Skip to main content Accessibility help
Hostname: page-component-768dbb666b-7lw58 Total loading time: 0.36 Render date: 2023-02-03T02:02:35.108Z Has data issue: true Feature Flags: { "useRatesEcommerce": false } hasContentIssue true

Animal welfare as preventative medicine

Published online by Cambridge University Press:  01 January 2023

MS Dawkins*
University of Oxford, Department of Zoology, Oxford OX1 3SZ, UK


Antimicrobial resistance is a major threat to both human and animal health, but reduction of use raises issues of how standards of animal health and welfare can be maintained without them. This turns the spotlight onto the role of good management and higher standards of animal welfare as drug-free ways of improving immune function and increasing resistance to infection. Research is urgently needed into the relationship between animal welfare, immunity, gut microbiota and disease and we are not yet in a position to claim that improving welfare will improve resistance to disease. ‘Boosting’ the immune system is not straightforward and an interdisciplinary approach is needed.

© 2019 Universities Federation for Animal Welfare

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Aidara-Kane, A, Angulo, FJ, Conly, J, Minato, Y, Silbergeld, EK, McEwen, SA and Collignon, PJ 2018 World Health Organisation (WHO) guidelines on use of medically important microbials in food-processing animals. Antimicrobial Resistance and Infection Control 7: AR7. Scholar
Angelakis, E 2017 Weight gain by gut microbiota manipulation in production animals. Microbial Pathogenesis 106: 162170. Scholar
Arranz, L, de Vicente, A, Munoz, M and de la Fuente, M 2009 Impaired immune function in a homeless population with stress-related disorders. Neuroimmunomodulation 16: 251260. Scholar
Bailey, MT and Cryan, JF 2017 The microbiome as a key regu-lator of brain, behaviour and immunity. Brain Behavior and Immunity 66: 1822. Scholar
Bartolomucci, A 2007 Social stress, immune function and dis-ease in rodents. Frontiers in Neuroendocronology 28: 2849. Scholar
Berghman, LR 2016 Immune responses to improving welfare Poultry Science 95: 22162218. ScholarPubMed
Berk, M, Williams, LJ, Jacka, FN, O’Neil, A, Pasco, JA, Moylan, S, Allen, NB, Stuart, AL, Hayley, AC, Byrne, ML and Maes, M 2013 So depression is an inflammatory disease, but where does the inflammation come from? BMC Medicine 11: AR 200. Scholar
Best, A and Hoyle, A 2013 The evolution of costly acquired immune memory. Ecology and Evolution 3: 22232232. ScholarPubMed
Boissy, A, Manteuffel, G, Jensen, MB, Oppermann, M, Spruijt, B, Keeling, LJ, Winckler, C, Forkman, B, Dimitrov, I, Langbein, J, Bakken, M, Veissier, I and Aubert, A 2007 Assessment of positive emotions in animals to improve their wel-fare. Physiology & Behavior 92: 375397. Scholar
Boots, M, Donnelly, R and White, A 2013 Optimal immune defence in the light of variation in lifespan. Parasite Immunology 35:331338. ScholarPubMed
Brock, PM, Hall, AJ, Goodman, SJ, Cruz, M and Acevedo-Whitehouse, K 2013 Immune activity. Body condition and human-associated environmental impacts in a wild marine mam-mal. PLOS One 8: AR E67132Google Scholar
Broom, DM and Johnson, KG 1993 Stress and Animal Welfare. Chapman and Hall: London, UK. Scholar
Christiansen, SH, Murphy, RA, Juul-Madsen, K, Fredborg, M, Hvam, ML, Axelgaard, E, Skovdal, SM, Meyer, RL, Skov Sørensen, UB, Möller, A, Nyengaard, JR, Nørskov-Lauritsen, N, Wang, M, Gadjeva, M, Howard, KA, Davies, JC, Petersen, E and Vorup-Jensen, T 2017 The immunomod-ulatory drug glatiramer acetate is also an effective antimicrobial agent that kills gram negative bacteria. Nature Scientific Reports article no 15653. Scholar
Cockram, S and Hughes, BO 2011 Health and disease. In: Appleby, MC, Mench, JA, Olsson, IAS and Hughes, BO (eds) Animal Welfare, Second Edition pp 12137. CABI: Wallingford, UK. Scholar
Dantzer, R, O-Connor, JC, Freund, GG, Johnson, RW and Kelley, KW 2008 From inflammation to sickness and depression: when the immune system subjugates the brain. Nature Reviews Neuroscience 9: 4657Google ScholarPubMed
Dawkins, MS 2008 The science of animal suffering. Ethology 114:937945. Scholar
ECDC (European Centre for Disease Prevention and Control), EFSA (European Food Safety Authority), and EMA (European Medicines Agency) 2017 ECDC/EFSA/EMA second joint report on the integrated analysis of the consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals – Joint Interagency Antimicrobial Consumption and Resistance Analysis (JIACRA) Report. EFSA Journal 15(7): 4872. Scholar
Ekkel, ED, Hessing, MJC and Tielen, MJM 1995 The specific-stress-free housing system has positive effects on productivity, health and welfare of pigs. Journal of Animal Science 73: 15441551. ScholarPubMed
Evans, K, Buchanan, KL, Griffith, SC, Klasing, KC and Addison, BA 2017 Ecoimmunology and microbial ecology: Contributions to avian behavior, physiology, and life history. Hormones and Behavior 88: 112121. ScholarPubMed
Gao, P, Ma, C, Sun, Z, Wang, L, Huang, S, Su, X, Xu, J and Zhang, H 2017 Feed-additive probiotics accelerate yet antibiotics delay intestinal microbiota maturation in broiler chicken. Microbiome 5: AR UNSP9 Scholar
Gimeno, C, Postma, M, Dewulf, J, Hogeveen, H, Laywers, L and Wauters, E 2016 Farm-economic analysis of reducing antimicrobial use while adopting improved management strategies on farrow-to-finish pig farms. Preventative Veterinary Medicine 129:7487. Scholar
Gross, WB and Siegel, PB 1981 Long-term exposure of chick-ens to three levels of social stress. Avian Disease 25: 312326. ScholarPubMed
Gross, WB and Siegel, HS 1983 Evaluation of the heterophil lymphocyte ratio as a measure of stress in chickens. Avian Diseases 27: 972979. ScholarPubMed
Hoerr, FJ 2010 Clinical aspects of immunosuppression in poultry. Avian Disease 54: 215. ScholarPubMed
Horsdal, HT, Kohlerorsberg, O, Benros, ME and Gasse, C 2017 C-reactive protein and white blood cell levels in schizophre-nia, bipolar disorders and depression-associations with mortality and psychiatric outcomes: a population-based study. European Psychiatry 44: 164172. Scholar
Houston, A, McNamara, JM, Barta, Z and Klasing, KC 2007 The effect of energy reserves and food availability on optimal immune defence. Proceedings of the Royal Society B274: 28352847. Scholar
Hudson, JA, Frewer, LJ, Jones, G, Brereton, PA, Whittingham, MJ and Stewart, G 2017 The agri-food chain and antimicrobial resistance: a review. Trends in Food Science and Technology 69: 131147. Scholar
Humphrey, BD and Klasing, KC 2004 Modulation of nutrient metabolism and homeostasis by the immune system. World's Poultry Science Journal 60: 90100. Scholar
Ingvarten, KL and Moyes, K 2013 Nutrition, immune function and health in dairy cattle. Animal 7: 122122Google Scholar
Iseri, VJ and Klasing, KC 2013 Dynamics of the systemic com-ponents of the chicken (Gallus gallus domesticus) immune system following activation by Escherichia coli: implications for the cost of immunity. Developmental Comparative Immunology 40: 248257. Scholar
Kaiser, P 2010 Advances in avian immunology: prospects for dis-ease control. A review. Avian Pathology 39: 309324. Scholar
Kemper, N 2008 Veterinary antibiotics in the aquatic and terres-trial environment. Ecological Indicators 8: 113. Scholar
Kidd, MT 2004 Nutritional modulation of immune function in broil-ers. Poultry Science 83: 650657. Scholar
Klasing, KC 2007 Nutrition and the immune system. British Poultry Science 48: 529537. ScholarPubMed
Kogut, MH and Klasing, K 2009 An immunologist's perspective on nutrition, immunity, and infectious diseases: Introduction and overview. Journal of Applied Poultry Research 18: 103110. Scholar
Lafuse, WP, Gearinger, R, Fisher, S, Nealer, C, Mackos, AR and Bailey, MT 2017 Exposure to a social stressor induces translocation of commensal Lactobacilli to the spleen and priming of the innate immune system. Journal of Immunology 198: 23832393. Scholar
Lennox, BR, Palmer-Cooper, EC and Pollak, T 2017 Prevalence and clinical characteristics of serum neuronal cell sur-face antibodies in first-episode psychosis: a case-control study. Lancet Psychiatry 4: 4248. Scholar
Leonard, BE 2018 Inflammation and depression: causal or coin-cidental link to the pathophysiology? Acta Neuropsychiatrica 30: 116. ScholarPubMed
Li, P, Yin, Y, Li, D and Wu, G 2007 Amino acids and immune function. British Journal of Nutrition 98: 237252. ScholarPubMed
Maes, M 2011 Depression as an inflammatory disease, but cell-mediated immune activation is the key component of depression. Progress in Neuro-psychopharmacology and Biological Psychiatry 35:664675. ScholarPubMed
McEwen, SA and Fedorka-Cray, PJ 2002 Antimicrobial use and resistance in animals. Clinical Infectious Diseases 34: S93S106. ScholarPubMed
McKean, KA, Yourth, CP, Lazzaro, BP and Clark, AG 2008 The evolutionary costs of immunological maintenance and deployment. Evolutionary Biology 8 AR 76. Scholar
Mendl M, Burman OHP and ES Paul 2010 An integrative and functional framework for the study of animal emotion and mood. Proceedings of the Royal Society B277: 28952904. Scholar
Moberg, GP 1985 Biological responses to stress: Key to assess-ment of animal well-being? In: Moberg, GP (eds) Animal Stress pp 2749. American Philosophical Society: Bethesda, Maryland, USA. Scholar
Murtaugh, MP, Steer, CJ, Sreeevatsan, S, Patterson, N, Kennedy, S and Sriramaran, P 2017 The science behind One Health: at the interface of humans, animals and the environment. Annals of the New York Academy of Sciences 1395: 1232. ScholarPubMed
Nakata, A, Takahashi, M, Irie, M and Swanson, NG 2010 Job satisfaction is associated with elevated natural killer cell immunity among healthy, white-collar employees. Brain, Behavior and Immunity 24: 12681275. ScholarPubMed
Shapiro, SJ 2002 Effects of social manipulations and environmen-tal enrichment on behaviour and cell-mediated immune respons-es in rhesus macaques. Pharmacology, Biochemistry, and Behavior 73:271278. Scholar
Silbergeld, EK, Graham, J and Price, LB 2008 Industrial food animal production, antimicrobial resistance and human health. Annual Review of Public Health 29: 151169. ScholarPubMed
Steiner, J, Bogerts, B, Sarnyai, Z, Walter, M, Bernstein, H-G and Myint, A-M 2012 Bridging the gap between the immune and glutamate hypotheses of schizophrenia and major depression: potential role of glial NMDA receptor modulators and impaired blood-brain barrier integrity. World Journal of Biological Psychiatry 13:482492. ScholarPubMed
Stephenson, JF, van Opsterhout, C and Cable, J 2015 Pace of life, predators and parasites: predator-induced life-history evolution in Trinidadian guppies predicts decrease in parasite tolerance. Biology Letters 11: AR 20150806CrossRefGoogle Scholar
Takao, Y, Okuno, Y, Mori, Y, Asasa, H, Yamanishi, K and Iso, H 2018 Associations of perceived mental stress, sense of purpose in life, and negative life events with the risk of incident herpes Zoster and postherpetic neuralgia. American Journal of Epidemiology 187: 251259. ScholarPubMed
Teuber, M 2001 Veterinary use and antibiotic resistance. Current Opinion in Microbiology 4: 493499. ScholarPubMed
Van Boeckel, TP, Brower, C, Gilbert, M, Grenfell, , Levin, SA, Robinson, TP, Teillant, A and Laxminarayan, R 2015 Global trends in antimicrobial use in food animals. Proceedings of the National Academy of Science 112: 56495654. ScholarPubMed
Veissier, I and Miele, M 2015 Short historical overview of ani-mal welfare sciences: how a societal concern has become a trans-disciplinary subject. INRA Productions Animales 28: 399409CrossRefGoogle Scholar
Vermette, CJ, Henrikson, ZA, Schwean-Lardner, KV and Crowe T, G 2017 Influence of hot exposure on 12-week-old turkey hen physiology, welfare, and meat quality and 16-week-old turkey tom core body temperature when crated at transport den-sity. Poultry Science 96(11): 38363843. Scholar
Yeoman, CJ, White, BA, Lewis, HA and Roberts, RM 2014 Gastrointestinal tract microbiota and probiotics in production animals. Annual Review of Animal Biosciences 2: 469486. ScholarPubMed
Ying, GG, He, LY, Ying, AJ, Zhang, QQ, Liu, YS and Zhao, JI 2017 China must reduce its antibiotic use. Environmental Science Technology 51: 10721073. ScholarPubMed
Zuk, M and Stoehr, AM 2010 Sex differences in susceptibility to infection: an evolutionary perspective. In: Klein, SL and Roberts, CW (eds) Sex Hormones and Immunity to Infection pp 110. Springer-Verlag: Berlin, Germany. Scholar
Zylberberg, M, Klasing, KC and Hahn, TO 2013 House finch-es (Carpodacus mexicanus) balance investment in behavioural and immunological defences against pathogens. Integrative and Comparative Biology 53(S1): E400Google Scholar
Cited by

Save article to Kindle

To save this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the or variations. ‘’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Animal welfare as preventative medicine
Available formats

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

Animal welfare as preventative medicine
Available formats

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

Animal welfare as preventative medicine
Available formats

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *