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Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs (2020)

Chapter: 5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs

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Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Page 145
Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Page 146
Suggested Citation:"5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs." National Academies of Sciences, Engineering, and Medicine. 2020. Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs. Washington, DC: The National Academies Press. doi: 10.17226/25772.
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Below is the uncorrected machine-read text of this chapter, intended to provide our own search engines and external engines with highly rich, chapter-representative searchable text of each book. Because it is UNCORRECTED material, please consider the following text as a useful but insufficient proxy for the authoritative book pages.

5 Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs This chapter begins with a discussion of the literature surrounding the latest approaches in animal care and welfare as well as the relevant regulations and standards that apply to laboratory dog care and welfare. The chapter ends with a discussion of recommended actions for the U.S. Department of Veterans Affairs (VA) to enhance the well-being of laboratory dogs used in biomedical research. CURRENT KNOWLEDGE IN THE SCIENCE OF ANIMAL WELFARE: A BRIEF OVERVIEW Over the past 50 years an impressive array of work has been done to understand the welfare of animals in a range of settings, from farms and laboratories to zoos, shelters, and the wild. To survey that work, even within the laboratory setting, is beyond the scope of this report, but four key conceptual advances from this period inform practice regarding the welfare of animals in human care today. These advances reflect four developments in the field of animal welfare: the recognition of animal sentience, the emergence of three distinct approaches to the nature and assessment of animal welfare, a focus on positive and negative welfare states, and the recognition that welfare assessments incorporate both resource-based and animal-based considerations. Recognition of Animal Sentience The first of these developments was the widespread acceptance that many kinds of animals—and certainly all of the higher vertebrates (mammals and birds)—are sentient organisms (Duncan, 2006; Proctor, 2012; Proctor et al., 2013). They have the ability to receive sensory input that originates inside or outside of their bodies, and the integration of that input can produce states that may range from negative to positive, which the animal can consciously experience (Proctor et al., 2013; Silverman, 2008). Acceptance of animal sentience paved the way for advances in understanding the nature of animal welfare and how to assess it. Three Approaches to the Nature and Assessment of Animal Welfare The second development stemmed from the emergence of three distinct schools of thought on the nature and assessment of animal welfare; these schools of thought can be referred to as “biological functioning,” “natural living,” and “affective states” (Duncan, 2006; Duncan and Petherick, 1991; Fraser, 1995, 2003, 2008; Green and Mellor, 2011; Hemsworth et al., 2015; Mellor, 2012, 2015a,b,c). The biological functioning approach associates good welfare with the 134 Prepublication Copy: Uncorrected Proofs

Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the VA satisfaction of an animal’s physical and behavioral needs and therefore focuses on ensuring survival and reproduction, the absence of disease or injury, and the absence of abnormal or pathological behaviors. The natural living approach defines optimal welfare conditions as those that approximate the animals’ natural habitat as closely as possible and that enable the animals to exhibit “natural” behaviors to the fullest extent possible. The affective states approach argues that how an animal feels is of primary importance in determining its welfare, and it associates good welfare with conditions in which an animal’s experience of positive emotions, feelings, and sensations outweighs the negative. Because emotions or feelings may not be directly measurable, this last approach relies on behavioral and physiological cues to indicate positive or negative affective states. Carried to its most extreme interpretation, each of these approaches to animal welfare may result in a situation where the animal’s welfare is arguably poor (Fraser, 2008). For example, a focus on biological functioning that leads to a use of extremely hygienic and restricted housing to prevent any risk of injury and illness may create such a barren or stimulus- poor environment that the animal suffers from boredom, stress, or anxiety due to separation from conspecifics. A natural living focus that allows animals to roam in large outdoor accommodations in natural social groups could expose the animals to diseases, parasites, predators, and aggression from conspecifics. And although the constant availability of unlimited rich food may cause an animal to “feel good” most of the time, satisfying the goals of the affective states approach, this can be lethal in the long run. It is also the case, however, that many types of animal welfare interventions can satisfy the goals of multiple approaches to animal welfare. For example, routine vaccination programs for canines not only provide protection from disease, but they also support better overall health, a greater propensity to behave naturally, and an avoidance of the negative affective states associated with disease, such as nausea or dehydration. Providing compatible dogs with conspecific socialization allows them to exhibit species-typical behaviors, obtain beneficial exercise, and have opportunities for pleasurable experiences such as play. There is no scientific consensus regarding which model— biological functioning, natural living, or affective states— best represents animal welfare (Fraser, 2008). Instead, conceptual frameworks that tie these approaches together have emerged in the agricultural and scientific arenas. The five freedoms framework, proposed in 1979 by the Farm Animal Welfare Council in the United Kingdom, argues that animals in human care should be free from hunger, thirst, and malnutrition; free from discomfort; free from pain, injury, and disease; free from fear and distress; and free to express normal behavior (Webster, 2005a, pp. 12–16). Responding to some of the limitations of the Five Freedoms framework (e.g., it is impossible to ensure that animals are never hungry), Mellor and Reid (1994) developed the five domains of welfare compromise model, with a scoring system to assess welfare in each of these domains. The original five domains framework focused on measurement of welfare compromise (i.e., negative welfare states). Positive and Negative Welfare States The third major development in animal welfare science was a shift in focus from minimizing or eliminating animal suffering to creating conditions that enhance positive welfare states and pleasurable experiences for animals (Boissy et al., 2007; Gonyou, 1993; Mellor, 2015a,b,c; Yeates and Main, 2008). The basic premise behind this shift was that welfare exists Prepublication Copy: Uncorrected Proofs 135

Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs on a continuum of poor to good, so merely eliminating negative welfare conditions would not necessarily move an animal into a positive welfare state. In this vein, the five domains model and other approaches to animal welfare management have since been extended to consider positive welfare states (Green and Mellor, 2011; Mellor and Beausoleil, 2015). In discussing welfare assessment methods for laboratory animals, Beaver and Bayne (2014) suggest that indicators of poor welfare be addressed first, before considering indicators of positive welfare. Certainly, a serious indicator of negative welfare (e.g., self-harming behavior) requires immediate action, but there is no reason to identify or address one type of indicator before the other; they can be assessed and addressed simultaneously. Extending the consideration of positive versus negative welfare states to an animal’s entire life, Yeates (2011) discusses the concept of a “life worth living,” which in general terms refers to an animal’s life in which positive experiences outweigh negative experiences in terms of frequency, duration, or degree. This is contrasted with a “life not worth living” in which negative experience outweighs positive experience (Yeates, 2011). While there are limitations with the implementation of this concept at a broad scale (Yeates, 2011), adopting a philosophy of providing animals with as much positive experience as possible while minimizing negative experiences when feasible is consistent with ethical use of animals. Animal-Based Assessment of Welfare The fourth development in animal welfare science, and specifically in welfare assessment, involved expanding the focus of assessment from purely resource-based measures, such as the quality of housing or diet, to include animal-based measures, such as wounding rates or behavior (Hewson, 2003; Leach et al., 2008; Webster, 2005b; Webster et al., 2004; Whay, 2007). This change reflected a widespread acknowledgement that the most relevant assessments of animal welfare, indeed by definition (Gonyou, 1993), are those that focus on the animal and how it is faring. Studies of farm animals demonstrate that animal-based measures of animal welfare can vary dramatically across facilities (Fraser, 2014; Main et al., 2003), even among farms that employ the same housing systems or resource-based welfare certification programs, and that performance on certain welfare indicators does not necessarily correlate with participation in a certification program (Main et al., 2003). Given the limited predictive value of resource-based welfare management and assessment, it has been suggested that welfare issues at individual sites would be better addressed at the local level rather than modifying overarching guidance, legislation, or certification programs (Main et al., 2003). The growing understanding of the need for animal-based assessment measures is particularly relevant to considerations regarding the welfare of laboratory animals, including dogs, for whom current requirements governing use, care, and housing (e.g., Guide for the Care and Use of Laboratory Animals [NRC, 2011; the Guide]) emphasize resource-based indicators, such as parameters of diet or housing, over animal-based indicators. Nonetheless, animal-based measures of welfare have been developed for laboratory animals, including mice (e.g., Leach et al., 2008; reviewed in Beaver and Bayne, 2014). A number of welfare assessment tools have been developed for dogs, including those with spinal cord injuries (e.g., Budke et al., 2008), cardiac disease (e.g., Freeman et al., 2005), and chronic pain (Wiseman-Orr et al., 2004, 2006), as well as for healthy dogs (e.g., Lavan, 2013), with a recent review by Belshaw et al. (2015). Comprehensive welfare assessments that include animal-based measures are now mandated by the Association of Zoos and Aquariums (AZA, n.d.), a professional accrediting body in the zoological profession. 136 Prepublication Copy: Uncorrected Proofs

Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the VA Conclusion 5-1: Animal welfare is multi-dimensional, reflecting the health, comfort, behavior, and emotions of animals in human care. There is a need for the U.S. Department of Veterans Affairs to combine aspects of each of the three major approaches to animal welfare, explicitly consider positive and negative welfare states, and measure animal-based welfare indicators in order to enhance the positive welfare of laboratory dogs. ADDITIONAL CONSIDERATIONS FOR ENHANCEMENT OF THE WELFARE OF LABORATORY DOGS Considerations Related to Human and Conspecific Contact Several studies suggest that the presence of human companions may be more effective in reducing behavioral and physiological indicators of stress in dogs than the presence of a canine companion (Pettijohn et al., 1977; Tuber et al., 1996). Specifically, physical contact with humans in the form of stroking or handling has been demonstrated to have a positive influence on a dog’s behavior and physiological reactions to stress (Fuller, 1967; Hennessy et al., 1998; Lynch and McCarthy, 1967; also see review by Payne et al., 2015). Slow, firm stroking after one venipuncture was found to decrease subsequent cortisol production after a second venipuncture 20 minutes later (Hennessy et al., 1997, 1998). These findings led Tuber et al. (1999) to conclude that even single instances of human interaction with familiar or unfamiliar people can have an ameliorating influence on dogs in shelter environments. Payne et al. (2015) review literature on dog–human bonding that demonstrates that certain human behaviors (e.g., affiliation and attention) contribute to positive emotional states in dogs and to stronger bonds between dogs and humans, and are associated with lower physiological arousal in dogs, as measured by cortisol levels. Experimental and observational research indicates that many dogs benefit from contact with other dogs as well as with humans (see Meunier and Beaver, 2014; Taylor and Mills, 2007, for reviews). For example, dog activity increased when human caretakers were actively working in a housing facility and decreased during lunch hours and overnight, although an additional 30 minutes of human contact did not appreciably increase activity (Hughes and Campbell, 1990). (The authors of this study were unable to distinguish between normal locomotor patterns and repetitive, possibly abnormal movements.) A study in shelter dogs showed that the most important variable contributing to the level of welfare of dogs was the opportunity to regularly leave the cage for a walk, whereas other variables like gender, cage size, individual housing, and reproductive intactness had no significant effect on the physiological indicators of welfare. Dogs that had the opportunity to go on walks had high antioxidant capacities and performed displacing activities or stereotyped behaviors less frequently (Cafazzo et al., 2014). Dogs that were simply given a larger cage to exercise in as opposed to a walk had total antioxidant capacity similar to dogs that were not put into larger exercise cages (Cafazzo et al., 2014). Clark et al. (1997) found that placing individual dogs in out-of-cage exercise areas for 20 minutes several days per week did not increase activity or prevent the development of abnormal behaviors. While there is no strong evidence that cage size has an effect on activity, many of the existing studies compared very small cages to slightly larger cages, which may not be saliently different to the dogs, and these studies involved small sample sizes (Taylor and Mills, 2007). While enclosure size may be less important than the quality of the space and opportunities for socialization, enclosures containing multiple animals must be large enough for the animals to rest Prepublication Copy: Uncorrected Proofs 137

Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs separately, to make use of visual barriers between themselves and cage mates, and to sleep and eat away from areas used for defecation and urination (Meunier and Beaver, 2014). Hubrecht and Buckwell (2007) go so far as to recommend that laboratory environments enable dogs to be housed in social groups and that solitary housing be avoided whenever possible and only implemented in exceptional circumstances. U.S. Department of Agriculture (USDA) regulations do not require social housing, but if the animals are group housed, they have to be compatible.1 Considerations Related to Comfortable Environments Many texts and overviews exist that provide guidance on optimal care, housing, and the management of dogs in laboratory environments in order to optimize welfare (e.g., Hubrecht and Buckwell, 2004; Meunier and Beaver, 2014; NRC, 1994; Prescott et al., 2004; Stafford, 2006). Tuber et al. (1999) describe the importance of having a simulated “living room” in a dog shelter, which has the added benefit of acclimating dogs to home-like environments. For laboratory dogs, this would correspond to having a place apart from the kennel environment and other dogs where humans and dogs can interact in a quieter setting. Dogs may vary, according to breed and disposition, in their requirement for this type of interaction and setting, but if it is made available, then individual dogs’ responses to such an environment can be evaluated through an animal-based assessment. Access to enrichment toys is important for visual, olfactory, and social stimulation. A frequent rotation of enrichment is recommended, as dogs can lose interest in a given item within 1 or 2 days (Overall and Dyer, 2005; Wells, 2004). RELATIONSHIP OF CURRENT STANDARDS, REQUIREMENTS, AND RECOMMENDATIONS TO DEVELOPMENTS IN ANIMAL WELFARE SCIENCE Legislation, policies, and regulations pertaining to the welfare of dogs in research were summarized in Chapter 2. While these various regulatory and oversight processes provide a wide-ranging framework for animal care and use with assessments mandated by regulation, their focus is almost exclusively input-based (concerned with practices and features provided to the animals). Current USDA regulations require daily observation of animals to assess their health and well-being; additionally, institutional animal care and use committees (IACUCs) are required to inspect all animal facilities and study areas every 6 months to review the condition of the animals. Conclusion 5-2: While the Guide for the Care and Use of Laboratory Animals and the Animal Welfare Act provide a foundation for the assessment of well-being, the U.S. Department of Veterans Affairs has an opportunity to incorporate current developments in animal welfare science into its animal care and use program. 1 CFR Title 9 Subchapter A: Animal Welfare; see §§ 3.7, 3.8. Available at https://www.govinfo.gov/content/pkg/CFR-2013-title9-vol1/pdf/CFR-2013-title9-vol1-chapI-subchapA.pdf (accessed March 24, 2020). 138 Prepublication Copy: Uncorrected Proofs

Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the VA Clarification of AAALAC International Accreditation and Use of the Guide as Regulations In addition to the general provisions in the Guide mentioned in Chapter 2, the Guide discusses several specific areas of attention pertinent to the welfare of dogs during routine care and in experimental training. The Guide notes that enclosures that provide greater freedom of movement and vertical height (e.g., kennels) are preferred for dogs, and if they are housed individually or in smaller enclosures, dogs should be given the opportunity to socialize and experience positive human interaction (NRC, 2011). Additional opportunities for socialization mentioned include being walked on a leash, having access to a run, or being moved into areas for play, exploration, and social contact (NRC, 2011). Manipulatable toys are useful for enrichment and should be rotated to maintain the animal’s interest (NRC, 2011). The Guide encourages the use of behavioral conditioning to habituate and train animals to participate voluntarily in experimental procedures. The comprehensive peer review process conducted by AAALAC International encompasses the review and assessment of the effectiveness of implementation of the elements noted above in programs of laboratory research with dogs. AAALAC International site visits normally occur triennially; however, due to the public interest in and visibility of research with dogs at the VA, visits focused on the care and use of dogs at the VA are now conducted by AAALAC International every 18 months. The AAALAC International accreditation process identifies programmatic strengths and weaknesses according to the Guide and engages the institution to pursue timely corrective actions of problematic areas. Moreover, the professional interactions of the AAALAC International site visit process incorporate two other important principles in ethics and in oversight from the Guide. First, programmatic leadership is reminded that the use of animals in research is a privilege and that “[e]thical considerations discussed here and in other sections of the Guide should serve as a starting point; readers are encouraged to go beyond these provisions” (NRC, 2011, p. 4). Second, as a practical and operational matter, “[t]he body of literature related to animal science and use of animals is constantly evolving, requiring Programs to remain current with the information and best practices” (NRC, 2011, pp. 12–13). Relevant International Guidelines or Non-USDA/AAALAC International Recommendations/Standards with Regard to Dogs While the VA is only required to follow U.S. regulations, there may be value in consulting regulations from other countries to determine if enhancements to existing programs could be made. Considering the committee’s Statement of Task and the directive in Chapter 1 of the Guide noted above, it is useful to examine approaches identified in other international regulatory frameworks that are intended to enhance the welfare of dogs used in research while permitting the attainment of research objectives. The countries of the European Union are expected to follow Directive 2010/63EU (EUR-Lex, n.d.) on the protection of animals used for scientific purposes through the transposition of the principles of the directive into national regulations. It is beyond the scope of this discussion to summarize each of the national regulations spawned by Directive 2010/63EU in order to identify elements that would potentially improve laboratory dog animal welfare. However, the implementation details of Directive 2010/63EU elaborated in the European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Purposes (ETS 123) (Council of Europe, n.d.) provide some insight. The principles in ETS 123 are largely consonant with those of the Guide but offer Prepublication Copy: Uncorrected Proofs 139

Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs specific provisions that may confer additional animal welfare benefits to laboratory dogs. For example, ETS 123 emphasizes that dogs may not be singly housed for more than 4 hours, and if for experimental purposes they must be singly housed for longer than that, then they should, if possible, be afforded time daily for human socialization and visual, auditory, and tactile contact with other dogs (Council of Europe, n.d.). Also, the space requirements for laboratory dog housing in ETS 123 afford dogs more space for all weight categories than the dog housing space recommendations of the Guide. In addition to specifying more space, the ETS stipulates that no less than 50 percent of the space will be dedicated to the indoor housing area and that an outdoor run area should be provided where possible (Council of Europe, n.d.). It is widely recognized that the mere availability of more space does not ensure that the space will stimulate increased exercise or beneficially enhance the environment of the enclosure for the dog; the quality of the space provided must also be recognized as an essential parameter (Campbell et al., 1988; Hite et al., 1977; Hughes et al., 1989). The Australian Guidelines for the Care and Housing of Dogs in Scientific Institutions (NSW Agriculture, 1999), citing the work of Serpell and others (Serpell, 1995), provides a detailed discussion of the design of the dog housing enclosure, emphasizing its important role in dog social interactions, environmental control/stimulation, comfort, and exercise. The UK National Centre for the Replacement, Refinement, and Reduction of Animals in Research provides comprehensive information on laboratory dog housing, tools for assessing the welfare of laboratory dogs, and opportunities for refining procedures in studies (NC3Rs, n.d.). Conclusion 5-3: In the pursuit of enhancements to the care and use of laboratory dogs in U.S. Department of Veterans Affairs (VA) research, international regulations and guidelines may be a useful resource for alternate approaches and recommendations. International guidelines and recommendations offer the VA programmatic leaders and institutional animal care and use committees expanded perspective on the contemporary literature and trends on laboratory dog care. ASSESSMENT OF CURRENT VA PRACTICES: DO THEY MEET CURRENT STANDARDS, REQUIREMENTS, AND RECOMMENDATIONS WITH REGARD TO THE CARE AND WELFARE OF DOGS? Members of the committee conducted site visits to two VA programs engaged in dog research—one at the McGuire VAMC Veterinary Medical Unit in Richmond, Virginia, and the other at Washington University School of Medicine in St. Louis, Missouri. The purpose of these visits was to meet with the personnel involved in the oversight, care, and research on dogs and to observe the conditions and practices associated with this use. Materials obtained in advance of the site visit to the Richmond VA Medical Center2 indicated that the practices relating to dog husbandry and care were sound and conformed with the requirements specified in the Animal Welfare Act (AWA)/Animal Welfare Regulations (AWRs)3 and the Guide (NRC, 2011). These materials included two letters of accreditation from AAALAC International, which strongly supported the VA’s assertion of a high-quality program for the care and use of dogs; the 2019 AAALAC International letter described the VA program as “exemplary.” An external review by 2 VA (U.S. Department of Veterans Affairs). 2019. McGuire VAMC Richmond NAS response, July 2019, and AAALAC International letter, 2019, to inform committee subgroup site visit. 3 CFR Title 9 Subchapter A: Animal welfare. Available at https://www.govinfo.gov/content/pkg/CFR-2013-title9- vol1/pdf/CFR-2013-title9-vol1-chapI-subchapA.pdf (accessed March 24, 2020). 140 Prepublication Copy: Uncorrected Proofs

Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the VA the National Institutes of Health’s Office of Laboratory Animal Welfare (OLAW, 2019) found provisions for the care of dogs at the Richmond VA Medical Center to be in compliance, as did upper management within the VA system. Strong administrative support for the Richmond VA dog research program was evident. Specifically, two new positions had recently been added, augmenting the resources available for dog care and use in the areas of surgery, post-procedural care, behavioral management, and socialization. These enhancements were buttressed by a new electronic clinical veterinary record system with which to document care. The administration also supported ample training and educational opportunities for the animal facility staff. A large body of research with livestock has demonstrated that general attitudes toward animals, attitudes about aspects of working with animals, and the behavior of stockpersons toward animals (specifically negative and positive interactions) have measurable impacts on the behavior and physiology—and thus the welfare—of the animals that these individuals care for. Such impacts extend to production metrics (e.g., milk yields, farrowing rates, egg production) in a variety of species (Hemsworth and Coleman, 2011). Research also demonstrates that human companion or caretaker attitudes and behavior correlate with welfare indicators in dogs (Payne et al., 2015) and in non-domesticated species maintained in zoos (e.g., Carlstead et al., 2019; Wielebnowski et al., 2002; see review by Cole and Fraser, 2018). Mellen (1991) observed that positive interactions with caretakers resulted in greater reproductive success in non-domestic, zoo-housed felids. Positive interactions with humans are also associated with positive impacts on laboratory species (e.g., Bayne, 2002; Bloomsmith et al., 1997; Waitt et al., 2002). Positive attitudes about animals are correlated with job enjoyment and willingness to learn in stockpeople (Coleman et al., 1998), whereas lower caretaker job satisfaction can be associated with a weaker human–animal bond (Carlstead et al., 2019). The strength of the human–animal relationship is reinforced through positive caretaker behaviors toward the animals and animal responses to the caretaker; the relationship is reciprocal (Hemsworth, 2003). This is relevant because during site visits at both the Richmond and St. Louis facilities, several observations surfaced that would suggest that human–animal relationships involving the laboratory dogs are positive, provide mutual benefits to animal and caretaker, and are reinforced via job satisfaction. First, at both facilities the laboratory dogs enthusiastically approached and engaged with caretakers and laboratory personnel, suggesting that the dogs viewed this contact positively, which would not be expected if the dogs were fearful of these individuals. Second, the staff reported high dedication to their jobs and commitment to the animals’ well-being. Associated with this, staff at both facilities reported having good access to resources, financial and otherwise, for enriching the dogs’ lives. Third, staff reported at both facilities that, despite their support for animal research, often the most difficult or least favorite parts of their jobs were managing their attachments to the animals, knowing the animals would be euthanized at the end of the study. Staff got to know each dog individually and developed a relationship with the dog, and this was at times difficult to manage when studies ended. Fourth, staff reported having excellent support for continuing education to maintain and advance their skills in animal care and saw opportunities for professional growth in their organizations. Finally, staff were knowledgeable and comfortable with the processes in place for bringing up concerns about animal care and welfare. Procedures were available for reporting animal welfare concerns anonymously, if the staff person so chose. Through discussion with IACUC members, researchers, and veterinary staff, it was determined that the IACUCs were functioning well within the guidelines of the VA and federal Prepublication Copy: Uncorrected Proofs 141

Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs regulations. In St. Louis, there appeared to be good communication between the Washington University IACUC and the VA IACUC. Both the Richmond and St. Louis IACUCs approached harm–benefit analysis by discussing concerns and weighing potential harms and benefits in a deliberative process. The IACUCs described well-defined procedures and practices for reporting unusual findings or adverse events in the laboratory dogs and ensuring prompt and appropriate engagement of the veterinary medical officer to manage clinical events arising either spontaneously or due to experimental complications. At Richmond, veterinary care was under the direction of an external consultant who had appropriate training, experience, and involvement in all relevant areas of the program and good rapport with research and animal care staff. At St. Louis, veterinary care was provided by the onsite veterinarian and his staff. The process for selection and approval of the dog model was reaffirmed in meetings that committee members had with the investigators conducting dog research and with the IACUC. Interestingly, the VA had also provided funding for studies approved by the IACUC to enable the investigators to explore the experimental feasibility of using pigs as an alternative to dogs. Dogs at both facilities were individually housed two to five per room in primary enclosures (pens) that met the federal space requirements and afforded the animals an opportunity to exercise. In Richmond, the pens were constructed of galvanized wire separators and did not contain rest boards or other structural embellishments. Padded beds were provided to some dogs when available. In St. Louis the pens were the size required by the AWRs for exercise opportunity for individually housed dogs. The runs had stainless steel partitions with chain link tops that allowed the dogs to see over the partition. The fronts of the cages were chain link so a dog could view the dog across from it in the room. There were only two dogs present in St. Louis. One was male and one was female, so they were separately housed, but they had visual contact with each other. Each run had a resting board. An enrichment toy was present in each cage and changed at least weekly or as needed for sanitation. At Richmond, the dogs were housed in individual pens due to constraints of the data collection technology. The dogs had surgically implanted sensors for collecting data on cardiac function. A portion of the sensor protruded from the dog’s ventrolateral thorax, raising concerns that dog–dog interactions could damage the sensor or injure the dog. Additionally, the data collection from the sensors is remote and continuous, and two sensors in very close proximity interfere with one another’s signals. In Richmond, groups of dogs were released into a communal exercise enclosure for approximately 45 minutes 5 days per week for additional supervised socialization with technicians, who encouraged dog–dog interactions and play with enrichment objects. Various enrichment devices were rotated through the dogs’ primary enclosures to maintain their interest, and a special food item was provided weekly. On weekends, dogs were released from their home cages for 10 minutes daily during the cage cleaning procedure. Sporadically, dogs were permitted to freely range or walk on leash more widely to the office areas of the animal facility with supervision. In St. Louis, the dogs were released into a hallway at least twice per week with human interaction. They could freely run the hall to chase balls or interact with people. Dogs were also released within the room while caretakers were cleaning runs. The staff at the St. Louis site is planning to obtain pen partitions that would allow the dogs to move between runs for more space. They are also considering a separate playroom to use rather than the current hallway. Both the Richmond and St. Louis support facilities, such as surgeries and treatment rooms, were state of the art and well maintained. 142 Prepublication Copy: Uncorrected Proofs

Care and Welfare of Laboratory Dogs Used in Biomedical Research Funded by or Conducted at the VA Conclusion 5-4: Based on the information obtained during site visits and in materials submitted to the committee, including AAALAC International accreditation letters and the Office of Laboratory Animal Welfare report on assessment of the U.S. Department of Veterans Affairs (VA) canine research program, the committee concludes that the VA appeared to meet or exceed current regulatory requirements. Nonetheless, the committee observed several areas where the VA’s animal program could be enhanced, and those enhancements are included in the recommendations below. CONSIDERATIONS FOR ENHANCEMENT AT THE VA Recommendation 6: Enhance the welfare of laboratory dogs used for biomedical research. The U.S. Department of Veterans Affairs (VA) should enhance the welfare of laboratory dogs used in biomedical research in their facilities in the following ways: • Submit to voluntary U.S. Department of Agriculture (USDA) inspections of dog facilities to increase transparency. o As a federal agency, the VA must meet all Animal Welfare Act requirements, but it is not subject to mandatory inspection by USDA. Requesting voluntary USDA inspections of dog facilities would not only increase transparency (as summaries of results from USDA inspection reports are posted on a public website), but it would also provide another independent peer review of the VA’s animal care practices and facility compliance from a neutral, independent third party. • Modify dog enclosures and staffing to enhance opportunities for social interaction, exercise, and sensory stimulation. o Ensure staffing is to a level sufficient for all dogs to have 30–45 minutes outside of their primary enclosures 7 days per week. o Deploy a system of adjoining cages with barriers or transfer doors. When the facility is not fully occupied, this type of system would provide the dogs with more space, more behavioral choices, and more opportunities for exercise and could enable compatible dogs to have tactile contact. o To the extent compatible with the needs of studies, maximize the amount of time dogs are able to interact with humans or be let out of their primary enclosures. o When it is compatible with study goals and safe for the dogs and personnel, create an outdoor space for laboratory dogs to visit on a regularly scheduled basis. This would provide additional opportunity for exercise as well as olfactory, sensory, and visual stimulation; a variety of experiences; and time with humans. o Increase the amount of enrichment available to dogs, and continue to evaluate and incorporate new options for environmental enrichment, including olfactory enrichment, on a regularly scheduled basis. • Address current experimental impediments to dog–dog interactions. Prepublication Copy: Uncorrected Proofs 143

Necessity, Use, and Care of Laboratory Dogs at the U.S. Department of Veterans Affairs o Given concerns about possible wounding or damage during the social housing of dogs wearing internal or external (implanted) devices, fund a pilot study at the end of an existing protocol to examine the risk of these outcomes. o Consider an alternative placement of implanted devices to decrease the likelihood of complications from socialization with other dogs. o Encourage the development and use of miniaturized devices that are less cumbersome for the animals and less likely to be damaged, especially if they can be implanted subcutaneously. • Conduct enhanced assessments of laboratory dog welfare. o To move beyond simple observations of dog’s health, VA staff involved in the care and welfare of laboratory dogs should collaborate on continuous education and continuous improvement of measures that advance laboratory dog welfare. o VA veterinary and animal care staff, facilities personnel, members of the institutional animal care and use committee, and principal investigators should conduct formal, written assessments of animal welfare that reflect the state of the art in animal welfare assessment methods. REFERENCES AZA (Association of Zoos and Aquariums). n.d. Accreditation standards. https://www.aza.org/accred- materials (accessed March 23, 2020). Bayne, K. 2002. Development of the human–research animal bond and its impact on animal well-being. ILAR Journal 43(1):4–9. Beaver, B. V., and K. Bayne. 2014. Animal welfare assessment considerations. In K. Bayne and P. V. Turner (eds.), Laboratory animal welfare. London: Elsevier Inc. Pp. 29–38. Belshaw, Z., L. Asher, N. D. Harvey, and R. S. Dean. 2015. Quality of life assessment in domestic dogs: An evidence-based rapid review. Veterinary Journal 206(2):203–212. Bloomsmith, M. A., S. P. Lambeth, A. M. Stone, and G. E. Laule. 1997. Comparing two types of human interaction as enrichment for chimpanzees. American Journal of Primatology 42(2):96. Boissy, A., G. Manteuffel, M. Bak Jensen, R. Oppermann Moe, B. Spruijt, L. J. Keeling, C. Winckler, B. Forkman, I. Dimitrov, J. Langbein, M. Bakken, I. Veissier, and A. Aubert. 2007. Assessment of positive emotions in animals to improve their welfare. Physiology & Behavior 92(3):375–397. Budke, C. M., J. M. Levine, S. C. Kerwin, G. J. Levine, B. F. Hettlich, and M. R. Slater. 2008. Evaluation of a questionnaire for obtaining owner-perceived, weighted quality-of-life assessments for dogs with spinal cord injuries. Journal of the American Veterinary Medical Association 233(6):925–930. Cafazzo, S., L. Maragliano, R. Bonanni, F. Scholl, M. Guarducci, R. Scarcella, M. Di Paolo, D. Pontier, O. Lai, F. Carlevaro, E. Bucci, N. Cerini, L. Carlevaro, L. Alfieri, C. Fantini, and E. Natoli. 2014. Behavioural and physiological indicators of shelter dogs’ welfare: Reflections on the no-kill policy on free-ranging dogs in Italy revisited on the basis of 15 years of implementation. Physiology & Behavior 133:223–229. Campbell, S. A., H. C. Hughes, H. E. Griffin, M. S. Landi, and F. M Mallon. 1988. Some effects of limited exercise on purpose-bred beagles. American Journal of Veterinary Research 49(8):1298–1301. Carlstead, K., S. Paris, and J. L. Brown. 2019. Good keeper–elephant relationships in North American zoos are mutually beneficial to welfare. Applied Animal Behaviour Science 211:103–111. Clark, J. D., D. R. Rager, S. Crowell-Davis, and D. L. Evans. 1997. Housing and exercise of dogs: Effects on behavior, immune function, and cortisol concentration. Laboratory Animal Science 47(5):500–510. Cole, J., and Fraser, D. 2018. Zoo animal welfare: The human dimension. Journal of Applied Animal Welfare Science 21(S1):49–58. 144 Prepublication Copy: Uncorrected Proofs

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For many years, laboratory dogs have served as important animal models for biomedical research that has advanced human health. Conducted at the request of the U.S. Department of Veterans Affairs (VA), this report assesses whether laboratory dogs are or will continue to be necessary for biomedical research related to the VA’s mission. The report concludes that using laboratory dogs in research at the VA is scientifically necessary for only a few areas of current biomedical research. The report recommends that the VA adopt an expanded set of criteria for determining when it is scientifically necessary to use laboratory dogs in VA biomedical research; that the VA promote the development and use of alternatives to laboratory dogs; and highlights opportunities for the VA to enhance the welfare of laboratory dogs that are being used in biomedical research areas for which they have been deemed necessary.

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