Ferdowsian, Hope

Fuentes, Agustin

Johnson, L. Syd M.

King, Barbara J.

Pierce, Jessica

PhilPapers

ARTICLEToward an Anti-Maleficent Research AgendaHope Ferdowsian1*, Agustin Fuentes2, L. Syd M Johnson3, Barbara J. King4 and Jessica Pierce51Department of Medicine, University of New Mexico School of Medicine, Albuquerque, New Mexico 87106, USA2Department of Anthropology, Princeton University, Princeton, New Jersey 08544, USA3Center for Bioethics and Humanities, Upstate Medical University, Syracuse, New York 13210, USA4Department of Anthropology, William & Mary, Williamsburg, Virginia 23187, USA5Center for Bioethics and Humanities, University of Colorado Anschutz Medical Campus, Aurora, Colorado 80045, USA*Corresponding author: Email. hferdowsian@salud.unm.eduAbstractImportant advances in biomedical and behavioral research ethics have occurred over the past few decades,many of them centered on identifying and eliminating significant harms to human subjects of research.Comprehensive attention has not been paid to the totality of harms experienced by animal subjects, althoughscientific and moral progress require explicit appraisal of these harms. Science is a public good and theprioritizing within, conduct of, generation of, and application of research must soundly address questionsabout which research is morally defensible and valuable enough to support through funding, publication,tenure, and promotion. Likewise, educational pathways of re-imagined science are critical.Keywords: research ethics; animal subjects; morally defensible researchThe past six decades have marked a significant revolution in research ethics in the United States.Following a number of research scandals, as described in Henry Beecher’s influential 1966New EnglandJournal of Medicine paper,1 the National Commission for the Protection of Human Subjects ofBiomedical and Behavioral Research published the Belmont Report, which established foundationalethical principles to guide research involving human subjects.2 One could describe their efforts toimprove human research ethics as “antimaleficent”—focused on actively identifying and reducing actualand potential harms—within a broad framework of justice or fairness.The current treatment of animals within the context of research suffers from some of the sameproblems that Beecher identified within human research.3 Despite significant advances over the past sixdecades in knowledge about the cognitive and emotional lives of animals, no effort to eliminate seriousharms of research or to apply a thoroughgoing principle of justice, similar to that of the Belmont Report,has yet been advanced for animals.4There is an urgent need for scientists and policymakers to acknowledge the importance of anti-maleficence within the context of human and animal research. Progress requires an ethically rigorousevaluation of animal research, including a full articulation of the harms that animals experience duringtheir use in research, and a reimagining of the financial, legislative, and social structures that perpetuateand reward harmful research.© The Author(s), 2022. Published by Cambridge University Press. This is an Open Access article, distributed under the terms of the CreativeCommons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproductionin any medium, provided the original work is properly cited.Cambridge Quarterly of Healthcare Ethics (2022), 31: 1, 54–58doi:10.1017/S0963180121000487https://doi.org/10.1017/S0963180121000487Downloaded from https://www.cambridge.org/core. IP address: 69.207.68.124, on 24 Jan 2022 at 16:08:51, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.Evidence of Harm to Animals Used in ResearchPhysical and Physiological HarmAs research targets, vertebrate animals are exposed to acute and chronic pain, including somatic orvisceral nociceptive pain and central or peripheral neuropathic pain. Similarly, a growing body ofresearch confirms that, despite their neuroanatomical differences from vertebrates, invertebrate animalsalso demonstrate coordinated responses to painful stimuli.5Animals can also experience “sickness behavior” as a result of induced and by-product disease, whichis characterized by lethargy, depression, anorexia, sleep disturbances, or increased pain sensitivity.6Additionally, during development and adulthood, research environments can reshape neurobiologicalactivity and connectivity, muscle and bone growth and structure, the functioning of sensory systems, andcardiovascular, endocrine, and digestive health.Many animals’ vulnerability to physiological harm can be partially explained by abnormalities in thehypothalamic–pituitary–adrenal axis, which have been described in animals who have been confined,restrained, or isolated, and after surgical procedures.7 Even low levels of trauma during early develop-ment can alter patterns and pathways of neurobiological and endocrine development such that adultfunctioning and capacities become constricted.Emotional and Psychological HarmBrain circuits and evolutionary histories prepare animals to experience and express a wide range ofemotions.8 When animals in laboratories are made to undergo, and attempt to cope with, sustainedexperiences of anxiety, fear, sadness, grief, and anger, their bodies andminds are affected, re-shaped, andoften damaged. This lasting harm alters their bodily and mental systems and stunts their capacity to feeland achieve healthy emotional lives.Sustained adverse emotional states also increase the risk for psychological disorders. Attachmentdisorders, depression, complex anxiety disorders, posttraumatic disorders, and other persistent disor-ders of social behavior such as increased aggression and stereotypic behaviors are seen across manyspecies of animals used in research.8Adverse experiences early in life can especially affect development and the propensity formental illness.Maternal–infant separation, confinement, social isolation, persistent fear and pain, and inadequate carecan independently and cumulatively contribute to psychopathology in animals used in research.Sources of Harm in Biomedical and Behavioral ResearchCaptivity“Captivity effects” refer to the range of harmful physical, psychological, and physiological changesinduced by confining captive conditions. These effects are similar in humans and animals, spanningacross mammals, reptiles, amphibians, and fish.9Research regulations often focus on the conditions of confinement (e.g., the size of cages and access tofood and water) as a means of improving welfare. Mere improvements to captive conditions areinsufficient to meet the totality of animals’ needs; captivity itself is a central harm.Loss of Self-Determination and Bodily SovereigntyMany animals have evolved to govern their own lives, make decisions about how to satisfy their needsand avoid danger, and live within broader social and ecological networks. Animals used in researchcommonly experience violations of their bodily sovereignty. Even the technical aspects of researchprocedures and husbandry—including caging and the use of tranquilizers, anesthetics, paralytics, andother forms of physical and chemical force—commonly interfere with bodily sovereignty.Like humans, some animals also have “higher order” needs, such as the need to exercise control overtheir lives. They may thrive only when they are able to form relationships with others and play, socialize,Toward an Anti-Maleficent Research Agenda 55https://doi.org/10.1017/S0963180121000487Downloaded from https://www.cambridge.org/core. IP address: 69.207.68.124, on 24 Jan 2022 at 16:08:51, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.or otherwise act creatively. Self-determination is fundamental to satisfying higher order needs and itprovides a necessary substrate for individuals to thrive.10Infliction of Pain, Injury, Disease, or DiscomfortAnimals used in research experience pain and discomfort as a result of a range of interventions includingdeprivation of or lack of control over access to food and water; extreme temperature exposure; physicalrestraint; deliberate infliction of injury, disability, and disease; medication side effects; incompletemedical or surgical care; and various methods of killing.Invasive procedures also cause pain and discomfort through penetrating trauma (e.g., injections,surgical lacerations, or oral gavage), blunt force trauma (e.g., crush injuries involving the spinal cord orexperimental trauma procedures), asphyxiation (e.g., near drowning with the “forced swim test”), burns(e.g., chemical or thermal burns, or electric shocks), restraint (e.g., head restraint with visual trackingexperiments), and suspension (e.g., the “tail suspension test”).Forced Sex, Coerced Reproduction, and Denial of Sexual FreedomsMany animals housed and used in research facilities are denied the opportunity to engage in a suite ofreproductive behaviors including courtship, mating, gestation, and parental caregiving. Animals are alsodeprived of potential emotional experiences associated with sex and reproduction (e.g., sexual attraction,pleasure, and bonding). Heteronormative cage pairings and forced sex funnel animals into narrowbehavioral patterns that prevent or constrain a diverse range of possibilities, including asexual behaviorsand sexual behaviors with members of the same sex.Other animals in captivity are forced to do nothing but reproduce, often through coercive humaninterventions. Female “breeders” are often forcibly inseminated, while male “semen donors” aresubjected to electroejaculation (repeated electric “stimuli” to the penis), rectal massage, or masturbationof the male by a human.Neonates are almost always taken from their mothers, imposing additional emotional wounds andphysical deprivations.Deprivation of Life’s Full DimensionsThe brains of animals who dwell in rich, complex, and stimulating environments (e.g., their nativehabitats) have higher rates of new neuron-to-neuron connections, whichmeans that vital brain activitieslike information-processing and memory capacity in these individuals increase.11In sterile and boring conditions like laboratories, brain activity is dampened. The loss of opportunitiesfor pleasurable sensory experiences and creative responses to them prevent animals from experiencinglife’s richness.Witnessing HarmsWhen animals used in research suffer physical or emotional pain and distress, their conspecifics maywitness these harms and experience trauma. Animals housed in pairs or small groups remain closelyattuned to what happens together in that shared space; even when caged singly, individuals are often ableto view and sense what happens to others around them because cages are in close proximity.Because animals feel empathy of various types for each other,12 harms inflicted on animals multiplyagain and again, as the experience of one negatively affects many.Deception and ManipulationPractices that are often labeled “humane,” such as positive reinforcement training of animal researchsubjects, are often manipulative, deceptive, and cause harm because they diminish control and enforce56 Hope Ferdowsian et al.https://doi.org/10.1017/S0963180121000487Downloaded from https://www.cambridge.org/core. IP address: 69.207.68.124, on 24 Jan 2022 at 16:08:51, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.conversion to or compliance with the goals of researchers. Acquiescence in the absence of alternatives,such as the freedom to refuse or leave, does not constitute consent or assent.Being KilledAnimals value their lives. Many animal species recognize and grieve death13 and will act to preserve theirown lives and the lives of others. Being killed, and having one’s life deliberately abbreviated, is a harm.The manner in which animals used in research are killed can also cause pain and suffering. Methodsfor killing animals for research include decapitation by guillotine, cervical dislocation with mechanicalforce, asphyxiation, gassing, and lethal injection with barbiturates. Animals are also killed as part ofexperimental protocols, including toxicology tests designed to measure the lethal dose of a substance(e.g., LD50 and LD100 tests).Implications and Recommendations1) The research paradigm must become more ethical and just.The time has come for research agendas to be shaped by social, economic, and cultural values thatare inclusive andmorally rigorous. Values guide science, and science cannot stand as an endeavorseparate from history, social constructs, or current realities, including concrete evidence of agencyand suffering in animals and well-recognized problems with the validity and reliability of researchconducted on animal subjects.142) Federal funding needs to shift.The priorities of funding agencies play a significant role in steering research. U.S. federal fundingof scientific research gives little priority—and little money—to developing alternatives to animalresearch. The General Accountability Office report of 2019, “Animal Use in Research: FederalAgencies Should Assess and Report on Their Efforts to Develop and Promote Alternatives,”contains details of the sparse funding for those alternatives.15A genuine commitment to antimaleficence in researchwill require a significant financial commitment,in the form of earmarked funds for discovering and developing alternatives, and reduced funding forresearchwith animals. Such a shift in priorities would be a radical departure from the status quo, and itis unlikely to happen without pressure from funding sources: Congress and taxpayers.3) Academic journals and publishers must require more of authors.Journals could incorporate a statement of adherence to an antimaleficent framework and to bestpractices, and a request that all submitted manuscripts do so as well. Submitted manuscripts that donot meet these expectations would need an addendum acknowledging the recognition and consid-eration of such criteria along with a specific justification in the addendum for how and why theguidelines were not met. Journal editors would then need to assess the validity of the rationalepresented in the addendum and make appropriate editorial decisions. When researchers are found,postpublication, to have violated established rules, journals should retract papers for ethical breaches.4) Reward structures, including tenure and promotion, need to emphasize and recognize ethics andinnovation.The reward structure in higher education, federal agencies, and other research institutions oughtto reflect the value of research and teaching that develops, implements, uses, or advocates for themethods that follow the highest ethical standards—including an antimaleficent framework. Usingthis approach, tenure, promotion, financial reward, and protected time away from teaching andclinical care opportunities would recognize and reward ethical innovation.Toward an Anti-Maleficent Research Agenda 57https://doi.org/10.1017/S0963180121000487Downloaded from https://www.cambridge.org/core. IP address: 69.207.68.124, on 24 Jan 2022 at 16:08:51, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.5) Education and training pathways need antimaleficent leadership and mentorship.A key connection exists between the reward structure in higher education and research institu-tions and the training students receive in the sciences from elementary school through college andgraduate education. What can be envisioned in research and teaching during one’s career isinfluenced by one’s experience as a student. If more students are to become researchers andeducators who exhibit leadership inmaking scientific advances with ethical and just research, theymust be exposed to and mentored in antimaleficent research methods.ConclusionThe last century saw a dramatic shift in research with humans, towardmore protection, andmore just andethical research. Science adapted. A comparable commitment to antimaleficence in research with animalswould change the status quo, and it would change science as we know it. Much of the incidental andintentional harm that is inflicted on animals would no longer be permissible, and scientists would be calledupon, as they were in generations past, to find new, better, andmore ethical ways of engaging with science.Notes1. Beecher H. Ethics and clinical research. New England Journal of Medicine 1966;274:1354–60.2. The Commission, Belmont Report: Ethical Principles and Guidelines for the Protection of HumanSubjects of Research. Bethesda, MD: The Commission; 1978.3. Ferdowsian H, Gluck, J. The ethical challenges of animal research: Honoring Henry Beecher’sapproach to moral problems. Cambridge Quarterly of Healthcare Ethics 2015;24:391–406.4. FerdowsianH, Johnson LSM, Johnson J, FentonA, Shriver A, Gluck J. A Belmont report for animals?Cambridge Quarterly of Healthcare Ethics 2020;29:19–37.5. Sneddon LU, Elwood RW, Adamo SA, Leach MC. Defining and assessing animal pain. AnimalBehaviour 2014;97:201–12.6. Hart BL, Hart LA. Sickness behavior in animals: Implications for health and wellness. In: Choe JC,ed. Encyclopedia of Animal Behavior. 2nd ed. Cambridge, MA: Academic Press; 2019, at 171–5.7. Gregory NG. Physiology and Behavior of Animal Suffering. London, UK: Wiley; 2004.8. Panksepp J. The basic emotional circuits of mammalian brains: Do animals have affective lives?Neuroscience & Biobehavioural Reviews 2011;35:1791–804.9. Bekoff M, Pierce J. The Animals’Agenda: Freedom, Compassion, and Coexistence in the Human Age.New York, NY: Penguin Random House; 2018.10. Ryan RM, Deci EL. Self-Determination Theory: Basic Psychological Needs in Motivation, Develop-ment, and Wellness. 1st ed. New York, NY: The Guilford Press; 2017.11. Markham JA, GreenoughWT. Experience-driven brain plasticity: Beyond the synapse.Neuron GliaBiology 2004;1:351–63.12. de Waal FBW, Preston SD. Mammalian empathy: Behavioral manifestations and neural basis.Nature Reviews Neuroscience 2017;18:498–509.13. King BJ. How Animals Grieve. Chicago, IL: University of Chicago Press; 2013.14. Bracken MB.Why animal studies are often poor predictors of human reactions to exposure. Journalof the Royal Society of Medicine 2009;102:120–2.15. U.S. Government Accountability Office (GAO). Animal use in research: Federal agencies shouldassess and report on their efforts to develop and promote alternatives. (Publication GAO-19-629,GAO, 2019; https://www.gao.gov/assets/710/707338.pdf).Cite this article: Ferdowsian, H. Fuentes, A. Johnson, L. S. M. King, B. J. and Pierce, J. 2022. Toward an Anti-MaleficentResearch Agenda. Cambridge Quarterly of Healthcare Ethics 31: 54–58, doi:10.1017/S096318012100048758 Hope Ferdowsian et al.https://doi.org/10.1017/S0963180121000487Downloaded from https://www.cambridge.org/core. IP address: 69.207.68.124, on 24 Jan 2022 at 16:08:51, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.

Toward an Anti-Maleficent Research Agenda

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Toward an Anti-Maleficent Research Agenda

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