How animal agriculture stakeholders define, perceive, and are impacted by antimicrobial resistance: challenging the Wellcome Trust’s Reframing Resistance principles

Abstract

Humans, animals, and the environment face a universal crisis: antimicrobial resistance (AR). Addressing AR and its multi-disciplinary causes across many sectors including in human and veterinary medicine remains underdeveloped. One barrier to AR efforts is an inconsistent process to incorporate the plenitude of stakeholders about what AR is and how to stifle its development and spread—especially stakeholders from the animal agriculture sector, one of the largest purchasers of antimicrobial drugs. In 2019, The Wellcome Trust released Reframing Resistance: How to communicate about antimicrobial resistance effectively (Reframing Resistance), which proposed the need to establish a consistent and harmonized messaging effort that describes the AR crisis and its global implications for health and wellbeing across all stakeholders. Yet, Reframing Resistance does not specifically engage the animal agriculture community. This study investigates the gap between two principles recommended by Reframing Resistance and animal agriculture stakeholders. For this analysis, the research group conducted 31 semi-structured interviews with a diverse group of United States animal agriculture stakeholders. Participants reported attitudes, beliefs, and practices about a variety of issues, including how they defined AR and what entities the AR crisis impacts most. Exploration of Reframing Resistance’s Principle 2, “explain the fundamentals succinctly” and Principle 3, “emphasis that this is universal issue; it can affect anyone, including you” reveals disagreement in both the fundamentals of AR and consensus of “who” the AR crisis impacts. Principle 2 may do better to acknowledge that animal agriculture stakeholders espouse a complex array of perspectives that cannot be summed up in a single perspective or principle. As a primary tool to combat AR, behavior change must be accomplished first through outreach to stakeholder groups and understanding their perspectives.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

Abbreviations

AR:

Antimicrobial resistance

Reframing resistance:

How to communicate about antimicrobial resistance effectively

Wellcome:

The Wellcome Trust

U.S.:

United States

USDA:

United States Department of Agriculture

WHO:

World Health Organization

OIE:

World Organisation for Animal Health

NGO:

Non-governmental Organization

FAO:

Food and Agriculture Organization of the United Nations

References

  1. Banfield Pet Hospital. 2017. Are We Doing Our Part to Prevent Superbugs?

  2. Baron, P., and S. Frattaroli. 2016. Awareness and perceptions of food safety risks and risk management in poultry production and slaughter: a qualitative study of direct-market poultry producers in Maryland. PLoS ONE. https://doi.org/10.1371/journal.pone.0158412.

    Article  Google Scholar 

  3. Bell, B.G., F. Schellevis, E. Stobberingh, H. Goossens, and M. Pringle. 2014. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance. BMC Infectious Diseases 14: 13. https://doi.org/10.1186/1471-2334-14-13.

    Article  Google Scholar 

  4. Blanchette, A. 2019. Living waste and the labor of toxic health on American Factory Farms. Medical Anthropology Quarterly 33: 80–100. https://doi.org/10.1111/maq.12491.

    Article  Google Scholar 

  5. Castillo Neyra, R., L. Vegosen, M.F. Davis, L. Price, and E.K. Silbergeld. 2012. Antimicrobial-resistant bacteria: an unrecognized work-related risk in food animal production. Safety and Health at Work 3: 85–91. https://doi.org/10.5491/SHAW.2012.3.2.85.

    Article  Google Scholar 

  6. Chantziaras, I., F. Boyen, B. Callens, and J. Dewulf. 2014. Correlation between veterinary antimicrobial use and antimicrobial resistance in food-producing animals: a report on seven countries. Journal of Antimicrobial Chemotherapy 69: 827–834. https://doi.org/10.1093/jac/dkt443.

    Article  Google Scholar 

  7. CIDRAP. 2019. Experts urge better antimicrobial resistance messaging.

  8. Coyne, L.A., G.L. Pinchbeck, N.J. Williams, R.F. Smith, S. Dawson, R.B. Pearson, and S.M. Latham. 2014. Understanding antimicrobial use and prescribing behaviours by pig veterinary surgeons and farmers: a qualitative study. Veterinary Record 175: 593. https://doi.org/10.1136/vr.102686.

    Article  Google Scholar 

  9. Creswell, J.W. 2003. RESEARCH DESIGN Qualitative, Quantitative. and Mixed Methods Approaches SECOND EDITION SAGE Publications International Educational and Professional Publisher Thousand Oaks London New Delhi.

  10. CVM, and FDA. 2017. 2017 Summary Report On Antimicrobials Sold or Distributed for Use in Food-Producing Animals.

  11. Dadgostar, P. 2019. Antimicrobial resistance: implications and costs. Infection and Drug Resistance 12: 3903–3910. https://doi.org/10.2147/IDR.S234610.

    Article  Google Scholar 

  12. Davis, M.F., and L. Rutkow. 2012. Regulatory strategies to combat antimicrobial resistance of animal origin: recommendations for a science-based U.S. Approach . Tulane Environmental Law Journal 25: 327–388.

    Google Scholar 

  13. Economou, V., and P. Gousia. 2015. Agriculture and food animals as a source of antimicrobial-resistant bacteria. Infection and Drug Resistance 8: 49–61. https://doi.org/10.2147/IDR.S55778.

    Article  Google Scholar 

  14. Edgar, T. 2012. Communication and behavior change challenges to limiting the development of antibiotic resistance. Journal of General Internal Medicine 27: 758–759. https://doi.org/10.1007/s11606-012-2000-1.

    Article  Google Scholar 

  15. Edgar, T., S.D. Boyd, and M.J. Palamé. 2009. Sustainability for behaviour change in the fight against antibiotic resistance: a social marketing framework. Journal of Antimicrobial Chemotherapy 63: 230–237. https://doi.org/10.1093/jac/dkn508.

    Article  Google Scholar 

  16. Ekakoro, J.E., M. Caldwell, E.B. Strand, and C.C. Okafor. 2019. Drivers, alternatives, knowledge, and perceptions towards antimicrobial use among Tennessee beef cattle producers: a qualitative study. BMC Veterinary Research 15: 1–14. https://doi.org/10.1186/s12917-018-1731-6.

    Article  Google Scholar 

  17. Ferguson, C. 2019. Animal agriculture is not the cause of antibiotic resistance. Baltimore Sun, May 16.

  18. Ferreira, J.P. 2017. Why antibiotic use data in animals needs to be collected and how this can be facilitated. Frontiers in Veterinary Science. https://doi.org/10.3389/fvets.2017.00213.

    Article  Google Scholar 

  19. Food and Drug Administration (FDA). 2019. List of Medically Important Antimicrobial Drugs Affected by GFI #213. https://www.fda.gov/animal-veterinary/judicious-use-antimicrobials/list-medically-important-antimicrobial-drugs-affected-gfi-213. Accessed 7 May 2019.

  20. Fortané, N. 2019. Veterinarian ‘responsibility’: conflicts of definition and appropriation surrounding the public problem of antimicrobial resistance in France. Palgrave Communications 5: 8. https://doi.org/10.1057/s41599-019-0273-2.

    Article  Google Scholar 

  21. FSIS, USDA. 2019. Food Safety and Inspection Service Labeling Guideline on Documentation Needed to Substantiate Animal Raising Claims for Label Submissions December 2019: 1–18.

  22. Furuya, E.Y., and F.D. Lowy. 2006. Antimicrobial-resistant bacteria in the community setting. Nature Reviews Microbiology 4: 36–45. https://doi.org/10.1038/nrmicro1325.

    Article  Google Scholar 

  23. Glover, Rebecca, Clare Chandler, John Manton, and MP Petticrew. 2019. The benefits and risks of public awareness campaigns: World Antibiotic Awareness Week in context—The BMJ. BMJ.

  24. Goossens, H., M. Ferech, R.V. Stichele, and M. Elseviers. 2005. Outpatient antibiotic use in Europe and association with resistance: a cross-national database study. Lancet (London, England) 365: 579–587. https://doi.org/10.1016/S0140-6736(05)17907-0.

    Article  Google Scholar 

  25. Hawkings, N.J., F. Wood, and C.C. Butler. 2007. Public attitudes towards bacterial resistance: a qualitative study. The Journal of Antimicrobial Chemotherapy 59: 1155–1160. https://doi.org/10.1093/jac/dkm103.

    Article  Google Scholar 

  26. Hicks, L.A., T.H. Taylor, and R.J. Hunkler. 2010. Outpatient antibiotic prescribing according to antibiotic category, antibiotic agent, geographic region, patient age, and provider specialty. New England Journal of Medicine 368: 1461–1462. https://doi.org/10.1056/NEJMc1212055.

    Article  Google Scholar 

  27. Holmberg, S.D., J.G. Wells, and M.L. Cohen. 1984. Animal-to-man transmission of antimicrobial-resistant Salmonella: investigations of U.S. outbreaks, 1971–1983. Science (New York, N.Y.) 225: 833–835. https://doi.org/10.1126/science.6382605.

    Article  Google Scholar 

  28. Hummel, R., H. Tschäpe, and W. Witte. 1986. Spread of plasmid-mediated nourseothricin resistance due to antibiotic use in animal husbandry. Journal of Basic Microbiology 26: 461–466. https://doi.org/10.1002/jobm.3620260806.

    Article  Google Scholar 

  29. Innes, G.K., P.R. Randad, A. Korinek, M.F. Davis, L.B. Price, A.D. So, and C.D. Heaney. 2020. External Societal Costs of Antimicrobial Resistance in Humans Attributable to Antimicrobial Use in Livestock. Annual Review of Public Health: No. 26189. https://doi.org/https://doi.org/10.1146/annurev-publhealth-040218-043954.

  30. Institute of Medicine. 1989. Human Health Risks With the Subtherapeutic Use of Penicillin or Tetracyclines in Animal Feed. Washington, DC: The National Academies Press. https://doi.org/https://doi.org/10.17226/19030.

  31. Kallel, H., F. Mahjoubi, H. Dammak, M. Bahloul, C.B. Hamida, H. Chelly, N. Rekik, A. Hammami, and M. Bouaziz. 2008. Correlation between antibiotic use and changes in susceptibility patterns of Pseudomonas aeruginosa in a medical-surgical intensive care unit. Indian Journal of Critical Care Medicine : Peer-Reviewed, Official Publication of Indian Society of Critical Care Medicine 12: 18–23. https://doi.org/10.4103/0972-5229.40945.

    Article  Google Scholar 

  32. Kirchhelle, C. 2020. Pyrrhic progress: the history of antibiotics in Anglo-American food production. New Brunswick, NJ: Rutgers University Press.

    Google Scholar 

  33. Knights, C.B., A. Mateus, and S.J. Baines. 2012. Current British veterinary attitudes to the use of perioperative antimicrobials in small animal surgery. The Veterinary Record 170: 646. https://doi.org/10.1136/vr.100292.

    Article  Google Scholar 

  34. Landers, T.F., B. Cohen, T.E. Wittum, and E.L. Larson. 2012. A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Reports 127: 4–22. https://doi.org/10.1177/003335491212700103.

    Article  Google Scholar 

  35. Levy, S.B., G.B. FitzGerald, and A.B. Macone. 1976. Changes in intestinal flora of farm personnel after introduction of a tetracycline-supplemented feed on a farm. The New England Journal of Medicine 295: 583–588. https://doi.org/10.1056/NEJM197609092951103.

    Article  Google Scholar 

  36. Liu, T., R.J.F. Bruins, and M.T. Heberling. 2018. Factors influencing farmers’ adoption of best management practices: a review and synthesis. Sustainability 10: 432. https://doi.org/10.3390/su10020432.

    Article  Google Scholar 

  37. MacFadden, D.R., S.F. McGough, D. Fisman, M. Santillana, and J.S. Brownstein. 2018. Antibiotic resistance increases with local temperature. Nature Climate Change 8: 510–514. https://doi.org/10.1038/s41558-018-0161-6.

    Article  Google Scholar 

  38. Magouras, I., L.P. Carmo, K.D.C. Stärk, and G. Schüpbach-Regula. 2017. Antimicrobial usage and -resistance in livestock: where should we focus? Frontiers in Veterinary Science. https://doi.org/10.3389/fvets.2017.00148.

    Article  Google Scholar 

  39. Maibach, E.W., L.C. Abroms, and M. Marosits. 2007. Communication and marketing as tools to cultivate the public’s health: a proposed “people and places” framework. BMC Public Health 7: 88. https://doi.org/10.1186/1471-2458-7-88.

    Article  Google Scholar 

  40. Maron, D.F., T.J.S. Smith, and K.E. Nachman. 2013. Restrictions on antimicrobial use in food animal production: an international regulatory and economic survey. Globalization and Health 9: 48. https://doi.org/10.1186/1744-8603-9-48.

    Article  Google Scholar 

  41. Mas, F.S., A.J. Handal, R.E. Rohrer, and E.T. Viteri. 2017. Health and safety in organic farming: a qualitative study. Journal of Agromedicine 23: 92–104. https://doi.org/10.1080/1059924X.2017.1382409.

    Article  Google Scholar 

  42. McEwen, S.A., and P.J. Collignon. 2018. Antimicrobial resistance: a one health perspective. In Antimicrobial resistance in bacteria from livestock and companion animals, 521–547. American Society of Microbiology. https://doi.org/https://doi.org/10.1128/microbiolspec.arba-0009-2017.

  43. Messenger, A.M., A.N. Barnes, and G.C. Gray. 2014. Reverse zoonotic disease transmission (Zooanthroponosis): a systematic review of seldom-documented human biological threats to animals. PLoS ONE. https://doi.org/10.1371/journal.pone.0089055.

    Article  Google Scholar 

  44. Michie, S., M.M. van Stralen, and R. West. 2011. The behaviour change wheel: a new method for characterising and designing behaviour change interventions. Implementation Science 6: 42. https://doi.org/10.1186/1748-5908-6-42.

    Article  Google Scholar 

  45. Miles, M.B., and A.M. Huberman. 1994. Qualitative Data Analysis A Methods Sourcebook Edition. Edited by Rebecca Holland. Second Edition. Thousand Oaks, California: SAGE Publications.

  46. National Institute of Child Health and Human Development. 2000. Chapter 4: Comprehension. In National Reading Panel. Teaching children to read: An evidence-based assessment of the scientific research literature on reading and its implications for reading instruction. Bethesda, MD: NIH Publication No.00–4769.

  47. Nordstrom, L., C.M. Liu, and L.B. Price. 2013. Foodborne urinary tract infections: a new paradigm for antimicrobial-resistant foodborne illness. Frontiers in Microbiology 4: 29. https://doi.org/10.3389/fmicb.2013.00029.

    Article  Google Scholar 

  48. Norris, J.M., A. Zhuo, M. Govendir, S.J. Rowbotham, M. Labbate, C. Degeling, G.L. Gilbert, D. Dominey-Howes, and M.P. Ward. 2019. Factors influencing the behaviour and perceptions of Australian veterinarians towards antibiotic use and antimicrobial resistance. PLoS ONE 14: e0223534–e0223534.

    Article  Google Scholar 

  49. O’Neill, J. 2014. AMR Review Paper-Tackling a crisis for the health and wealth of nations. AMR Review Paper.

  50. O’Neill, J. 2016. Tackling drug-resistant infections globally: final report and recommendations. Government of the United Kingdom. APO-63983.

  51. Oishi, S. 1984. A search for the ideal society. The assimilation of immigrants into American life. Journal of UOEH 6: 109–120. https://doi.org/10.7888/juoeh.6.109.

    Article  Google Scholar 

  52. Olesen, S.W., M.L. Barnett, D.R. MacFadden, J.S. Brownstein, S. Hernández-Díaz, M. Lipsitch, and Y.H. Grad. 2018. The distribution of antibiotic use and its association with antibiotic resistance. eLife 7: e39435. https://doi.org/10.7554/eLife.39435.

    Article  Google Scholar 

  53. Pearson, M., and C. Chandler. 2019. Knowing antmicrobial resistance in practice: a multi-country qualitative study with human and animal healthcare professionals. Global Health Action 12: 1599560. https://doi.org/10.1080/16549716.2019.1599560.

    Article  Google Scholar 

  54. Peters, D.H. 2014. The application of systems thinking in health: why use systems thinking? Health research policy and systems 12. BioMed Central. https://doi.org/10.1186/1478-4505-12-51.

    Article  Google Scholar 

  55. Phillips, I., M. Casewell, T. Cox, B. De Groot, C. Friis, R. Jones, C. Nightingale, R. Preston, and J. Waddell. 2004. Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. Journal of Antimicrobial Chemotherapy 53: 28–52. https://doi.org/10.1093/jac/dkg483.

    Article  Google Scholar 

  56. Podolsky, S.H. 2018. The evolving response to antibiotic resistance (1945–2018). Palgrave Communications 4: 124. https://doi.org/10.1057/s41599-018-0181-x.

    Article  Google Scholar 

  57. Pomba, C., M. Rantala, C. Greko, K.E. Baptiste, B. Catry, E. van Duijkeren, A. Mateus, et al. 2017. Public health risk of antimicrobial resistance transfer from companion animals. The Journal of Antimicrobial Chemotherapy 72. England: 957–968. https://doi.org/https://doi.org/10.1093/jac/dkw481.

  58. Ricke, S.C. 2012. Organic meat production and processing. Hoboken, NJ: Wiley.

    Google Scholar 

  59. Riedel, S., S.E. Beekmann, K.P. Heilmann, S.S. Richter, J. Garcia-de-Lomas, M. Ferech, H. Goosens, and G.V. Doern. 2007. Antimicrobial use in Europe and antimicrobial resistance in Streptococcus pneumoniae. European Journal of Clinical Microbiology & Infectious Diseases: Official Publication of the European Society of Clinical Microbiology 26: 485–490. https://doi.org/10.1007/s10096-007-0321-5.

    Article  Google Scholar 

  60. Rochefort, D.A., and R.W. Cobb, eds. 1994. The politics of problem definition: shaping the policy agenda. Studies in government and public policy. Lawrence, Kan: University Press of Kansas.

    Google Scholar 

  61. Saldaña, J. 2015. Chapter 1. An introduction to codes and coding. The coding manual for qualitative researchers, 1–31. Los Angeles, California: SAGE.

  62. Silbergeld, E.K., J. Graham, and L.B. Price. 2008. Industrial food animal production, antimicrobial resistance, and human health. Annual Review of Public Health 29: 151–169. https://doi.org/10.1146/annurev.publhealth.29.020907.090904.

    Article  Google Scholar 

  63. Sinclair, M., C. Fryer, and C.J.C. Phillips. 2019. The benefits of improving animal welfare from the perspective of livestock stakeholders across asia. Animals. MDPI AG. https://doi.org/https://doi.org/10.3390/ani9040123.

  64. Smith, T.C., M.F. Davis, and C.D. Heaney. 2018. Pig movement and antimicrobial use drive transmission of livestock-associated Staphylococcus aureus CC398. https://doi.org/https://doi.org/10.1128/mBio.02142-18.

  65. Suzuki, S., A. Pruden, M. Virta, and T. Zhang. 2017. Editorial: Antibiotic resistance in aquatic systems. Frontiers in Microbiology 8: 14.

    Google Scholar 

  66. Thakur, S., and G.C. Gray. 2019. The mandate for a global “one health” approach to antimicrobial resistance surveillance. American Journal of Tropical Medicine and Hygiene. https://doi.org/10.4269/ajtmh.18-0973.

    Article  Google Scholar 

  67. Thomas, J., and D. McDonagh. 2013. Shared language:Towards more effective communication. The Australasian medical journal 6. Australasian Medical Journal: 46–54. https://doi.org/https://doi.org/10.4066/AMJ.2013.1596.

  68. TNS Opinion & Social. 2010. Special Eurobarometer 338 Report Antimicrobial Resistance. Food Microbiology. https://doi.org/10.1128/9781555818463.ch2.

    Article  Google Scholar 

  69. Tong, A., P. Sainsbury, and J. Craig. 2007. Consolidated criteria for reporting qualitative research (COREQ): a 32-item checklist for interviews and focus groups. International Journal for Quality in Health Care 19: 349–357. https://doi.org/10.1093/intqhc/mzm042.

    Article  Google Scholar 

  70. Walker, S. 2019. Effective antimicrobial resistance communication: the role of information design. Palgrave Communications. https://doi.org/10.1057/s41599-019-0231-z.

    Article  Google Scholar 

  71. Wellcome Trust. 2020. Drug-resistant infections: transforming the global response. https://wellcome.org/what-we-do/our-work/drug-resistant-infections. Accessed 2 Dec 2020.

  72. Trust, Wellcome. 2019a. Reframing Resistance: How to communicate about antimicrobial resistance effectively. London: United Kingdom.

    Google Scholar 

  73. Wellcome Trust. 2019b. Webinar: how to talk about antimicrobial resistance effectively. United Kingdom.

  74. WHO, FAO, and OIE. 2016. Antimicrobial Resistance: A manual for developing national action plans. ISBN: 978 92 4 154953 0.

  75. Williams, M.A. 2019. We can’t despair about our antibiotic crisis. The Washington Post.

  76. World Organisation for Animal Health. 2016. The OIE Strategy on Antimicrobial Resistance and the Prudent Use of Antimicrobials. World Oragnization for Animal Health: 1–12.

Download references

Acknowledgements

We thank all of the animal agriculture stakeholder participants who were gracious and willing to speak their minds and thoughts on record, despite obvious controversies around these issues. We are grateful of Caitlin Ceryes for her help and guidance in qualitative analysis and research. We also acknowledge Joan Casey, Christopher Heaney, and Sara Tartof for their instrumental roles in the ARES Grant and the progression of the ARES project.

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Gabriel K. Innes or Meghan F. Davis VMD, PHD, MPH.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Innes, G.K., Markos, A., Dalton, K.R. et al. How animal agriculture stakeholders define, perceive, and are impacted by antimicrobial resistance: challenging the Wellcome Trust’s Reframing Resistance principles. Agric Hum Values (2021). https://doi.org/10.1007/s10460-021-10197-y

Download citation

Keywords

  • Antimicrobial resistance
  • Animal agriculture
  • Qualitative research
  • Antimicrobial use
  • Animal husbandry
  • One Health