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A Belmont Report for Animals?

  • HOPE FERDOWSIAN, L. SYD M JOHNSON, JANE JOHNSON, ANDREW FENTON, ADAM SHRIVER and JOHN GLUCK...
  • Please note a correction has been issued for this article.

Abstract:

Human and animal research both operate within established standards. In the United States, criticism of the human research environment and recorded abuses of human research subjects served as the impetus for the establishment of the National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research, and the resulting Belmont Report. The Belmont Report established key ethical principles to which human research should adhere: respect for autonomy, obligations to beneficence and justice, and special protections for vulnerable individuals and populations. While current guidelines appropriately aim to protect the individual interests of human participants in research, no similar, comprehensive, and principled effort has addressed the use of (nonhuman) animals in research. Although published policies regarding animal research provide relevant regulatory guidance, the lack of a fundamental effort to explore the ethical issues and principles that should guide decisions about the potential use of animals in research has led to unclear and disparate policies. Here, we explore how the ethical principles outlined in the Belmont Report could be applied consistently to animals. We describe how concepts such as respect for autonomy and obligations to beneficence and justice could be applied to animals, as well as how animals are entitled to special protections as a result of their vulnerability.

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Copyright

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Footnotes

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Adam Shriver’s work on this project is supported by Wellcome Trust grant 203132/Z/16/Z.

The section title was incorrectly listed as “Guest Editorial” in the original online version of this article. This will be corrected in print and an erratum will be published.

Footnotes

References

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Notes

1. HHS Common Rule. 45 C.F.R. § 46.111(3).

2. Beecher, HK. Ethics and clinical research. New England Journal of Medicine 1966;274:1354–60.

3. U.S. Public Health Service Syphilis Study at Tuskegee. Centers for Disease Control and Prevention 2015 Dec 22; available at https://www.cdc.gov/tuskegee/timeline.htm (last accessed 30 Nov 2017).

4. 7 U.S.C. §§ 2131–2159 (1966), as amended.

5. Ferdowsian, HR, Gluck, JP. The ethical challenges of animal research: Honoring Henry Beecher’s approach to moral problems. Cambridge Quarterly of Healthcare Ethics 2015;24(4):391406.

6. See note 4, 7 U.S.C. §§ 2131–2159 (1966), as amended.

7. National Research Council Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the Care and Use of Laboratory Animals, 8th ed. Washington, DC: National Academies Press; 2011.

8. Beauchamp, TL, Childress, JF. Principles of Biomedical Ethics, 7th ed. New York, NY: Oxford University Press; 2012.

9. Russell, WMS, Burch, RL. The Principles of Humane Experimental Technique. London, UK: Methuen & Co., Ltd; 1959.

10. National Centre for the Replacement, Refinement, and Reduction of Animals in Research. What Are the 3Rs?; available at https://www.nc3rs.org.uk/the-3rs (last accessed 30 Nov 2017).

11. Canadian Council on Animal Care. Three Rs Microsite: About the 3 Rs; available at http://3rs.ccac.ca/en/about/three-rs.html (last accessed 30 Nov 2017).

12. UK Government Home Office. Guidance: Animal Testing and Research; available at https://www.gov.uk/guidance/research-and-testing-using-animals (last accessed 30 Nov 2017).

13. Australian Government National Health and Medical Research Council. Guidelines to Promote the Wellbeing of Animals Used for Scientific Purposes: The Assessment and Alleviation of Pain and Distress in Research Animals; available at https://www.deakin.edu.au/__data/assets/pdf_file/0004/536629/nhmrc-pain-and-distress-pdf.pdf (last accessed 30 Nov 2017).

14. Houde, L, Dumas, C. An ethical analysis of the 3Rs. Between the Species 2007:7; available at https://digitalcommons.calpoly.edu/bts/vol13/iss7/.

15. Beauchamp, TL, Ferdowsian, HR, Gluck, J. Where are we in the justification of research involving chimpanzees? Kennedy Institute of Ethics Journal 2012;22:211–42.

16. National Research Council. Chimpanzees in Biomedical and Behavioral Research: Assessing the Necessity. Washington, DC: The National Academies Press; 2011.

17. Collins FS. NIH Will No Longer Support Biomedical Research on Chimpanzees 17 Nov 2015; available at https://www.nih.gov/about-nih/who-we-are/nih-director/statements/nih-will-no-longer-support-biomedical-research-chimpanzees (last accessed 30 Nov 2017). See also Reardon, S. NIH to retire all research chimpanzees: Fifty animals held in “reserve” by the US government will be sent to sanctuaries. Nature 18 Nov 2015; available at https://www.nature.com/news/nih-to-retire-all-research-chimpanzees-1.18817 (last accessed 30 Nov 2017).

18. Booker Legislation Seeks to End Unethical and Unnecessary Testing on Primates, Press Release, December 18, 2018; available at https://www.booker.senate.gov/?p=press_release&id=873 (last accessed 8 Jan 2019).

19. Grimm, D. Decision to end monkey experiments based on finances, not animal rights. Science Magazine 2015 Dec 14; available at https://www.sciencemag.org/news/2015/12/decision-end-monkey-experiments-based-finances-not-animal-rights-nih-says (last accessed 8 Jan 2019).

20. Strauss, M. Americans are divided over the use of animals in scientific research. Pew Research 2018 Aug 16; available at http://www.pewresearch.org/fact-tank/2018/08/16/americans-are-divided-over-the-use-of-animals-in-scientific-research/ (last accessed 8 Jan 2019).

21. Riffkin, R. In U.S., more say animals should have same rights as people. Gallup 2015 May 18; available at https://news.gallup.com/poll/183275/say-animals-rights-people.aspx (last accessed 8 Jan 2019).

22. CBC News. Safe Haven for Chimps: Canada’s Position on Chimpanzees in Research; available at http://www.cbc.ca/natureofthings/features/using-chimps-for-research-in-canada (last accessed 2 Feb 2018).

23. Weatherall, D. The Use of Non-Human Primates in Research: A Working Group Report Chaired by Sir David Weatherall FRS FMedSci 12 Dec 2006; available at https://royalsociety.org/topics-policy/publications/2006/weatherall-report/ (last accessed 30 Nov 2017).

24. European Commission Scientific Committee on Health and Environmental Risks (SCHER). The Need for Non-Human Primates in Biomedical Research, Production and Testing of Products and Devices 18 May 2017; available at https://ec.europa.eu/health/sites/health/files/scientific_committees/scheer/docs/scheer_o_004.pdf (last accessed 30 Nov 2017).

25. The Sundowner Report represents perhaps the most substantive attempt by a U.S. agency to create ethical principles for animal research. In 1996, it established three principles to guide decisions about the use of animals by the National Aeronautics and Space Administration (NASA): respect for life, societal benefit, and nonmaleficence. However, the report did not offer a clear defense for or specific applications of its principles, including how the interests of individual animals should be weighed in decisions about their inclusion in research. See National Aeronautics and Space Administration. 1996 Principles for the Ethical Care and Use of Animals – Sundowner Report; available at http://www.iacuc.ucsf.edu/Links/awSundwnr.asp (last accessed 30 Nov 2017). Outside the U.S., some guidelines have incorporated noteworthy but vague language about “respect for” the “dignity of” animals; however, questions about the interpretation and application of these concepts remain. Furthermore, these principles have not been widely applied to decisions about the use of animals in research. See Australian Government National Health and Medical Research Council. Australian Code for the Care and Use of Animals for Scientific Purposes, 8th ed. (2013); available at https://www.nhmrc.gov.au/guidelines-publications/ea28 (last accessed 30 Nov 2017). See also Schindler, S. The animal’s dignity in Swiss Animal Welfare Legislation--challenges and opportunities. European Journal of Pharmaceutics and Biopharmaceutics 2013;84(2):251–4.

26. See note 5, Ferdowsian, Gluck 2015;24:391–406.

27. Gruen L. The moral status of animals. Stanford Encyclopedia of Philosophy 2017 Aug 23; available at https://plato.stanford.edu/entries/moral-animal/ (last accessed 8 Jan 2019). See also Singer, P. Practical Ethics. Cambridge, UK: Cambridge University Press; 2011. See also Choe Smith CU. Confronting ethical permissibility in animal research: Rejecting a common assumption and extending a principle of justice. Theoretical Medical Bioethics 2014;35:175–85.

28. Ferdowsian, H, Choe, C. Extending human research protections to non-human animals. In: Corbey, R, Lanjouw, A. The Politics of Species: Reshaping Our Relationships with Other Animals. Cambridge, UK: Cambridge University Press; 2013, 232–40. See also Ferdowsian, H. Phoenix Zones: Where Strength Is Born and Resilience Lives. Chicago, IL: The University of Chicago Press; 2018.

29. Fenton, A. Decisional authority and animal research subjects. In: Andrews, K, Beck, J, eds. The Routledge Handbook of Philosophy of Animal Minds. New York, NY: Routledge; 2018, 475–84.

30. See note 28, Ferdowsian, Choe 2013, 232–40. See also note 28, Ferdowsian 2018.

31. There are noteworthy dissimilarities between the human and animal research environments. The Belmont Report, like the Declaration of Helsinki and Nuremberg Code, focuses on one species: humans. Efforts to create a similar document for all other animals may appear difficult. In our discussion, we foreground interests and vulnerabilities that can reasonably and broadly be ascribed to many animals. This approach allows for anticipated gains in knowledge about other species, as well as corresponding societal changes in how animal research is perceived, and evolving critical ethical discourse.

32. Tom Beauchamp, who drafted the Belmont Report for the Commission, has speculated that the Commission selected “respect for persons” as its first principle to indicate a level of moral status associated with personhood. See Public Responsibility in Medicine and Research. People & Perspectives: Tom Beauchamp, PhD - (Excerpt) Reflections on "Respect for Persons" 17 Nov 2014; available at https://www.youtube.com/watch?v=v2hrMWEmQLw (last accessed 30 Nov 2017). There is still no agreed upon list of capacities for personhood favored by contemporary philosophers; see Andrews K. The Animal Mind: An Introduction to the Philosophy of Animal Cognition. New York, NY: Routledge; 2015. Although, many tend to favor capacities like “autonomy, rationality, self-awareness, linguistic competence, sociability, moral agency, and the capacity for intentional action”; see DeGrazia D. Human-animal chimeras: Human dignity, moral status, and species prejudice. Metaphilosophy 2007;38(2–3):309–29. However, a commitment to the personhood (and not just the potential personhood) of toddlers, many neuro-diverse humans as well as humans with neurodegenerative disorders, cautions against strongly favoring any capacities from this list as jointly necessary. Though this opens a door to the personhood of other animals who possess a number of the same capacities, a lack of consensus on the necessary capacities for personhood leaves this, at present, an unresolved issue. It is possible that a principle such as “respect for bodily sovereignty,” which summarily includes respect for bodily liberty and integrity, as recognized in human rights law, would have been more appropriate for what the National Commission intended. Such a principle could also be applied to the case of animals.

33. National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research. The Belmont Report 18 April 1979; Washington, DC: US Department of Health, and Human Services; available at https://www.hhs.gov/ohrp/regulations-and-policy/belmont-report/index.html (last accessed 30 Nov 2017). See Belmont Report, Pt. (B)(1).

34. See note 8, Beauchamp, Childress 2012. See also Beauchamp, TL, Wobber, V. Autonomy in chimpanzees. Theoretical Medicine and Bioethics 2014;35:117–32. See also Pierce, J. Animals and autonomy. Psychology Today 10 Mar 2013; available at https://www.psychologytoday.com/blog/all-dogs-go-heaven/201303/animals-and-autonomy (last accessed 30 Nov 2017).

35. de Waal, FBM, Tyack, PL, eds. Animal Social Complexity: Intelligence, Culture, and Individualized Societies. Cambridge, UK: Harvard University Press; 2003. See also Safina, C. Beyond Words: What Animals Think and Feel. New York, NY: Henry Holt and Co.; 2015; and Emery, N. Bird Brain: An Exploration of Avian Intelligence. Princeton, NJ: Princeton University Press; 2016.

36. See note 35, de Waal, Tyack 2003.

37. van Noordwijk, MA. From maternal investment to lifetime maternal care. In: Mitani, JC, Call, J, Kappeler, PM, Polombit, RA, Silk, JB, eds. The Evolution of Primate Societies. Chicago, IL: University of Chicago Press; 2012. See also Kuczaj, SA II, Winship, KA. How do dolphin calves make sense of their world? In: Herzing, DL, Johnson, CM, eds. Dolphin Communication and Cognition: Past, Present, and Future. Cambridge, UK: The MIT Press; 2015, 201–26.

38. Gregory, NG. Physiology and Behavior of Animal Suffering. Oxford, UK: Blackwell Science; 2004. See also McMillan, F, ed. Mental Health and Well-Being in Animals, 1st edition. Ames, IA: Blackwell Publishing; 2005. See also Panksepp, J. Affective Neuroscience: The Foundations of Human and Animal Emotions. New York, NY: Oxford University Press; 2004.

39. See note 33, National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research 1979, Pt. (B)(1).

40. Perlman, JE, Bloomsmith, MA, Whittaker, MA, McMillan, JL, Minier, DE, McCowan, B. Implementing positive reinforcement animal training programs at primate laboratories. Applied Animal Behaviour Science 2012;137:114–26.

41. Information should include “the research procedure, their purposes, risks and anticipated benefits, alternative procedures (where therapy is involved), and a statement offering the subject the opportunity to ask questions and to withdraw at any time from the research.” Information should be adapted to meet the subject’s capacities, and this obligation increases as risks to the individual become more serious. See note 33, Belmont Report 1979, Pt. (C)(1).

42. See note 33, National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research 1979, Pt. (C)(1).

43. See note 33, National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research 1979, Pt. (C)(1).

44. Diekema, DS. Conducting ethical research in pediatrics: A brief historical overview and review of pediatric regulations. The Journal of Pediatrics 2006;149:S3–11. See also Wendler, D. Assent in pediatric research: Theoretical and practical considerations. Journal of Medical Ethics 2006;32:229–34.

45. Fenton, A. Can a chimp say “no”? Reenvisioning chimpanzee dissent in harmful research. Cambridge Quarterly of Healthcare Ethics 2014;23(2):130–9.

46. See note 29, Fenton 2018.

47. See note 34, Beauchamp, Wobber 2014. See also Kantin, H, Wendler, D. Is there a role for assent or dissent in animal research? Cambridge Quarterly of Healthcare Ethics 2015;24(4):459–72. See also note 29, Fenton 2018.

48. See note 33, National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research 1979, Pt. (B)(2).

49. Bennett, AJ. New era for chimpanzee research: Broad implications of chimpanzee research decisions. Developmental Psychobiology 2015;57:279–88.

50. Pound, P, Nicol, CJ. Retrospective harm benefit analysis of pre-clinical animal research for six treatment interventions. PloS ONE 2018;13:e0193758.

51. See note 7, National Research Council Committee for the Update of the Guide for the Care and Use of Laboratory Animals 2012, at 27.

52. Brønstad A, Newcomer CE, Decelle T, Everitt JI, Guillen J, Laber K. Current concepts of harm–benefit analysis of animal experiments–report from the AALAS–FELASA working group on harm–benefit analysis–part 1. Laboratory Animals 2016;50(1_suppl):1–20. See also Laber, K, Newcomer, CE, Decelle, T, Everitt, JI, Guillen, J, Brønstad, A. Recommendations for addressing harm–benefit analysis and implementation in ethical evaluation–Report from the AALAS–FELASA working group on harm–benefit analysis–part 2. Laboratory Animals 2016;50(1_suppl):2142.

53. Olsson, IAS, Silva, SPD, Townend, D, Sandøe, P. Protecting animals and enabling research in the European Union: An overview of development and implementation of directive 2010/63/EU. ILAR Journal 2016;57(3):347–57.

54. Many applied ethicists understand harm to consist of a setback to interests that an individual would not otherwise experience arising from the actions or omissions of another or a naturally occurring event. When animals are killed, they often experience a setback to their interests as described here. Their death, in such circumstances, constitutes harm.

55. Gruen, L, ed. The Ethics of Captivity. Oxford, UK: Oxford University Press; 2014.

56. Many animals are capable of feeling pain and experience the same types of nociceptive and neuropathic pain as humans. They experience pain and discomfort associated with disease (also called “sickness behavior”), which can result in lethargy, depression, anorexia, reduced bodily care and grooming, sleep disturbances, and enhanced sensitivity to pain. See Dantzer R, Kelley KW. Twenty years of research on cytokine-induced sickness behavior. Brain, Behavior, and Immunity 2007;21:153–160. Additionally, when deprived of a normal life, many animals can experience mental disorders like anxiety disorders, posttraumatic stress disorder, and mood disorders, such as depression. It is also possible that some animals, as well as some humans, are more vulnerable to suffering because of their inability to make sense of their plight, or to escape, or alter their circumstances. The absence of maturation of certain neurological structures might also affect the capacity for suffering, if associated with less flexibility and more limited coping mechanisms. See Varner GE. Personhood, Ethics, and Animal Cognition: Situating Animals in Hare’s Two Level Utilitarianism. Oxford, UK: Oxford University Press; 2012. See also Akhtar, S. Animal pain and welfare: Can pain sometimes be worse for them than for us? In: Beauchamp, TL, Frey, RG, eds. The Oxford Handbook of Animal Ethics. New York: Oxford University Press; 2011:495518; Ferdowsian, HR, Merskin, D. Parallels in trauma, pain, distress, and suffering in humans and nonhuman animals. Journal of Trauma and Dissociation 2012;13:448–69; and note 50, Pound, Nicol 2018.

57. See note 33, National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research 1979, Pt. (C)(2).

58. This statement applies even when allowing for current veterinary medical research.

59. See note 33, National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research 1979, Pt. (C)(2).

60. Although the concept of replacement is meant to prompt consideration of alternative research methods, this often does not occur in practice.

61. See note 27, Singer 2011. See also Satz, A. Animals as vulnerable subjects: Beyond interest-convergence, hierarchy, and property. Animal Law 2009;16:150.

62. See Akhtar, A. The flaws and human harms of animal experimentation. Cambridge Quarterly of Healthcare Ethics 2015;24(4):407–19.

63. See note 33, National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research 1979, Pt. (C)(3).

64. See Lederer, SE. Subjected to Science. Baltimore, MD: The Johns Hopkins University Press; 1995. See also The Final Report of the Advisory Committee on Human Radiation Experiments. The Human Radiation Experiments. New York, NY: Oxford University Press; 1996.

65. See note 33, National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research 1979, Pt. (B)(3).

66. See note 33, National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research 1979, Pt. (C)(3).

67. See note 33, National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research 1979, Pt. (B)(3).

68. See note 33, National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research 1979, Pt. (B)(3).

69. See note 33, National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research 1979, Pt. (C)(3).

70. Council for the International Organizations of Medical Sciences. International Ethical Guidelines for Health-Related Research Involving Humans. Geneva, Switzerland: Council for the International Organizations of Medical Sciences; 2016, Guideline 15; available at https://cioms.ch/wp-content/uploads/2017/01/WEB-CIOMS-EthicalGuidelines.pdf (last accessed 30 Nov 2017).

71. CIOMS does not include animals within its expansive list of vulnerable subjects. See Council for the International Organizations of Medical Sciences. International Ethical Guidelines for Biomedical Research Involving Human Subjects. Geneva, Switzerland: Council for the International Organizations of Medical Sciences; 2002, Guideline 13; available at https://cioms.ch/shop/product/international-ethical-guidelines-for-biomedical-research-involving-human-subjects-2/ (last accessed 30 Nov 2017). If we take the understanding of vulnerability provided by CIOMS seriously, however, and consider evidence that this kind of vulnerability is not bounded by species, then animals are vulnerable in the same ways that many humans are vulnerable. Importantly, CIOMS applies the concept of vulnerability to individuals, not to groups. Some individuals within less vulnerable groups are still particularly vulnerable. This is an important point with respect to animals. While animals living in their natural environments might have vulnerabilities (to predation, weather, famine, etc.), they are not vulnerable in the way that their captive conspecifics are. A captive animal in a laboratory is (generally) protected from weather and food shortages, but is vulnerable in other ways specific to captivity and use in research—such as pain, death, loss of autonomy and freedom, loss of social group and family, etc.

72. Johnson, J. Vulnerable subjects? The case of nonhuman animals in experimentation. Journal of Bioethical Inquiry 2013;10:497504.

73. Mackenzie, C, Rogers, W, Dodds, S. Introduction: What is vulnerability and why should it matter for moral theory. In: Mackenzie, C, Rogers, W, Dodds, S, eds. Vulnerability: New Essays in Ethics and Feminist Philosophy. New York, NY: Oxford University Press; 2014, at 129.

74. Choe Smith, C. Confronting ethical permissibility in animal research: Rejecting a common assumption and extending a principle of justice. Theoretical Medicine and Bioethics 2014;35:175–85. See also note 61, Satz 2009.

75. See note 33, National Commission for the Protection of Human Subjects of Biomedical and Behavioral Research 1979, B(2).

76. See note 1, 45 CFR 46 §46.407.

77. Wendler, D. Should protections for research with humans who cannot consent apply to research with nonhuman primates? Theoretical Medicine and Bioethics 2014;35:157173.

78. There is a fundamental problem of knowing another mind. See Nagel, T. What is it like to be a bat? Philosophical Review 1974;83:435–50. Recent ideas about “embodied cognition” provide further empirical grounding to this philosophical question. See also note 32, Andrews 2016.

79. Some scientists might also fall in this category. For example, Marc Bekoff, Nathan Emery, Jane Goodall, and Tetsuro Matsuzawa, who have observed animals for extended periods, also come to know many of these animals, their individual personalities, desires, and interests well.

80. Ferdowsian, HR, Fuentes, A. Harms and deprivation of benefits for nonhuman primates in research. Theoretical Medicine and Bioethics 2014;35:143–56.

81. Johnson, J, Degeling, C. Animals-as-patients: Improving the practice of animal experimentation. Between the Species 2012;15(1):4358, at 44.

82. Such an approach would frequently resemble the way human research subjects live during their research participation, which may have the added benefit of improving the translatability of research.

Adam Shriver’s work on this project is supported by Wellcome Trust grant 203132/Z/16/Z.

The section title was incorrectly listed as “Guest Editorial” in the original online version of this article. This will be corrected in print and an erratum will be published.

A Belmont Report for Animals?

  • HOPE FERDOWSIAN, L. SYD M JOHNSON, JANE JOHNSON, ANDREW FENTON, ADAM SHRIVER and JOHN GLUCK...
  • Please note a correction has been issued for this article.

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