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The associations between animal-based welfare measures and the presence of indicators of food safety in finishing pigs

Published online by Cambridge University Press:  01 January 2023

I Alpigiani*
Affiliation:
Department of Veterinary Science, University of Parma, Parma, Italy
C Bacci
Affiliation:
Department of Veterinary Science, University of Parma, Parma, Italy
LJ Keeling
Affiliation:
Swedish University of Agricultural Sciences, Department of Animal Environment and Health, Uppsala, Sweden
MD Salman
Affiliation:
Animal Population Health Institute, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, USA
F Brindani
Affiliation:
Department of Veterinary Science, University of Parma, Parma, Italy
S Pongolini
Affiliation:
Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia-Romagna, Parma, Italy
PL Hitchens
Affiliation:
Swedish University of Agricultural Sciences, Department of Animal Environment and Health, Uppsala, Sweden
S Bonardi
Affiliation:
Department of Veterinary Science, University of Parma, Parma, Italy
*
* Contact for correspondence and requests for reprints: irene.alpigiani@nemo.unipr.it

Abstract

Stressful housing and management practices affect animals, potentially increasing their receptiveness to pathogens. Since some pathogens do not lead to clinical signs of sickness, subclinical pigs could enter the food-chain, contaminating carcases and offal at slaughter, representing a threat to human health. Here, we assess the feasibility of a new approach (using animal-based welfare outcomes) to investigate the association between the animal welfare status of finishing pigs on-farm and the occurrence of Yersinia enterocolitica and Salmonella enterica in slaughtered pigs in Northern Italy. Thirty batches of finishing pigs were assessed for animal-, resource- and management-based measures according to the Welfare Quality® protocol for pigs on-farm and at slaughter. A sample of five individuals per batch was tested for Y. enterocolitica and S. enterica in tonsils and in mesenteric lymph nodes, respectively, and gross pathological changes were recorded. Environmental faecal samples per batch on-farm were tested for the same pathogens. Univariable logistic regression models were used to investigate the association between batches of pigs that were positive to Y. enterocolitica and S. enterica and indicators of poor welfare. The animal-based measures of welfare, greater on-farm mortality and poor human-animal relationship, were found to be associated with Y. enterocolitica. This study provides a good indication of the validity of this approach, but there is a need for larger-scale studies in the future to confirm the magnitude of the associations between these animal welfare and food safety indicators.

Type
Research Article
Copyright
© 2016 Universities Federation for Animal Welfare

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References

Bahnson, PB, Fedorka-Cray, PJ, Ladely, SR and Mateus-Pinilla, NE 2006 Herd-level risk factors for Salmonella enterica subsp. enterica in US market pigs. Preventive Veterinary Medicine 76:249262. http://dx.doi.org/10.1016/j.prevetmed.2006.05.009CrossRefGoogle ScholarPubMed
Bonardi, S, Alpigiani, I, Pongolini, S, Morganti, M, Tagliabue, S, Bacci, C and Brindani, F 2014 Detection, enumeration and characterization of Yersinia enterocolitica 4/O:3 in pig tonsils at slaughter in Northern Italy. International Journal of Food Microbiology 177: 915. http://dx.doi.org/10.1016/j.ijfoodmi-cro.2014.02.005CrossRefGoogle ScholarPubMed
Bonardi, S, Bassi, L, Brindani, F, D’Incau, M, Barco, L, Carra, E and Pongolini, S 2013 Prevalence, characterization and antimi-crobial susceptibility of Salmonella enterica and Yersinia enterocoliti-ca in pigs at slaughter in Italy. International Journal of Food Microbiology 163: 248257. http://dx.doi.org/10.1016/j.ijfoodmi-cro.2013.02.012CrossRefGoogle Scholar
Bottone, EJ 2015 Yersinia enterocolitica: Revisitation of an enduring human pathogen. Clinical Microbiology Newsletter 37: 18. http://dx.doi.org/10.1016/j.clinmicnews.2014.12.003CrossRefGoogle Scholar
Bull, SA, Humphrey, TA, Ellis-Iversen, J, Cook, AJ, Lovell, R and Jorgensen, F 2008 Flock health indicators and Campylobacter spp in commercial housed broilers reared in Great Britain. Applied Environmental Microbiology 74: 54085413. http://dx.doi.org/10.1128/AEM.00462-08CrossRefGoogle ScholarPubMed
Callaway, TR, Morrow, JL, Edrington, TS, Genovese, KJ, Dowd, S, Carroll, J, Dailey, JW, Harvey, RB, Poole, TL, Anderson, RC and Nisbet, DJ 2006 Social stress increases fecal shedding of Salmonella typhimurium by early weaned piglets. Current Issues in Intestinal Microbiology 7: 6571Google ScholarPubMed
Cogan, TA, Thomas, AO, Rees, LEN, Taylor, AH, Jepson, MA, Williams, PH, Ketley, J and Humphrey, TJ 2007 Norepinephrine increases the pathogenic potential of Campylobacter jejuni. Gut 56: 10601065. http://dx.doi.org/10.1136/gut.2006.114926CrossRefGoogle ScholarPubMed
De Passillé, AM and Rushen, J 2005 Food safety and environ-mental issues in animal welfare. Revue scientifique et technique (International Office of Epizootics) 24: 757766Google Scholar
Dowd, SE, Callaway, TR and Morrow-Tesch, J 2007 Handling may cause increased shedding of Escherichia coli and total col-iforms in pigs. Foodborne Pathogenes and Disease 4: 99102. http://dx.doi.org/10.1089/fpd.2006.53CrossRefGoogle ScholarPubMed
EFSA (European Food Safety Authority) 2012 Statement on the use of animal-based measures to assess the welfare of ani-mals. EFSA Journal 10 (2767): 29CrossRefGoogle Scholar
EFSA and ECDC 2013 The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2011. EFSA Journal 11 (3129): 250CrossRefGoogle Scholar
EFSA and ECDC 2014 The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2012. EFSA Journal 12 (3547): 312CrossRefGoogle Scholar
European Commission 2008 Commission Decision (EC)55/2008 concerning a financial contribution from the Community towards a survey on the prevalence of Salmonella spp and Methicillin-resistant Staphylococcus aureus in herds of breeding pigs to be carried out in the Member States, Annex 1 Part B. Official Journal of the European Union L14: 10-25Google Scholar
Fosse, J, Seegers, H and Magras, C 2009 Prevalence and risk factors for bacterial food-borne zoonotic hazards in slaughtered pigs: A review. Zoonoses and Public Health 56: 429454. http://dx.doi.org/10.1111/j.1863-2378.2008.01185.xCrossRefGoogle ScholarPubMed
Fredriksson-Ahomaa, M, Stolle, A and Stephan, R 2007 Prevalence of pathogenic Yersinia enterocolitica in pigs slaughtered at a Swiss abattoir. International Journal of Food Microbiology 119:207212. http://dx.doi.org/10.1016/j.ijfoodmicro.2007.07.050CrossRefGoogle Scholar
Garcıa-Feliz, C, Carvajal Angel Collazos, J and Rubio, P 2009 Herd-level risk factors for faecal shedding of Salmonella enterica in Spanish fattening pigs. Preventive Veterinary Medicine 91:130136. http://dx.doi.org/10.1016/j.prevetmed.2009.05.011CrossRefGoogle ScholarPubMed
Hemsworth, PH 2003 Human-animal interaction in livestock production. Applied Animal Behaviour Science 81: 185198. http://dx.doi.org/10.1016/S0168-1591(02)00280-0CrossRefGoogle Scholar
Kopinski, JS and McKenzie, RA 2007 Oesophagogastric ulceration in pigs: a visual morphological scoring guide. Australian Veterinary Journal 85: 356361. http://dx.doi.org/10.1111/j.1751-0813.2007.196_1.xCrossRefGoogle ScholarPubMed
Nesbakken, T, Iversen, T, Eckner, K and Lium, B 2006 Testing of pathogenic Yersinia enterocolitica in pig herds based on the natural dynamic of infection. International Journal of Food Microbiology 111: 99104. http://dx.doi.org/10.1016/j.ijfoodmicro.2006.04.019CrossRefGoogle ScholarPubMed
Noordhuizen, JPTM and Frankena, K 1999 Epidemiology and qual-ity assurance: applications at farm level. Preventive Veterinary Medicine 39:93110. http://dx.doi.org/10.1016/S0167-5877(98)00151-2CrossRefGoogle Scholar
Petersen, B, Knura-Desczka, S, Pönsgen-Schmidt, E and Gymnich, S 2002 Computerised food safety monitoring in animal production. Livestock Production Science 76: 207213. http://dx.doi.org/10.1016/S0301-6226(02)00120-3CrossRefGoogle Scholar
Pilon, J, Higgins, H and Quessy, S 2000 Epidemiological study of Yersinia enterocolitica in swine herds in Quebec. Canadian Veterinary Journal 41: 383387Google ScholarPubMed
Rostagno, MH 2009 Can stress in farm animals increase food safety risk? Foodborne Pathogens and Disease 6: 767776. http://dx.doi.org/10.1089/fpd.2009.0315CrossRefGoogle ScholarPubMed
Rostagno, MH, Eicher, SD and Lay, DC Jr 2011 Immunological, physiological, and behavioral effects of Salmonella enterica carriage and shedding in experimentally infected finishing pigs. Foodborne Pathogens and Disease 8: 623630. http://dx.doi.org/10.1089/fpd.2010.0735CrossRefGoogle ScholarPubMed
Smith, RP, Sanchez-Vazquez, MJ, Cook, AJC and Edwards, SA 2011 Abattoir-based study investigating the association between gross pathological lesions and serological tests for Salmonella infection in pigs. Veterinary Record 168: 240. http://dx.doi.org/10.1136/vr.c6823CrossRefGoogle ScholarPubMed
Temple, D, Dalmau, A, Ruiz de la Torrea, JL, Manteca, X and Velarde, A 2011 Application of the Welfare Quality®pro-tocol to assess growing pigs kept under intensive conditions in Spain. Journal Veterinary Behavior 6: 138149. http://dx.doi.org/10.1016/j.jveb.2010.10.003CrossRefGoogle Scholar
Verbrugghe, E, Boyen, F, Gaastra, W, Bekhuis, L, Leyman, B, Van Parys, A, Haesebrouck, F and Pasmans, F 2011 The complex interplay between stress and bacterial infections in ani-mals. Veterinary Microbiology 23: 115127Google Scholar
Von-Borell, E, Bockisch, FJ, Büscherc, W, Hoy, S, Krieter, J, Müller, C, Parvizi, N, Richter, T, Rudovsky, A, Sundrum, A and Van den Weghe, H 2001 Critical control points for on-farm assessment of pig housing. Livestock Production Science 72:177184. http://dx.doi.org/10.1016/S0301-6226(01)00278-0CrossRefGoogle Scholar
Welfare Quality® 2009 Welfare Quality®Assessment Protocol for Pigs. Welfare Quality® Consortium: Lelystad, The NetherlandsGoogle Scholar
Whay, HR, Main, DCJ, Green, LE and Webster, AJF 2003 Animal-based measures for the assessment of welfare state of dairy cattle, pigs and laying hens: consensus of expert opinion. Animal Welfare 12: 205217Google Scholar
Zheng, DM, Bonde, M and Sørensen, JT 2007 Associations between the proportion of Salmonella seropositive slaughter pigs and the presence of herd level risk factors for introduction and transmission of Salmonella in 34 Danish organic, outdoor (non-organic) and indoor finishing-pig farms. Livestock Science 106: 189199. http://dx.doi.org/10.1016/j.livsci.2006.08.003CrossRefGoogle Scholar
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