Journal of Public Health Policy

, Volume 39, Issue 4, pp 389–406 | Cite as

Policy options for reducing antibiotics and antibiotic-resistant genes in the environment

  • Ellen Bloomer
  • Martin McKeeEmail author
Original Article


Responses to the threat posed by antimicrobial resistance have been inadequate. Most attention has focused on the emergence of resistant organisms in human medicine and in agriculture. Much less attention has been given to antibiotic contamination of the environment. To assist health advocates to engage with this issue, we review the evidence on the role of agriculture, aquaculture, domestic waste and pharmaceutical manufacturing in the spread of antibiotic resistance, concluding that all of these activities pose a potentially serious threat. We then examine ways that this threat might be mitigated by specific measures, such as improved wastewater treatment processes, reduction of manufacturing emissions, consideration of environmental impacts in procurement and drug approval decisions, and better manure management. We conclude by placing this problem within the growing literature on commercial determinants of health, stressing the need for effective legislation and regulation developed independent of vested interests.


Environment Antimicrobial resistance Agriculture Aquaculture Pharmaceuticals Corporate determinants 


  1. 1.
    Kessler DA. Antibiotics and the meat we eat. New York Times. 2013. Updated 27 Mar 2013. Cited 28 June 2018.
  2. 2.
    O’Neill J. Tackling drug-resistant infections globally: final report and recommendations. London: Review on Antimicrobial Resistance; 2016.Google Scholar
  3. 3.
    United Nations General Assembly. High-level meeting on antimicrobial resistance. New York: UN. 2016. Cited 4 June 2018.
  4. 4.
    Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Levin SA, et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci USA. 2018;115(15):E3463–70.CrossRefGoogle Scholar
  5. 5.
    Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, et al. Global trends in antimicrobial use in food animals. Proc Natl Acad Sci USA. 2015;112(18):5649–54.CrossRefGoogle Scholar
  6. 6.
    Watt H. How much does big pharma make from animal antibiotics? The Guardian. 2018. Updated 19 June 2018. Cited 20 June 2018.
  7. 7.
    Mellon M, Benbrook C, Benbrook KL. Hogging it: estimates of antimicrobial abuse in livestock. Washington DC: Union of Concerned Scientists; 2001.Google Scholar
  8. 8.
    Martin A, Hopkins JS. Trump’s USDA fights global guidelines on livestock antibiotics. Bloomberg. 2018. Cited 28 July 2018.
  9. 9.
    McVeigh K. Scientists: overuse of antibiotics in animal agriculture endangers humans. The Guardian. 2012. Updated 19 Sep 2012. Cited 28 July 2018.
  10. 10.
    Halabi SF. The Codex Alimentarius commission, corporate influence, and international trade: a perspective on FDA’s global role. Am J Law Med. 2015;41(2–3):406–21.CrossRefGoogle Scholar
  11. 11.
    Farming UK. Brexit threatens ‘bold but essential’ EU rules on reducing farm antibiotics, warns MEP. Farming: Farming UK News; 2018. Cited 28 July 2018.
  12. 12.
    Roca I, Akova M, Baquero F, Carlet J, Cavaleri M, Coenen S, et al. The global threat of antimicrobial resistance: science for intervention. New Microbes New Infect. 2015;6:22–9.CrossRefGoogle Scholar
  13. 13.
    World Health Organization. Global Action Plan on antimicrobial resistance. Geneva: World Health Organization; 2015. Accessed 3 Sept 2018.
  14. 14.
    European Commission. A European One Health Action Plan against Antimicrobial Resistance (AMR). 2017. Accessed 3 Sept 2018.
  15. 15.
    Animal Agriculture Alliance. What the centre for a livable future, pew commission & others aren’t telling you about food production. Washington DC: Animal Agriculture Alliance; 2013.Google Scholar
  16. 16.
    Kim BE, Laestadius LI, Lawrence RS, Martin RP, McKenzie SE, Nachman KE, et al. Industrial food animal production in America: examining the impact of the Pew Commission’s Priority Recommendations. Baltimore, MD: Johns Hopkins Center for a Livable Future.Google Scholar
  17. 17.
    Neslen A. Antibiotic apocalypse: EU scraps plans to tackle drug pollution, despite fears of rising resistance. Guardian. 2018. Updated 01 June 2018. Cited 2 June 2018.
  18. 18.
    Responsible Use of Medicines in Agriculture A. RUMA Members. 2018. Cited 20 June 2018.
  19. 19.
    Bodkin H. Brexit Britain should lead the way by banning mass antibiotic use in agriculture, says top doctors. Daily Telegraph; 2018. Cited 20 June 2018.
  20. 20.
    The Bureau of Investigative Journalism. The story behind the mom, the chicken and the superbug threat. The Bureau of Investigative Journalism. 2018. Cited 20 June 2018.
  21. 21.
    Madureira Lima J, Galea S. Corporate practices and health: a framework and mechanisms. Glob Health. 2018;14(1):21.CrossRefGoogle Scholar
  22. 22.
    Greenhalgh T, Thorne S, Malterud K. Time to challenge the spurious hierarchy of systematic over narrative reviews? Eur J Clin Investig. 2018;48(6):e12931.CrossRefGoogle Scholar
  23. 23.
    Wong G, Greenhalgh T, Westhorp G, Buckingham J, Pawson R. RAMESES publication standards: realist syntheses. BMC Med. 2013;11:21.CrossRefGoogle Scholar
  24. 24.
    O’Neill J. Antimicrobials in agriculture and the environment: reducing unnecessary use and waste. The review on antimicrobial resistance.Google Scholar
  25. 25.
    Maron DF, Smith TJ, Nachman KE. Restrictions on antimicrobial use in food animal production: an international regulatory and economic survey. Glob Health. 2013;9(1):48.CrossRefGoogle Scholar
  26. 26.
    Veterinary Medicines Directorate. Understanding the Population Correction Unit used to calculate antibiotic use in food-producing animals. 2016. Cited 4 June 2018.
  27. 27.
    Van Boeckel TP, Glennon EE, Chen D, Gilbert M, Robinson TP, Grenfell BT, et al. Reducing antimicrobial use in food animals. Science. 2017;357(6358):1350–2.CrossRefGoogle Scholar
  28. 28.
    Martinez JL. Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut. 2009;157(11):2893–902.CrossRefGoogle Scholar
  29. 29.
    Watts JE, Schreier HJ, Lanska L, Hale MS. The rising tide of antimicrobial resistance in aquaculture: sources, sinks and solutions. Marine Drugs. 2017;15(6):158.CrossRefGoogle Scholar
  30. 30.
    Burridge L, Weis JS, Cabello F, Pizarro J, Bostick K. Chemical use in salmon aquaculture: a review of current practices and possible environmental effects. Aquaculture. 2010;306(1–4):7–23.CrossRefGoogle Scholar
  31. 31.
    Topp E, Larsson DGJ, Miller DN, Van den Eede C, Virta MPJ. Antimicrobial resistance and the environment: assessment of advances, gaps and recommendations for agriculture, aquaculture and pharmaceutical manufacturing. FEMS Microbiol Ecol. 2018. Scholar
  32. 32.
    Watts JEM, Schreier HJ, Lanska L, Hale MS. The rising tide of antimicrobial resistance in aquaculture: sources, sinks and solutions. Mar Drugs. 2017;15(6):158.CrossRefGoogle Scholar
  33. 33.
    Singer AC, Shaw H, Rhodes V, Hart A. Review of antimicrobial resistance in the environment and its relevance to environmental regulators. Front Microbiol. 2016;7:1728.CrossRefGoogle Scholar
  34. 34.
    Christou A, Aguera A, Bayona JM, Cytryn E, Fotopoulos V, Lambropoulou D, et al. The potential implications of reclaimed wastewater reuse for irrigation on the agricultural environment: the knowns and unknowns of the fate of antibiotics and antibiotic resistant bacteria and resistance genes—a review. Water Res. 2017;123:448–67.CrossRefGoogle Scholar
  35. 35.
    Verlicchi P, Al Aukidy M, Galletti A, Petrovic M, Barcelo D. Hospital effluent: investigation of the concentrations and distribution of pharmaceuticals and environmental risk assessment. Sci Tot Environ. 2012;430:109–18.CrossRefGoogle Scholar
  36. 36.
    Berkner S, Konradi S, Schonfeld J. Antibiotic resistance and the environment–there and back again: Science & Society series on Science and Drugs. EMBO Rep. 2014;15(7):740–4.CrossRefGoogle Scholar
  37. 37.
    Larsson DG. Pollution from drug manufacturing: review and perspectives. Philos Trans R Soc Lond B Biol Sci. 2014;369(1656):20130571.CrossRefGoogle Scholar
  38. 38.
    Larsson DG, de Pedro C, Paxeus N. Effluent from drug manufactures contains extremely high levels of pharmaceuticals. J Hazard Mater. 2007;148(3):751–5.CrossRefGoogle Scholar
  39. 39.
    Grenni P, Anacona V, Caracciolo AB. Ecological effects of antibiotics on natural ecosystems. Microchem J. 2017;136:25–39.CrossRefGoogle Scholar
  40. 40.
    Bueno I, Williams-Nguyen J, Hwang H, Sargeant JM, Nault AJ, Singer RS. Systematic review: Impact of point sources on antibiotic-resistant bacteria in the natural environment. Zoonoses Public Health. 2018;65(1):e162–84.CrossRefGoogle Scholar
  41. 41.
    Bueno I, Williams-Nguyen J, Hwang H, Sargeant JM, Nault AJ, Singer RS. Impact of point sources on antibiotic resistance genes in the natural environment: a systematic review of the evidence. Anim Health Res Rev. 2017;12:1–16.Google Scholar
  42. 42.
    Finley RL, Collignon P, Larsson DG, McEwen SA, Li XZ, Gaze WH, et al. The scourge of antibiotic resistance: the important role of the environment. Clin Infect Dis. 2013;57(5):704–10.CrossRefGoogle Scholar
  43. 43.
    Coleman BL, Salvadori MI, McGeer AJ, Sibley KA, Neumann NF, Bondy SJ, et al. The role of drinking water in the transmission of antimicrobial-resistant E. coli. Epidemiol Infect. 2012;140(4):633–42.CrossRefGoogle Scholar
  44. 44.
    Andersson DI, Hughes D. Microbiological effects of sublethal levels of antibiotics. Nat Rev Microbiol. 2014;12(7):465–78.CrossRefGoogle Scholar
  45. 45.
    Karkman A, Do TT, Walsh F, Virta MP. Antibiotic-resistance genes in waste water. Trends Microbiol. 2017;26(3):220–8.CrossRefGoogle Scholar
  46. 46.
    Lundström SV, Östman M, Bengtsson-Palme J, Rutgersson C, Thoudal M, Sircar T, et al. Minimal selective concentrations of tetracycline in complex aquatic bacterial biofilms. Sci Tot Environ. 2016;553:587–95.CrossRefGoogle Scholar
  47. 47.
    Murray AK, Zhang L, Yin X, Zhang T, Buckling A, Snape J, et al. Novel Insights into Selection for Antibiotic Resistance in Complex Microbial Communities. mBio. 2018;9(4).Google Scholar
  48. 48.
    Ashiru-Oredope D, Hopkins S. Antimicrobial resistance: moving from professional engagement to public action. J Antimicrob Chemother. 2015;70(11):2927–30.CrossRefGoogle Scholar
  49. 49.
    Chaintarli K, Ingle S, Bhattacharya A, Ashiru-Oredope D, Oliver I, Gobin M. Impact of a United Kingdom-wide campaign to tackle antimicrobial resistance on self-reported knowledge and behaviour change. BMC Public Health. 2016;16:393.CrossRefGoogle Scholar
  50. 50.
    O’Neill J. Tackling drug-resistant infections globally: final report and recommendations. London. 2016. Accessed 3 Sept 2018.
  51. 51.
    Pruden A, Larsson DG, Amezquita A, Collignon P, Brandt KK, Graham DW, et al. Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environ Health Perspect. 2013;121(8):878–85.CrossRefGoogle Scholar
  52. 52.
    European Commission. Guidelines for the prudent use of antimicrobials in veterinary medicine (2015/C 299/04). Official Journal of the European Union. 2015. Accessed 3 Sept 2018.
  53. 53.
    EMA (European Medicines Agency), EFSA (European Food Safety Authority). EMA and EFSA Joint Scientific Opinion on measures to reduce the need to use antimicrobial agents in animal husbandry in the European Union, and the resulting impacts on food safety. EFSA J. 2017;15(1):4666.Google Scholar
  54. 54.
    Barancheshme F, Munir M. Strategies to combat antibiotic resistance in the wastewater treatment plants. Front Microbiol. 2017;8:2603.CrossRefGoogle Scholar
  55. 55.
    Michael-Kordatou I, Karaolia P, Fatta-Kassinos D. The role of operating parameters and oxidative damage mechanisms of advanced chemical oxidation processes in the combat against antibiotic-resistant bacteria and resistance genes present in urban wastewater. Water Res. 2018;129:208–30.CrossRefGoogle Scholar
  56. 56.
    Deloitte Sustainabiliy. Background document for public consultation on pharmaceuticals in the environment. 2017. Accessed 3 Sept 2018.
  57. 57.
    Bengtsson-Palme J, Larsson DG. Concentrations of antibiotics predicted to select for resistant bacteria: proposed limits for environmental regulation. Environ Int. 2016;86:140–9.CrossRefGoogle Scholar
  58. 58.
    Changing Markets. Bad Medicine. Addressing pharmaceutical pollution: a key cause of AMR. 2018. Accessed 12 July 2018.
  59. 59.
    European Public Health Alliance. Joint Statement: Europe must align policies to tackle Pharmaceuticals in the Environment and Antimicrobial Resistance. 2018. Accessed 3 Sept 2018.
  60. 60.
    European Public Health Alliance. Investors, NGOs and water industry urge European Commission to take action on pharmaceuticals in the environment and halt Antimicrobial Resistance (AMR). 2018.
  61. 61.
    European Public Health Alliance. EU Health Policy Platform. Joint Statement on Antimicrobial Resistance (AMR). 2018. Accessed 3 Sept 2018.
  62. 62.
    Graham JP, Boland JJ, Silbergeld E. Growth promoting antibiotics in food animal production: an economic analysis. Public Health Rep. 2007;122(1):79–87.CrossRefGoogle Scholar
  63. 63.
    Romero J, Feijoo C, Navarrtet P. Antibiotics in aquaculture—use, abuse and alternatives. In: Carvalho E, David G, Silva R, editors. Health and environment in aquaculture. London: IntechOpen; 2012.Google Scholar
  64. 64.
    Declaration by the Pharmaceutical, Biotechnology and Diagnostics Industries on Combating Antimicrobial Resistance. January 2016. Accessed 3 Sept 2018.
  65. 65.
    Industry Roadmap for Progress on Combating Antimicrobial Resistance. September 2016. Accessed 3 Sept 2018.
  66. 66.
    ECO-PHARMACO-STEWARDSHIP (EPS). A holistic environmental risk management program. Accessed 3 Sept 2018.
  67. 67.
    Cécile K, Mark P, Alison DM, Courtney S, Lesley J, Anushka M, et al. The Public Health Responsibility deal: has a public–private partnership brought about action on alcohol reduction? Addiction. 2015;110(8):1217–25.CrossRefGoogle Scholar
  68. 68.
    Knai C, James L, Petticrew M, Eastmure E, Durand M, Mays N. An evaluation of a public–private partnership to reduce artificial trans fatty acids in England, 2011–2016. Eur J Public Health. 2017;27(4):605–8.CrossRefGoogle Scholar
  69. 69.
    Knai C, Petticrew M, Durand M, Eastmure E, James L, Mehrotra A, et al. Has a public–private partnership resulted in action on healthier diets in England? An analysis of the Public Health Responsibility Deal food pledges. Food Policy. 2015;54:1–10.CrossRefGoogle Scholar
  70. 70.
    Caraher M, Perry I. Sugar, salt, and the limits of self regulation in the food industry. BMJ. 2017;357:1709.CrossRefGoogle Scholar
  71. 71.
    SustainAbility. Tracking progress to address AMR. 2018. Accessed 3 Sept 2018.

Copyright information

© Springer Nature Limited 2018

Authors and Affiliations

  1. 1.London School of Hygiene and Tropical MedicineLondonUK

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