{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,3,26]],"date-time":"2025-03-26T04:23:54Z","timestamp":1742963034118,"version":"3.40.3"},"reference-count":44,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2025,3,25]],"date-time":"2025-03-25T00:00:00Z","timestamp":1742860800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/publicdomain\/zero\/1.0\/"}],"funder":[{"DOI":"10.13039\/100008370","name":"National Pork Board","doi-asserted-by":"publisher","award":["22-084"],"award-info":[{"award-number":["22-084"]}],"id":[{"id":"10.13039\/100008370","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100008370","name":"National Pork Board","doi-asserted-by":"publisher","award":["22-085"],"award-info":[{"award-number":["22-085"]}],"id":[{"id":"10.13039\/100008370","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>The threat of foreign animal disease outbreaks to U.S. swine herds warrants effective and readily available depopulation methods. Current American Veterinary Medical Association-recommendations using preferred physical methods for swine depopulation are unsuitable for large commercial swine herds. Our objectives were to assess and compare the efficacy and performance of three suggested large-scale depopulation methods: 1) medium-expansion water-based foam, 2) prototype high-expansion nitrogen foam and, 3) carbon dioxide gas for finisher pigs under field conditions. Out of 793 finisher pigs included in the study, 84 were implanted with bio-loggers recording electrocardiogram and pig movement data. Aversive pig behaviors were collected manually on a group level for each depopulation method. A subsample of pigs from each method were examined post-mortem for lesions and compared to a reference group of nine pigs euthanized with pentobarbital. Depopulation method assessments included container fill time, the number of aversive pig behaviors observed during depopulation, overall pig movement intensity, time to cessation of movement, time to and cause of cardiac arrest, and respiratory lesions. No difference in fill times between water-based foam and nitrogen foam was observed. The total number of aversive swine behaviors was higher for carbon-dioxide compared to both foam methodologies (<jats:italic>P<\/jats:italic> &lt;\u2009 0.01). The total pig activity was higher in water-based foam compared to nitrogen foam (<jats:italic>P<\/jats:italic> =\u2009 0.02) and carbon-dioxide methods (<jats:italic>P<\/jats:italic> =\u2009 0.01). The mean time to cessation of movement was significantly shorter for water-based foam and nitrogen foam compared to carbon-dioxide (<jats:italic>P &lt;\u2009<\/jats:italic> 0.01). No differences in cardiac activity were observed. Water-based foam pigs had increased odds of distal trachea occlusions compared to other methods. All depopulation methods demonstrated high efficacy with a 100% mortality rate. The results from this study support large-scale water-based foam, nitrogen foam and carbon dioxide as viable AVMA depopulation guideline candidates for swine.<\/jats:p>","DOI":"10.1371\/journal.pone.0320217","type":"journal-article","created":{"date-parts":[[2025,3,25]],"date-time":"2025-03-25T23:45:47Z","timestamp":1742946347000},"page":"e0320217","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["Assessment of three large-scale depopulation methods for swine"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4226-7339","authenticated-orcid":true,"given":"Janice Y.","family":"Park","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3575-7890","authenticated-orcid":true,"given":"Magnus R.","family":"Campler","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3732-9147","authenticated-orcid":true,"given":"Ting-Yu","family":"Cheng","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Brad L.","family":"Youngblood","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dawn","family":"Torrisi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michael D.","family":"Cressman","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Justin D.","family":"Kieffer","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-7618-2559","authenticated-orcid":true,"given":"Todd E.","family":"Williams","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andr\u00e9ia G.","family":"Arruda","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gary A.","family":"Flory","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daniel P.","family":"Hougentogler","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jeff","family":"Hill","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lucia","family":"Hunt","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Albert","family":"Canturri","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3547-7576","authenticated-orcid":true,"given":"Marie R.","family":"Culhane","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jesse","family":"Miller","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andrew S.","family":"Bowman","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2025,3,25]]},"reference":[{"key":"pone.0320217.ref001","volume-title":"AVMA Guidelines for the depopulation of animals: 2019 Edition","author":"S Leary","year":"2019"},{"issue":"11","key":"pone.0320217.ref002","doi-asserted-by":"crossref","first-page":"911","DOI":"10.3390\/ani9110911","article-title":"Humanely ending the life of animals: research priorities to identify alternatives to carbon dioxide","volume":"9","author":"AR Steiner","year":"2019","journal-title":"Animals (Basel)"},{"issue":"1","key":"pone.0320217.ref003","doi-asserted-by":"crossref","first-page":"140","DOI":"10.3390\/ani13010140","article-title":"The rise of heatstroke as a method of depopulating pigs and poultry: implications for the US veterinary profession","volume":"13","author":"G Reyes-Illg","year":"2022","journal-title":"Animals (Basel)"},{"key":"pone.0320217.ref004","volume-title":"Regulation - 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Controlled atmosphere stunning of pigs using nitrogen, argon and carbon dioxide in high-expansion foam. Conference paper, 27th Congress of the Nordic Association of Agricultural Sciences, 27-29 September, 2022, Selfoss, Iceland."},{"issue":"3","key":"pone.0320217.ref021","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1016\/j.neuropharm.2008.01.005","article-title":"Mechanisms of ischemic brain damage","volume":"55","author":"KP Doyle","year":"2008","journal-title":"Neuropharmacology"},{"issue":"5","key":"pone.0320217.ref022","doi-asserted-by":"crossref","first-page":"1145","DOI":"10.3382\/ps.2012-02587","article-title":"Physiological and behavioral responses of poultry exposed to gas-filled high expansion foam","volume":"92","author":"DEF McKeegan","year":"2013","journal-title":"Poult Sci"},{"issue":"12","key":"pone.0320217.ref023","doi-asserted-by":"crossref","first-page":"2210","DOI":"10.3390\/ani10122210","article-title":"Responses of pigs to stunning with nitrogen filled high-expansion foam","volume":"10","author":"C Lindahl","year":"2020","journal-title":"Animals (Basel)"},{"key":"pone.0320217.ref024","unstructured":"Wallenbeck A, Sindh\u00f6j E, Brattlund Hellgren R, Berg C, Lindahl C. 2020. Improved pig welfare at slaughter: Pigs\u2019 responses to air- or nitrogen foam. In: International Society for Applied Ethology, Nordic Region Winter Meeting. p. 25."},{"key":"pone.0320217.ref025","unstructured":"Poehlmann, K. 2012. Corporate Strategic Responses to Institutional Pressures: A Study of the Global Pulp and Paper Industry. Doctoral dissertation, Freie Universit\u00e4t Berlin. Available at: https:\/\/refubium.fu-berlin.de\/bitstream\/handle\/fub188\/13065\/Poehlmann_online.pdf?sequence=1&isAllowed=y"},{"issue":"4","key":"pone.0320217.ref026","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1017\/S1751731111001911","article-title":"Stunning pigs with nitrogen and carbon dioxide mixtures: effects on animal welfare and meat quality","volume":"6","author":"P Llonch","year":"2012","journal-title":"Animal"},{"key":"pone.0320217.ref027","doi-asserted-by":"crossref","first-page":"31","DOI":"10.54846\/jshap\/1243","article-title":"Modification of a standard dump trailer into a mobile carbon dioxide depopulation unit for swine","volume":"30","author":"B Pepin","year":"2022","journal-title":"J Swine Health Prod"},{"issue":"5","key":"pone.0320217.ref028","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1111\/acem.12643","article-title":"Intraarrest rhythms and rhythm conversion in asphyxial cardiac arrest","volume":"22","author":"G Varvarousi","year":"2015","journal-title":"Acad Emerg Med"},{"issue":"2","key":"pone.0320217.ref029","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1097\/00000433-200106000-00006","article-title":"Morphologic determinants of asphyxia in lungs: a semiquantitative study in forensic autopsies","volume":"22","author":"C Delmonte","year":"2001","journal-title":"Am J Forensic Med Pathol"},{"key":"pone.0320217.ref030","first-page":"1","article-title":"Drowning and bodies recovered from water","volume":"2","author":"B McEwen","year":"2018","journal-title":"Veterinary Forensic Pathology"},{"issue":"1","key":"pone.0320217.ref031","doi-asserted-by":"crossref","first-page":"16798","DOI":"10.1038\/s41598-022-21353-7","article-title":"Description of electroencephalographic data gathered using water-based medium-expansion foam as a depopulation method for nursery pigs","volume":"12","author":"J Korenyi-Both","year":"2022","journal-title":"Sci Rep"},{"key":"pone.0320217.ref032","volume-title":"Welfare assessment of gas-filled foam as an agent for killing poultry","author":"M Gerritzen","year":"2010"},{"issue":"1","key":"pone.0320217.ref033","doi-asserted-by":"crossref","first-page":"11","DOI":"10.3390\/ani8010011","article-title":"Depopulation of caged layer hens with a compressed air foam system","volume":"8","author":"S Gurung","year":"2018","journal-title":"Animals (Basel)"},{"key":"pone.0320217.ref034","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1002\/9781119421375.ch6","article-title":"Euthanasia and humane killing.","volume-title":"Veterinary Anesthesia and Analgesia: The Fifth Edition of Lumb and Jones","author":"RE. Meyer","year":"2015"},{"issue":"9","key":"pone.0320217.ref035","doi-asserted-by":"crossref","first-page":"1355","DOI":"10.1111\/j.1540-8159.1996.tb04215.x","article-title":"Effects of autonomic manipulation on ventricular fibrillation and internal cardiac defibrillation thresholds in pigs","volume":"19","author":"CA Morillo","year":"1996","journal-title":"Pacing Clin Electrophysiol"},{"issue":"11","key":"pone.0320217.ref036","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1016\/S0361-1124(79)80058-1","article-title":"Asystole and its treatment: the possible role of the parasympathetic nervous system in cardiac arrest","volume":"8","author":"DC Brown","year":"1979","journal-title":"JACEP"},{"issue":"5","key":"pone.0320217.ref037","first-page":"491","article-title":"Review of CO\u2082 as a euthanasia agent for laboratory rats and mice","volume":"56","author":"GP Boivin","year":"2017","journal-title":"J Am Assoc Lab Anim Sci"},{"key":"pone.0320217.ref038","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/0168-1591(96)01067-2","article-title":"Behavioural responses of domestic pigs and cattle to humans and novel stimuli","volume":"50","author":"P Hemsworth","year":"1996","journal-title":"Appl Anim BehavSci"},{"key":"pone.0320217.ref039","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1016\/S0168-1591(97)00142-1","article-title":"Sound avoidance by domestic pigs depends upon characteristics of the signal","volume":"58","author":"J Talling","year":"1998","journal-title":"Appl Anim Behav Sci"},{"issue":"8","key":"pone.0320217.ref040","doi-asserted-by":"crossref","first-page":"45","DOI":"10.3390\/ani6080045","article-title":"Evaluation of low versus high volume per minute displacement CO\u2082 methods of euthanasia in the induction and duration of panic-associated behavior and physiology","volume":"6","author":"DL Hickman","year":"2016","journal-title":"Animals (Basel)"},{"key":"pone.0320217.ref041","author":"Everstream Analytics","year":"2022"},{"issue":"5","key":"pone.0320217.ref042","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1177\/0300985816643370","article-title":"Nondrowning asphyxia in veterinary forensic pathology: suffocation, strangulation, and mechanical asphyxia","volume":"53","author":"BJ McEwen","year":"2016","journal-title":"Vet Pathol"},{"issue":"2","key":"pone.0320217.ref043","doi-asserted-by":"crossref","first-page":"159","DOI":"10.3109\/15376516.2011.610388","article-title":"\u201cFoam Cone\u201d exuding from the mouth and nostrils following heroin overdose","volume":"22","author":"RJ Dinis-Oliveira","year":"2012","journal-title":"Toxicol Mech Methods"},{"issue":"5","key":"pone.0320217.ref044","doi-asserted-by":"crossref","first-page":"472","DOI":"10.3357\/ASEM.2217.2008","article-title":"Pulmonary edema induced by cerebral hypoxic insult in a canine model","volume":"79","author":"DC Irwin","year":"2008","journal-title":"Aviat Space Environ Med"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0320217","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,3,25]],"date-time":"2025-03-25T23:47:01Z","timestamp":1742946421000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0320217"}},"subtitle":[],"editor":[{"given":"I Anna S","family":"Olsson","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2025,3,25]]},"references-count":44,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2025,3,25]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0320217","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,3,25]]}}}