Alternatives to Carbon Dioxide—Taking Responsibility for Humanely Ending the Life of Animals
2. Listening and Discussing—Gathering the Perspectives of Different Stakeholders
- Researchers from academia, higher education institutions, and the pharmaceutical industry
- Swiss animal welfare officers
- Swiss 3R Competence Centre
- German Centre for the Protection of Laboratory Animals (Deutsches Zentrum zum Schutz von Versuchstieren)
- Pig and poultry slaughtering, meat industry
- Veterinary anesthesia experts
- Laboratory animal medicine experts
- Swiss laboratory animal science teaching institutions
- Swiss cantonal veterinary offices
- Swiss cantonal animal experimentation committees
- Swiss Federal Commission for Animal Experimentation
- Swiss Federal Office of Public Health
- German, Norwegian, and Danish governmental animal welfare institutions for animal experimentation and slaughtering
- Swiss and international animal welfare organizations
2.1. What is a Good Death for Animals?
- What are your first thoughts in reaction to the question ‘What is a good death for animals?’
- How do you know that an animal is suffering?
- What makes up a ‘good death’ from the perspective of the animal (that is being killed) and the human (that kills the animal)?
- Is a ‘good death’ different depending on the purpose or environment? [For example, livestock (slaughter versus companion animals versus experimental animals (termination of the study /destruction of surplus animals)]?
- Which criteria would you include in a checklist for ‘What is a good death for animals’?
- is not associated with suffering, pain, anxiety, stress, or distress
- is reliable and under control and expert supervision until death
- is immediate, without delay, and irreversible
- is safe for the staff and other animals
- avoids contamination of the environment
2.2. Alternatives to Carbon Dioxide
2.3. A World Café
- What would you do if you could not use carbon dioxide today for euthanasia?
- Can you suggest any novel methods or novel refinements to existing methods (not covered by the talks today) that might be a humane and practical alternative to carbon dioxide?
- How can your professional experience contribute to the search of alternatives to carbon dioxide?
3. Identified Roadblocks
- Better use of technology to identify and define parameters that occur during death (e.g., behavior, physiological changes) that are species and category dependent.
- Finding ways of reducing the number of animals that need to be killed. For example, many laboratory animals are killed simply because these are deemed as surplus animals from the breeding program. Therefore, continued refinement of the breeding program, combined with better programs to match animals and researchers (e.g., AniMatch (www.swiss.animatch.eu)), need to be encouraged.
- Undertaking a comprehensive evaluation of the entire infrastructure from housing type to transportation to limit stress from the beginning until the end of an animal’s life.
- Reflection on the practice of research as an entity, from experimental design and grant application to publication of results. For example, there is pressure on scientists to obtain grants and publish the results as soon as possible. Several steps in this process (ethical evaluation, review, and decision to award a grant or publish a manuscript) depend on a severely taxed voluntary peer review system. For many scientists performing animal experiments, there is little time, funding, or incentive to adopt refinements in their procedures, including procedures used for killing.
- Finally, participants called for more research on humane killing methods and societal acceptance of these procedures (as part of more general move towards more transparency regarding animal use).
4. Next Steps
Conflicts of Interest
- Hawkins, P.; Prescott, M.J.; Carbone, L.; Dennison, N.; Johnson, C.; Makowska, I.J.; Marquardt, N.; Readman, G.; Weary, D.M.; Golledge, H.D. A Good Death? Report of the Second Newcastle Meeting on Laboratory Animal Euthanasia. Animals 2016, 6, 50. [Google Scholar] [CrossRef] [PubMed]
- Terlouw, C.; Bourguet, C.; Deiss, V. Consciousness, unconsciousness and death in the context of slaughter. Part I. Neurobiological mechanisms underlying stunning and killing. Meat Sci. 2016, 118, 133–146. [Google Scholar] [CrossRef] [PubMed]
- Conlee, K.M.; Stephens, M.L.; Rowan, A.N.; King, L.A. Carbon dioxide for euthanasia: Concerns regarding pain and distress, with special reference to mice and rats. Lab. Anim. 2005, 39, 137–161. [Google Scholar] [CrossRef] [PubMed]
- Danneman, P.J.; Stein, S.; Walshaw, S.O. Humane and practical implications of using carbon dioxide mixed with oxygen for anesthesia or euthanasia of rats. Lab. Anim. Sci. 1997, 47, 376–385. [Google Scholar] [PubMed]
- European Union. Directive 2010/63/EU of the European Parliament and of the council of 22 September 2010 on the protection of animals used for scientific purposes. Off. J. Eur. Union 2010, 276, 33–79. [Google Scholar]
- Bailey, J.E.; Argyropoulos, S.V.; Kendrick, A.H.; Nutt, D.J. Behavioral and cardiovascular effects of 7.5% CO2 in human volunteers. Depress Anxiety 2005, 21, 18–25. [Google Scholar] [CrossRef]
- Vollmer, L.L.; Ghosal, S.; McGuire, J.L.; Ahlbrand, R.L.; Li, K.Y.; Santin, J.M.; Ratliff-Rang, C.A.; Patrone, L.G.; Rush, J.; Lewkowich, I.P.; et al. Microglial Acid Sensing Regulates Carbon Dioxide-Evoked Fear. Biol. Psychiatry 2016, 80, 541–551. [Google Scholar] [CrossRef][Green Version]
- Ziemann, A.E.; Allen, J.E.; Dahdaleh, N.S.; Drebot, I.I.; Coryell, M.W.; Wunsch, A.M.; Lynch, C.M.; Faraci, F.M.; Howard, M.A., 3rd; Welsh, M.J.; et al. The amygdala is a chemosensor that detects carbon dioxide and acidosis to elicit fear behavior. Cell 2009, 139, 1012–1021. [Google Scholar] [CrossRef]
- Wong, D.; Makowska, I.J.; Weary, D.M. Rat aversion to isoflurane versus carbon dioxide. Biol. Lett. 2013, 9, 20121000. [Google Scholar] [CrossRef]
- Boulanger Bertolus, J.; Nemeth, G.; Makowska, I.J.; Weary, D.M. Rat aversion to sevoflurane and isoflurane. Appl. Anim. Behav. Sci. 2015, 164, 73–80. [Google Scholar] [CrossRef]
- Johnson, P.L.; Fitz, S.D.; Hollis, J.H.; Moratalla, R.; Lightman, S.L.; Shekhar, A.; Lowry, C.A. Induction of c-Fos in ‘panic/defence’-related brain circuits following brief hypercarbic gas exposure. J. Psychopharmacol. 2011, 25, 26–36. [Google Scholar] [CrossRef]
- Hu, J.; Zhong, C.; Ding, C.; Chi, Q.; Walz, A.; Mombaerts, P.; Matsunami, H.; Luo, M. Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse. Science 2007, 317, 953–957. [Google Scholar] [CrossRef]
- Bleymehl, K.; Perez-Gomez, A.; Omura, M.; Moreno-Perez, A.; Macias, D.; Bai, Z.; Johnson, R.S.; Leinders-Zufall, T.; Zufall, F.; Mombaerts, P. A Sensor for Low Environmental Oxygen in the Mouse Main Olfactory Epithelium. Neuron 2016, 92, 1196–1203. [Google Scholar] [CrossRef][Green Version]
- Swiss Confederation. Animal Welfare Ordinance. 23 April 2008. Available online: https://www.admin.ch/opc/de/classified-compilation/20080796/index.html (accessed on 27 June 2019).
- Niel, L.; Kirkden, R.D.; Weary, D.M. Effects of novelty on rats’ responses to CO2 exposure. Appl. Anim. Behav. Sci. 2008, 111, 183–194. [Google Scholar] [CrossRef]
- Niel, L.; Weary, D.M. Rats avoid exposure to carbon dioxide and argon. Appl. Anim. Behav. Sci. 2007, 107, 100–109. [Google Scholar] [CrossRef]
- Kirkden, R.D.; Niel, L.; Lee, G.; Makowska, I.J.; Pfaffinger, M.J.; Weary, D.M. The validity of using an approach-avoidance test to measure the strength of aversion to carbon dioxide in rats. Appl. Anim. Behav. Sci. 2008, 114, 216–234. [Google Scholar] [CrossRef]
- Makowska, I.J.; Vickers, L.; Mancell, J.; Weary, D.M. Evaluating methods of gas euthanasia for laboratory mice. Appl. Anim. Behav. Sci. 2009, 121, 230–235. [Google Scholar] [CrossRef]
- Moody, C.M.; Weary, D.M. Mouse aversion to isoflurane versus carbon dioxide gas. Appl. Anim. Behav. Sci. 2014, 158, 95–101. [Google Scholar] [CrossRef]
- Gent, T.C.; Detotto, C.; Vyssotski, A.L.; Bettschart-Wolfensberger, R. Epileptiform activity during inert gas euthanasia of mice. PLoS ONE 2018, 13, e0195872. [Google Scholar] [CrossRef]
- Detotto, C.; Isler, S.; Wehrle, M.; Vyssotski, A.L.; Bettschart-Wolfensberger, R.; Gent, T.C. Nitrogen gas produces less behavioural and neurophysiological excitation than carbon dioxide in mice undergoing euthanasia. PLoS ONE 2019, 14, e0210818. [Google Scholar] [CrossRef]
- Gent, T.C.; Vyssotski, A.L.; Detotto, C.; Isler, S.; Wehrle, M.; Bettschart-Wolfensberger, R. Is Xenon a suitable euthanasia agent for mice? Vet. Anaesth. Analg. 2019, in press. [Google Scholar] [CrossRef]
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Axiak Flammer, S.; Eskes, C.; Kohler, I.; Ochieng Pernet, A.; Jakob, P.; Marahrens, M.; Gent, T.C.; Golledge, H.; Weary, D. Alternatives to Carbon Dioxide—Taking Responsibility for Humanely Ending the Life of Animals. Animals 2019, 9, 482. https://doi.org/10.3390/ani9080482
Axiak Flammer S, Eskes C, Kohler I, Ochieng Pernet A, Jakob P, Marahrens M, Gent TC, Golledge H, Weary D. Alternatives to Carbon Dioxide—Taking Responsibility for Humanely Ending the Life of Animals. Animals. 2019; 9(8):482. https://doi.org/10.3390/ani9080482Chicago/Turabian Style
Axiak Flammer, Shannon, Chantra Eskes, Ingrid Kohler, Awilo Ochieng Pernet, Peter Jakob, Michael Marahrens, Thomas C. Gent, Huw Golledge, and Dan Weary. 2019. "Alternatives to Carbon Dioxide—Taking Responsibility for Humanely Ending the Life of Animals" Animals 9, no. 8: 482. https://doi.org/10.3390/ani9080482