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Humanely Ending the Life of Animals: Research Priorities to Identify Alternatives to Carbon Dioxide

Department of Clinical and Diagnostic Services, Section of Anaesthesiology, Vetsuisse Faculty, University of Zurich, Winterthurerstrasse 258c, 8057 Zurich, Switzerland
Department of Clinical Veterinary Medicine, Section of Anesthesia and Analgesia, Vetsuisse Faculty, University of Berne, Laenggassstrasse 124, 3012 Bern, Switzerland
Animal Welfare Science and Bioethics Centre, School of Veterinary Science, Massey University, Palmerston North 4410, New Zealand
Department of Animal Environment and Health, Swedish University of Agricultural Sciences, Box 234, SE-53223 Skara, Sweden
Animal and Plant Health Agency and Department for Environment, Food and Rural Affairs, Nobel House, 17 Smith Square, London SW1P 3JR, UK
Universities Federation for Animal Welfare (UFAW), The Old School, Brewhouse Hill, Wheathampstead, Hertfordshire AL4 8AN, UK
Institute of Animal Welfare and Animal Husbandry, Friedrich-Loeffler-Institut, Dörnbergstraße 25/27, 29223 Celle, Germany
Department of Clinical Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, MS 39762, USA
Roche Pharma Research and Early Development, Pharmaceutical Sciences, Roche Innovation Center Basel, F. Hoffmann-La Roche Ltd., Grenzacherstrasse 124, 4070 Basel, Switzerland
Center for Proper Housing: Poultry and Rabbits (ZTHZ), Animal Welfare Division, VPH Institute, University of Bern, 3052 Zollikofen, Switzerland
Department of Pathobiology, University of Guelph, Guelph, ON N1G 2W1, Canada and Charles River, Wilmington, MA 01887, USA
Animal Welfare Program, University of British Colombia, 2357 Main Mall, Vancouver, BC V6T 1Z4, Canada
Author to whom correspondence should be addressed.
Animals 2019, 9(11), 911;
Received: 19 September 2019 / Revised: 14 October 2019 / Accepted: 25 October 2019 / Published: 2 November 2019
(This article belongs to the Special Issue 60 Years of the Three Rs and Their Impact on Animal Welfare)
Carbon dioxide is commonly used for stunning animals prior to killing. It allows several animals to be killed at once, reduces the need for handling, and is a reliable method. However, research in laboratory rodents, poultry, and pigs has indicated that it causes considerable aversion at concentrations above ambient conditions. Currently, there are no available alternatives with desirable characteristics. This manuscript describes a list of research priorities to find and implement the use of alternative methods or agents to improve animal welfare.
The use of carbon dioxide (CO2) for stunning and killing animals is considered to compromise welfare due to air hunger, anxiety, fear, and pain. Despite decades of research, no alternatives have so far been found that provide a safe and reliable way to induce unconsciousness in groups of animals, and also cause less distress than CO2. Here, we revisit the current and historical literature to identify key research questions that may lead to the identification and implementation of more humane alternatives to induce unconsciousness in mice, rats, poultry, and pigs. In addition to the evaluation of novel methods and agents, we identify the need to standardise the terminology and behavioural assays within the field. We further reason that more accurate measurements of consciousness state are needed and serve as a central component in the assessment of suffering. Therefore, we propose a roadmap toward improving animal welfare during end-of-life procedures. View Full-Text
Keywords: animal welfare; carbon dioxide; stunning; killing; euthanasia; rodents; poultry; pigs; aversion; air hunger animal welfare; carbon dioxide; stunning; killing; euthanasia; rodents; poultry; pigs; aversion; air hunger
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Steiner, A.R.; Axiak Flammer, S.; Beausoleil, N.J.; Berg, C.; Bettschart-Wolfensberger, R.; García Pinillos, R.; Golledge, H.D.; Marahrens, M.; Meyer, R.; Schnitzer, T.; Toscano, M.J.; Turner, P.V.; Weary, D.M.; Gent, T.C. Humanely Ending the Life of Animals: Research Priorities to Identify Alternatives to Carbon Dioxide. Animals 2019, 9, 911.

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