1
Introduction
Vertebrate animals have occupied a central role in biomedical research since the early days of medicine, owing to their broad anatomical and physiological similarities to humans. Research on these animals is generally performed to satisfy one of several overarching goals: answer basic questions relevant to the understanding and treatment of human disease; develop and improve on medical interventions, such as surgical procedures; or evaluate the safety and efficacy of drugs, devices, or other therapeutic approaches before they can be tested in humans.
The dog (Canis lupus familiaris) was the first animal species to be domesticated, occurring at least 14,000 and perhaps as far back as 36,000 years ago. Over the millennia humans have bred dogs for multiple uses while selecting them for diverse traits, including sociability and obedience. The ubiquitous presence of dogs and their comfort with humans likely contributed to their use in biomedical research as early as the 1st century CE (Ovodov et al., 2011; Serpell, 2019), and it continues to do so to the present day. Although the precise numbers are unknown, dogs were arguably the primary vertebrate species in use from the late 19th to the mid-20th century (Kinter and DeGeorge, 2016).
In the latter part of the 20th century, mice and rats rapidly replaced dogs in the laboratory, and rodents remain the preferred subjects for the majority of contemporary studies (Franco, 2013). When a process cannot be effectively studied in rodents, then another species will be sought; commonly used species include rabbits, birds, guinea pigs, hamsters, pigs, sheep, non-human primates, cats, and dogs.
Many public and private institutions throughout the United States use animals for biomedical research purposes. The past half-century saw a steep decline in dog use reported by the U.S. Department of Agriculture (USDA), which tallies all dogs used for research in the United States, with 60 percent fewer dogs used in 2017 than in 19731 (USDA APHIS, 2020, n.d.). In the United States in 2017 (the most recent year with complete data when this analysis was initiated in mid-2019), 60,190 dogs were used for biomedical research and testing purposes, according to annual reports submitted to USDA as required by the Animal Welfare Act of 1966 (USDA, 2019). Of these,
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1 B. Juarez, USDA APHIS, personal communication, May 31, 2019.
22,933 dogs were reported by academic institutions and affiliated hospitals engaging in biomedical research and education; 34,875 by companies and private research organizations engaging in applied biomedical research and product development, including testing required by regulatory agencies; 832 by government organizations (including U.S. Department of Veterans Affairs [VA] research labs) conducting priority basic and applied research in support of their missions; and 1,550 by other, non-research groups. A more detailed discussion of USDA data and trends in dog use in research is presented in Appendix B.
The very character traits that make dogs attractive subjects for study also lead to concerns being raised about their use in biomedical research. Public vivisections of dogs elicited strong objections as early as the mid-1700s and inspired the anti-vivisection movement a century later (Patterson-Kane and Golab, 2014). Over a 140-year period leading to the present, a framework of laws and regulations was constructed to prevent the abuse of dogs used in research (see Chapter 2). These regulations also address the particular needs of dogs and other sensitive species (Serpell, 2019).
The VA, as part of its mission to care for America’s veterans, supports and conducts a wide range of preclinical animal research to help advance scientific knowledge and the understanding of how diseases affect veterans (VA, n.d.). The ultimate goal of VA research is to restore or improve the health and well-being of veterans (Bever, 2019; Ramoni, 2019). All animal research performed at the VA is required to comply with the Animal Welfare Act of 1996 and its corresponding animal welfare regulations as well as U.S. Public Health Service policy, and such research is subject to approval and regular inspection by local institutional animal care and use committees (IACUCs). The regulations governing animal use and care at the VA are described in detail in Chapter 2 of this report.
Currently, most VA animal research studies use rodents. In fiscal year (FY) 2017, mice constituted 93 percent and rats 6 percent of all animals used at the VA. That year, a total of 119 dogs were used in VA biomedical research, constituting less than 0.05 percent of all animals used (VA, 2018). For FY 2018, VA animal research programs reported work with 83 dogs in 6 studies. For FY 2019, VA animal research programs reported research conducted with 55 dogs in 6 studies. A seventh study was in progress in FY 2019, but that work is a clinical trial with client-owned dogs (companion animals), which USDA reporting requirements exclude.
ORIGIN OF THIS STUDY
Although the use of animals in biomedical research is regulated by federal laws and is subject to institutional oversight to ensure the humane use and care of laboratory animals, this practice remains a contentious issue and a focus of intense public scrutiny, particularly in the case of dogs. In May 2017, reporting on an animal use protocol for an invasive study performed on dogs at the Greater Los Angeles VA facility found that the study had been mischaracterized as observational, leading some members of the U.S. Congress to question the transparency of VA-supported dog research and to further investigate dog research in the Greater Los Angeles VA facility (Garcia, 2017; Titus et al., 2017; Wire, 2016).
Also in May 2017, the VA Office of Research Oversight (ORO) reported on its investigation, Canine Research Studies and Associated Facility Oversight, carried out at the Hunter Holmes McGuire VA Medical Center (HHMGVAMC) in Richmond, Virginia, which had been undertaken to address seven allegations referred by the Office of Inspector General (VA ORO, 2017). The ORO substantiated three allegations relating to animal welfare, all of which had been previously self-identified and reported by VA personnel, with corrective actions taken by the local IACUC. The ORO made additional findings related to deficient recordkeeping, non-adherence to provisions of the facility’s written program of veterinary care, and deviations from approved study procedures without prior IACUC approval. The HHMGVAMC took corrective actions to address these findings (VA, 2017). In the January 2019 Report on the Office of Laboratory Animal Welfare Site
Visits to the Veterans Affairs Medical Centers with Focus on Canine Care and Use in Research, the National Institutes of Health’s Office of Laboratory Animal Welfare found that the HHMGVAMC “responded appropriately to the allegations of animal welfare concerns, recordkeeping and reporting inconsistencies” and “not only executed and implemented, but has consistently maintained, the appropriate corrective measures in response to the animal welfare concerns” (OLAW, 2019).
In December 2017 the VA required all research projects using dogs to undergo a secondary review by the Office of the Chief Veterinary Medical Officer after the initial review by the local IACUC, followed by additional reviews by senior Veterans Health Administration managers (VHA, 2018). Section 254 of the Consolidated Appropriations Act of 2018 (Public Law 115-141) included a stipulation that no new canine research could begin at the VA unless it was directly approved by the VA Secretary.2
In March 2018 the VA announced its intention to conduct an in-depth internal review of existing canine research projects (VA OPIA, 2018). The VA requested the National Academies of Sciences, Engineering, and Medicine (the National Academies) to convene an ad hoc committee that would conduct an independent assessment of whether dogs are or will continue to be necessary for any type of biomedical research directly related to the VA’s mission. The charge to the committee is presented in Box 1-1. Note that non-human primates were excluded from the committee’s consideration according to the Statement of Task.
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2 Consolidated Appropriations Act of 2018, H.R. 1625, 115th Cong., 2nd sess. (January 3, 2018). Available at https://www.congress.gov/115/bills/hr1625/BILLS-115hr1625enr.xml (accessed June 25, 2019).
RECENT LEGISLATION CONCERNING THE USE OF LABORATORY DOGS AT THE VA
On December 20, 2019, roughly 1 year after this committee was convened, additional constraints were placed on the use of dogs in biomedical research at the VA by the U.S. Congress, as detailed in Section 249 of the Further Consolidated Appropriations Act of 2020.3 This regulation placed further restrictions on the ability of the Secretary of the VA to approve research using “canines, felines, or non-human primates,” again limiting their use to conditions where “the scientific objectives of the research can only be met” by using these animals. The additional constraint was added that these animals could only be used where “such scientific objectives are directly related to an illness or injury that is combat-related.” In addition, the legislation requires the VA Secretary to personally report all new research on canines, felines, or non-human primates to the U.S. Congress, with continued biannual reporting, and to submit a plan by December 31, 2020, for eliminating or reducing research on these species over the next 5 years.
The committee notes that the legislation raises three points of particular significance for its work:
- While the committee was charged with considering the necessity of dog use “related to the VA’s mission,” the legislation restricts dog use to research that is “directly related to an illness or injury that is combat-related.” The stated mission of the VA is “[t]o fulfill President Lincoln’s promise ‘To care for him who shall have borne the battle, and for his widow, and his orphan’ by serving and honoring the men and women who are America’s Veterans.” The VA is charged with providing health care to veterans throughout their life span, and it engages in research that supports this charge, including research on cardiovascular disease, cancer, diabetes, and a range of other disorders that may no longer be eligible for study in dogs under this new legislation (see Chapter 3 for a discussion of ways in which dogs have historically been used at the VA). Likewise, the use of naturally infected military dogs to study infectious diseases that both dogs and soldiers contract during deployments overseas (also discussed in Chapter 3) may not be permissible under this stipulation.
- The legislation does not distinguish between the use of laboratory dogs and the use of companion (pet) dogs in biomedical research. Unlike laboratory dogs, companion dogs have naturally occurring diseases or injuries, are volunteered by their owners, and stand to benefit from the results of the research. Public interest in and support for companion dog studies is generally high. The committee’s recommendations rely heavily on the ability of the VA to move research from laboratory dogs to companion dogs where feasible as well as to find novel opportunities to engage in companion dog research where it would satisfy the VA’s mission.
- By restricting dog use to situations in which the scientific objective can only be met by using dogs, the legislation privileges dogs over other large mammals, such as pigs. In other words, VA researchers are required to use other animal species in all cases where the scientific objectives of the research can be met using other species as well as dogs. This is the case even when the particular scientific question could be addressed using fewer dogs than, for example, pigs, or would cause less harm to dogs than to pigs. Choosing to use pigs instead of dogs under these circumstances would constitute a potential contradiction of the Three Rs (reduce, refine, replace) that are used to guide ethical decisions in animal research and discussed in depth in Chapter 2.
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3 Further Consolidated Appropriations Act of 2020, H.R. 1865, 116th Cong., 1st sess. (January 3, 2019). Available at https://www.congress.gov/bill/116th-congress/house-bill/1865 (accessed January 24, 2020).
STUDY PROCESS
A Statement of Task guides each National Academies study and determines what kinds of expertise are needed on a committee. A committee writes a report to answer as rigorously as possible the questions posed in the Statement of Task.
Committee Formation
Members of the committee that conducted this study4 were selected from among more than 100 persons nominated during the committee-formation phase of the study. Individuals appointed to the committee were chosen for their individual expertise and the relevance of their experience and knowledge to the Statement of Task (see Box 1-1), not their affiliation with any institution. All committee members volunteer their time to serve on a study. Areas of expertise represented on the committee included laboratory animal veterinary medicine, biomedical sciences, medicine, translational research, animal welfare science, animal welfare regulation, bioethics, and animal law. Biographies of the committee members are in Appendix C.
Public Input
As with all National Academies studies, members of the public were invited to provide oral or written statements and information to the committee, especially during the information-gathering phase of the study. The in-person meetings held in Washington, DC, in December 2018, February 2019, and March 2019 included time for members of the public to provide comments to the committee. Recordings of the public comment sessions are archived on the study’s website.5
Written comments to the committee could be submitted at any point during the study process. Comments and information could be delivered to National Academies staff at committee meetings and via email. Members of the public could also submit comments or upload relevant documents to the study’s website. More than 4,100 comments and documents were submitted to the committee, and the committee read all of them.
Some commenters told the committee in written statements or at its public meetings that the committee should make a decisive pronouncement endorsing the use of dogs in biomedical research as categorically beneficial. Others encouraged the committee to denounce the use of dogs in biomedical research. Comments were also submitted with literature on non-animal approaches, welfare, transparency in research, and the use of dogs in biomedical research.
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4 Every National Academies committee is provisional until the appointed members have had an opportunity to discuss as a group their points of view and any potential conflicts of interest related to the Statement of Task. They also determine whether the committee is missing expertise that may be necessary to answer questions in the Statement of Task. As part of their discussion, committee members consider comments submitted by the public about the committee’s composition. The discussion takes place during the first in-person meeting of the committee. The committee is no longer provisional when it has determined that no one with an avoidable conflict of interest is serving on the committee and that its membership has the necessary expertise to address the Statement of Task.
The committee is no longer provisional when it has determined that no one with an avoidable conflict of interest is serving on the committee and that its membership has the necessary expertise to address the Statement of Task. The Committee on Assessment of the Use and Care of Dogs in Biomedical Research Funded by or Conducted at the U.S. Department of Veterans Affairs did not identify any conflicts of interest among its members. However, in light of comments received from the public before its first meeting and because of two resignations, two new members with experience as American College of Laboratory Animal Medicine board-certified veterinarians and with service on an institutional animal care and use committee, one member with animal research ethics and law experience, and two members with biomedical research experience were added to the committee.
For more information about the National Academies study process, including definitions and procedures related to points of view and conflicts of interest, visit http://www.nationalacademies.org/studyprocess (accessed January 8, 2020).
5 The study website includes recordings of public sessions; see https://www.nationalacademies.org/our-work/assessment-of-the-care-and-use-of-dogs-in-biomedical-research-funded-by-or-conducted-at-the-us-department-of-veterans-affairs (accessed June 16, 2020).
To address the Statement of Task, the committee drew on information presented during public meetings, webinars, and the workshop. The committee typically requested additional data or documentation from invited speakers following their presentations. It also reviewed statements and articles that were submitted or referred to by speakers or members of the public, and it thoroughly consulted the relevant peer-reviewed scientific literature.
Committee Deliberations and Information-Gathering Activities
To address the study charge, the committee deliberated from December 2018 to December 2019, holding six meetings (five meetings in Washington, DC, and one in Woods Hole, Massachusetts), including one 2-day public workshop (March 27–28, 2019, in Washington, DC), public comment sessions (during the open sessions of four committee meetings), and two webinars (May 7, 2019, and May 28, 2019). Agendas for the committee meeting open sessions, 2-day workshop, and webinars are included in Appendix A. Subgroups of the committee with expertise in laboratory animal care and welfare also visited facilities conducting VA-funded research in Richmond, Virginia (August 20, 2019), and St. Louis, Missouri (November 14, 2019). Throughout the study, the committee also received input from interested stakeholders and the public via the study website. All submitted comments and documents were added to the study’s public access file, which is available on request from the National Academies’ Public Access Records Office. Requests can be directed to PARO@nas.edu.
Information from the VA
The VA submitted several documents to the committee during the course of the study, including information surrounding 14 biomedical research protocols. For each of the 14 protocols, the VA included the animal component of research protocol form, a secondary review form, and a summary of the literature search done by the Office of the Chief Veterinary Medical Officer. The VA also submitted summaries of 30 past research projects involving dogs as well as representative publications from 28 of these projects ranging in date from 1960 to 2018. To evaluate the impact of this research, the committee reviewed the scientific literature in the decade 2009–2018, with the goal of understanding the contribution of past VA research involving dogs to clinical questions related to the VA’s mission. A list of all the documents provided by the VA can be found in Appendix A of this report.
Adding to the information in the documents received from the VA, several public sessions allowed the committee to delve further into the context for the study and the Statement of Task as provided by the VA. During open sessions, VA representatives discussed the relevance of dog research to the VA’s mission and current procedures for evaluating and monitoring dog use and care (December 9, 2018); addressed follow-up questions from the committee in writing and in person (February 14, 2019); and described the procedure for internal review and funding of research grants (March 28, 2019). Video recordings and slides from all VA presentations are publicly available from the study website.6
Report Review Process
The concluding phase of a National Academies report is the review process. When a draft report is complete, it is submitted to the National Academies’ Report Review Committee (RRC).
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6 The study website includes recordings of public sessions; see https://www.nationalacademies.org/our-work/assessment-of-the-care-and-use-of-dogs-in-biomedical-research-funded-by-or-conducted-at-the-us-department-of-veterans-affairs (accessed June 16, 2020).
The RRC recruits a diverse and critical group of reviewers who have expertise complementary to that of the committee to ensure that critical gaps and misinformation are identified. The reviewers are anonymous to the committee during the review process, and their comments remain anonymous after the report is published (see the Reviewers section on p. vii). Reviewers are asked to assess how well a report addresses a study’s Statement of Task. The committee must respond to, but need not agree with, reviewers’ comments in a detailed “response to review” that is examined by one or two independent report review “monitors” responsible for ensuring that the report review criteria have been satisfied. When the RRC decides that the committee has adequately and appropriately addressed the reviewers’ comments, the report is ready to be released to the public and to the sponsor.
THE COMMITTEE’S INTERPRETATION OF ITS TASK
In this study, the committee addressed the care and use of laboratory-housed dogs and not of privately-owned companion dogs enrolled in clinical trials. In accordance with the committee’s charge, recommendations contained in this report focus on the committee’s determination as to whether laboratory dogs are or will continue to be necessary for biomedical research conducted at or funded by the VA.
As one component of its effort to understand the procedures governing animal care and use at the VA and the scientific justification for undertaking research in dogs, the committee reviewed elements of research protocols provided by the VA. With a few exceptions as noted in the text, this report does not critique individual protocols.
The committee supplemented information from the VA panels with a review of the current scientific literature regarding clinical questions related to the VA’s mission that have traditionally used dogs, taking into account both animal and non-animal alternatives to laboratory dog use (see the literature search parameters in Appendix A). In applying expert opinion to the issues raised in the study charge, the committee was guided by scientific, social, regulatory, and ethical considerations.
TERMINOLOGY USED IN THIS REPORT
The committee was faced with competing terminologies for describing the analytical process that weighs the risk of harm to laboratory dogs against the potential benefit of the research to humans—specifically, it had to choose between the terms “harm–benefit analysis” and “risk–benefit analysis.” The semantics remain a topic of continuing debate among many stakeholders; Box 1-2 offers a brief background and explanation of the committee’s decision. Ultimately, the committee decided to use “harm–benefit analysis” in this report in order to be consistent with the terminology used in VA documents (see Box 1-2). It was beyond the scope of this committee’s work to make a determination regarding the scientific, ethical, and regulatory merit of the competing terminologies, and the use of “harm–benefit analysis” in this report should not be construed as a recommendation of this committee, the Institute for Laboratory Animal Research, or the National Academies.
ORGANIZATION OF THE REPORT
To produce this report, the committee identified scientific, social, legal, and ethical considerations; regulatory requirements; and currently accepted standards guiding the use, care, and welfare of laboratory dogs at the VA (Chapter 2). After surveying past and current dog use in biomedical research in fields relevant to the VA mission and reviewing current and recent dog protocols at the VA, the committee established criteria to guide the decisions of whether and how to use laboratory dogs in biomedical research at the VA (Chapter 3). The committee then
reviewed current and likely future alternatives to the use of laboratory dogs in fields relevant to the VA mission (Chapter 4). Finally, the committee evaluated current review and oversight practices governing laboratory dog care at the VA and made recommendations to enhance the care and welfare of dogs in VA facilities (Chapter 5).
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