics would say that the term "euthanasia" only applies to 2) in the cited example. I understand that you are aware of the controversy and briefly mention it in the introduction with a reference to Kuře, J., Euthanasia: The" Good Death" Controversy in Humans and Animals. 2011: BoD–652 Books on Demand. Please consider changing to "killing" and justify your choice. Thank you for your suggestion – this is really interesting. I have now used the word ‘killing’ throughout, but have explained the term euthanasia to relate to the act of putting an animal out of avoidable suffering.

Table 1 I really appreciate the use of colour coding - please add that higher numbers are represented in more saturated colours. Thank you, I have now added this in.

Line 379 the owner is provided with appropriate housing and feeding for the rehomed animal(s). Thank you, I have changed in line with your comments.

Line 155 Existing literature notes this as an essential next step in (or the essential). Thank you! This has been changed accordingly.

Lines 474-476 "there are challenges that come with rehoming to staff – an NVS explained how the rodents could not be rehomed to employees as staff might “acquire rodents from other sources” that are “microbiologically dirty […] which could present a risk of inadvertent delivery of disease”. This statement is a little puzzling as there is no obvious relation between rehoming rodents to staff and the same staff acquiring rodents from other sources. I assume that the relation may be that because microbiological contamination is considered a risk, staff are not allowed to keep rodents as pets, and therefore can't receive rehomed rodents. Do you know if this is the case? Yes – that is the case. I have now made this clearer, and inserted: “Microbiological contamination is thus considered a risk, and therefore some facility staff cannot keep rodents as pets, including those from the laboratory.”

Lines 496-500 and section Biosecurity Please provide a reference for that rehoming GA animals is not in itself illegal in the UK. Thank you, I have now inserted a reference for the Home Office 2015 Advice Note that outlines that additional legislation may also apply to the rehoming of genetically altered animals.

Figures 3-5: Please consider merging the 3 sets of graphs into one figure with 3 panels. Thank you for the useful suggestion, I have now merged the 3 graphs into one figure.

Reference list: Reference manager generated lists require careful manual checking. For example, "Office, H." is not the right way to refer to the Home Office! There are also inconsistencies in whether journal titles are capitalized or not (they should be). Thanks - this has now been addressed.

Reviewer #1: Thank you for this very careful revision. You have implemented the reviewers' comments well. Please capitalize the word "owner" in the captions of Tables 4 and 5. Thank you for your very helpful comments – tables 4 and 5 now have a capitalised ‘Owner’.

Reviewer #2: The authors were able to significantly improve the manuscript.

There is a remaining major concern about the discussion for me, which requires some additional work and consists of the following:

- Although it is true that not many papers exist on rehoming of research animals, there are some. Particularly with relevance to the section "finding the right home", I feel that it is appropriate to compare the practices to the shelter literature and investigated approach / recommended good practices. Thank you for this very useful suggestion. I have added in some animal shelter literature and compared this to the findings of this research, mainly under the section “finding the right home”.

- The authors report on the involvement of third party rehoming organisations. However, they should at least consider that these consist of volunteers who mean well, but who are rarely trained professionally for the duties they perform. This should be briefly discussed in relation to available literature on animal welfare volunteers. Thanks for this – I have now reflected on this: “However, some of those that work at rehoming organisations are volunteers – and literature notes that these volunteers are not always taught the required skills to adequately train and socialise animals [32] In fact, only 12% of animal shelter employees across the US rated volunteers as well trained “to a great extent” [33]. Research also finds an irregular schedule of social contact with animals from volunteers and frequent changes in active volunteers [34, 35].”

- The fact that an extrapolation was made from 2017 data to 2015 and 2016 (see lines 215-217 in the methods section) should be mentioned as a limitation to the study, as this is based on the assumption that numbers are similar in those three years (if there is a good reason to assume this, then it should be mentioned as well). Thank you for this useful thought – I have now added “Finally, an extrapolation was made from 2017 Home Office data to the years 2015 and 2016 to calculate an approximate number of surplus animals across the 3 years. However, there is likely to be some variance in the proportions of surplus animals by species year by year that is not accounted for.”

The remaining minor concerns:

Line 37: "this period" should be clarified. Thank you, this period has now been clarified to between 2015-2017.

Line 104: "desire" is perhaps a bit inappropriately anthropomorphic. Perhaps better to say something like "includes the degree to which the animal is provided with what it needs as well as wants" (or use "needs and wants" as these are commonly used terms in animal welfare science). I have now added in “It includes the degree to which the animal is provided with its needs and wants”.

Line 142: why use "sentient" here explicitly for companion animals? This implies that the subsequent species mentioned (rabbits, rats, guinea pigs and mice) are not sentient, which is not commonly accepted as they are vertebrates as well. I have now removed the word sentient.

Table 1 : mention the number of UK facilities in the column header of the second column. In the caption, explain the coding of the shading, i.e. darker shading indicates a higher number. Thank you for your comments, I have now added in an explanation of the darker shading, and the total number of UK facilities.

Lines 300 - 314: this feels repetitive (title is also almost identical to the one above). Why not introduce the percentages of animal groups in the text in the section above, and then refer to table 1 for details? Thank you – I have removed table 2, and added in the text: “Although 94.15% of species kept in laboratories are rodents, they make up under a fifth (19.14%) of all animals known to be rehomed between 2015-2017. Conversely, birds, cats, dogs, horses, amphibians and agricultural animals constitute 80.86% of total species rehomed, despite making up just 5.84% of those kept (see Table 1 for more details). This is based on the following grouping: dogs (beagles and all other dog breeds), small mammals (rats, mice, gerbils, rabbits, hamsters, ferrets, guinea pigs), birds (common quail and all other birds), agricultural animals (cattle, sheep, pigs and goats), and cats, horses, amphibians and primates. Fish were excluded from this analysis due to one outlier facility having rehomed over 1200. There thus exists a preference for the rehoming of some species over others”

Tables 3 and 4: captions should mention the total number of respondents. I have now added in n=19 on the table caption.

Lines 378-379: did the institution provide all the housing and food that the animal needed or did they provide some of it? It would be useful to have a specific example of what is meant. Thank you – I have explained that it was generally initial food to help the animals acclimatise. I have also added in a quote “The animals are always released with items from their home cages and some diet. We inform the new owners it will take them quite a while to acclimatise and for the initial few days just to place their hands in the cage and let the animals come to them” to provide a specific example of what is meant.

Lines 568-571: sentence not entirely clear, particularly the first part "this does not mean rehoming... kept in UK facilities". Thank you – this had been modified to “Despite the clear impossibility of finding homes for all of the rodents and fish currently kept in UK facilities, there would be merit in understanding the drivers and processes of rehoming even small numbers of these species.”

Attachment

Submitted filename: Response to reviewers.docx

Decision Letter 3

I Anna S Olsson

5 Jun 2020

A semi-structured questionnaire survey of laboratory animal rehoming practice across 41 UK animal research facilities

PONE-D-20-01484R3

Dear Dr. Skidmore,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

I Anna S Olsson, Ph.D.

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Acceptance letter

I Anna S Olsson

9 Jun 2020

PONE-D-20-01484R3

A semi-structured questionnaire survey of laboratory animal rehoming practice across 41 UK animal research facilities

Dear Dr. Skidmore:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr I Anna S Olsson

Academic Editor

PLOS ONE

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Appendix

    (DOCX)

    Attachment

    Submitted filename: Response to reviewers.docx

    Attachment

    Submitted filename: Response to reviewers.docx

    Attachment

    Submitted filename: Response to reviewers.docx

    Data Availability Statement

    There are ethical restrictions on sharing the data gathered from the questionnaire. Data cannot be shared resulting from the impossibility of fully anonymising questionnaire results. To allow access to the data through sharing is in direct contradiction to the ethical agreement signed by participants, and approved by the University of Southampton’s ethical committee. The University of Southampton’s ethical committee (Head of Research Governance) can be contacted at: rgoinfo@soton.ac.uk.


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