1932

Abstract

Antimicrobial use (AMU) in animal agriculture contributes to antimicrobial resistance (AMR) in humans, which imposes significant health and economic costs on society. Economists call these costs negative externalities, societal costs that are not properly reflected in market prices. We review the relevant literature and develop a model to quantify the external costs of AMU in animal agriculture on AMR in humans. Parameters required for this estimate include () the health and economic burden of AMR in humans,() the impact of AMU in animal agriculture on AMR in animals, () the fraction of AMR in humans attributable to animal agriculture, and () AMU in animals. We use a well-documented historic case to estimate an externality cost of about US$1,500 per kilogram of fluoroquinolones administered in US broiler chicken production. Enhanced data collection, particularly on the third and fourth parameters, is urgently needed to quantify more fully the externalities of AMU in animal agriculture.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-publhealth-040218-043954
2020-04-01
2024-12-07
Loading full text...

Full text loading...

/deliver/fulltext/publhealth/41/1/annurev-publhealth-040218-043954.html?itemId=/content/journals/10.1146/annurev-publhealth-040218-043954&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Aust. Pestic. Vet. Med. Auth. 2014.. Quantity of antimicrobial products sold for veterinary use in Australia. Rep., Aust. Gov., Kingston:. https://apvma.gov.au/sites/default/files/images/antimicrobial_sales_report_march-2014.pdf
    [Google Scholar]
  2. 2. 
    Brown G, Layton DF. 1996.. Resistance economics: social cost and the evolution of antibiotic resistance. . Environ. Dev. Econ. 1:(3):34955
    [Google Scholar]
  3. 3. 
    Burnham JP, Olsen MA, Kollef MH. 2019.. Re-estimating annual deaths due to multidrug-resistant organism infections. . Infect. Control Hosp. Epidemiol. 40:(1):11213
    [Google Scholar]
  4. 4. 
    Cassini A, Högberg LD, Plachouras D, Quattrocchi A, Hoxha A, et al. 2019.. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. . Lancet Infect. Dis. 19:(1):5666
    [Google Scholar]
  5. 5. 
    CDC (Cent. Dis. Control Prev.), US DHHS (Dep. Health Hum. Serv.). 2013.. Antibiotic resistance threats in the United States, 2013. Rep., CDC, US DHHS, Atlanta:. https://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf
    [Google Scholar]
  6. 5a. 
    CDC (Cent. Dis. Control Prev.), US DHHS (Dep. Health Hum. Serv.). 2019.. Antibiotic resistance threats in the United States, 2019. Rep., CDC, US DHHS, Atlanta:. https://www.cdc.gov/drugresistance/pdf/threats-report/2019-ar-threats-report-508.pdf
    [Google Scholar]
  7. 6. 
    CDC (Cent. Dis. Control Prev.), US FDA (Food Drug Adm.). 1999.. National Antimicrobial Resistance Monitoring System (NARMS) for enteric bacteria: 1999 annual report. Rep., CDC, Atlanta:. https://www.cdc.gov/narms/annual/1999/NARMS_final_report_1999_full.pdf
    [Google Scholar]
  8. 7. 
    CIPARS (Can. Integr. Progr. Antimicrob. Resist. Surveill.). 2016.. Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS). 2016 annual report. Rep., CIPARS, Guelph, Ontario:. http://publications.gc.ca/collections/collection_2018/aspc-phac/HP2-4-2016-eng.pdf
    [Google Scholar]
  9. 8. 
    Cohen B, Larson EL, Stone PW, Neidell M, Glied SA. 2010.. Factors associated with variation in estimates of the cost of resistant infections. . Med. Care 48:(9):76775
    [Google Scholar]
  10. 9. 
    Crawford LM. 2005.. Enrofloxacin for poultry; final decision on withdrawal of new animal drug application following formal evidentiary public hearing; availability. . Fed. Regist. 70::44105
    [Google Scholar]
  11. 10. 
    Cuong NV, Padungtod P, Thwaites G, Carrique-Mas JJ. 2018.. Antimicrobial usage in animal production: a review of the literature with a focus on low- and middle-income countries. . Antibiotics 7:(3):75
    [Google Scholar]
  12. 11. 
    CVM (Cent. Vet. Med.), US FDA (Food Drug Adm.). 2000.. Human health impact of fluoroquinolone resistant campylobacter attributed to the consumption of chicken. Rep., CVM, US FDA, Rockville, MD:
    [Google Scholar]
  13. 12. 
    CVM (Cent. Vet. Med.), US FDA (Food Drug Adm.). 2003.. Guidance for industry. Evaluating the safety of antimicrobial new animal drugs with regard to their microbiological effects on bacteria of human health concern. Guid. Doc. 152, CVM, US FDA, Rockville, MD:. https://www.fda.gov/regulatory-information/search-fda-guidance-documents/cvm-gfi-152-evaluating-safety-antimicrobial-new-animal-drugs-regard-their-microbiological-effects
    [Google Scholar]
  14. 13. 
    CVM (Cent. Vet. Med.), US FDA (Food Drug Adm.). 2018.. 2017 Summary report on antimicrobials sold or distributed for use in food-producing animals. Rep., US FDA, Rockville, MD:. https://www.fda.gov/media/119332/download
    [Google Scholar]
  15. 14. 
    Dutil L, Irwin R, Finley R, Ng LK, Avery B, et al. 2010.. Ceftiofur resistance in Salmonellaenterica serovar Heidelberg from chicken meat and humans, Canada. . Emerg. Infect. Dis. 16:(1):4854
    [Google Scholar]
  16. 15. 
    Economou V, Gousia P. 2015.. Agriculture and food animals as a source of antimicrobial-resistant bacteria. . Infect. Drug Resist. 8::4961
    [Google Scholar]
  17. 16. 
    Ellis LJ, Turner JL. 2007.. Surf and turf: environmental and food safety concerns of China's aquaculture and animal husbandry. . China Environ. Ser. 9::1940
    [Google Scholar]
  18. 17. 
    EMA (Eur. Med. Agency). 2019.. Sales of veterinary antimicrobial agents in 30 European countries. Trends from 2010 to 2016. 8th ESVAC Rep., EMA, London:. https://www.ema.europa.eu/en/documents/report/sales-veterinary-antimicrobial-agents-30-european-countries-2016-trends-2010-2016-eighth-esvac_en.pdf
    [Google Scholar]
  19. 18. 
    FAO (Food Agric. Organ. U.N.). 2016.. Supporting the food and agriculture sectors in implementing the Global Action Plan on Antimicrobial Resistance to minimize the impact of antimicrobial resistance. Rep., FAO, Rome:. http://www.fao.org/3/a-i5996e.pdf
    [Google Scholar]
  20. 19. 
    Frieri M, Kumar K, Boutin A. 2017.. Antibiotic resistance. . J. Infect. Public Health 10::36978
    [Google Scholar]
  21. 20. 
    Gandra S, Barter DM, Laxminarayan R. 2014.. Economic burden of antibiotic resistance: How much do we really know?. Clin. Microbiol. Infect. 20:(10):97380
    [Google Scholar]
  22. 21. 
    Hao H, Cheng G, Iqbal Z, Ai X, Hussain HI, et al. 2014.. Benefits and risks of antimicrobial use in food-producing animals. . Front. Microbiol. 5::288
    [Google Scholar]
  23. 22. 
    Hatcher SM, Rhodes SM, Stewart JR, Silbergeld E, Pisanic N, et al. 2017.. The prevalence of antibiotic-resistant Staphylococcusaureus nasal carriage among industrial hog operation workers, community residents, and children living in their households: North Carolina, USA. . Environ. Health Perspect. 125:(4):56069
    [Google Scholar]
  24. 23. 
    Hiki M, Kawanishi M, Abo H, Kojima A, Koike R, et al. 2015.. Decreased resistance to broad-spectrum cephalosporin in Escherichia coli from healthy broilers at farms in Japan after voluntary withdrawal of ceftiofur. . Foodborne Pathog. Dis. 12:(7):63943
    [Google Scholar]
  25. 24. 
    Hoffmann S, Devleesschauwer B, Aspinall W, Cooke R, Corrigan T, et al. 2017.. Attribution of global foodborne disease to specific foods: findings from a World Health Organization structured expert elicitation. . PLOS ONE 12:(9):e0183641
    [Google Scholar]
  26. 25. 
    IFSAC (Interagency Food Saf. Anal. Collab.). 2017.. Foodborne illness source attribution estimates for 2013 for Salmonella, Escherichia coli O157, Listeria monocytogenes, and Campylobacter using multi-year outbreak surveillance data, United States. Rep., IFSAC, US Dep. Health Hum. Serv., Cent. Dis. Control Prev., US Food Drug Adm., Atlanta, GA/Rockville, MD:. https://www.cdc.gov/foodsafety/pdfs/IFSAC-2013FoodborneillnessSourceEstimates-508.pdf
    [Google Scholar]
  27. 26. 
    Kar A, Wallinga D. 2018.. Livestock antibiotic sales see big drop, but remain high. NRDC Blog, Dec. 18. https://www.nrdc.org/experts/avinash-kar/livestock-antibiotic-sales-drop-remain-very-high
    [Google Scholar]
  28. 27. 
    Korinek A. 2019.. The externalities of antimicrobial resistance, a technical note. . Resources on the Externalities of Antimicrobial Resistance. http://www.korinek.com/AMR
    [Google Scholar]
  29. 28. 
    KPMG. 2014.. The global economic impact of anti-microbial resistance. Rep., KPMG, Amstelveen, Neth. https://home.kpmg/content/dam/kpmg/pdf/2014/12/amr-report-final.pdf
    [Google Scholar]
  30. 29. 
    Laxminarayan R, Brown GM. 2001.. Economics of antibiotic resistance: a theory of optimal use. . J. Environ. Econ. Manag. 42:(2):183206
    [Google Scholar]
  31. 30. 
    Liu Y-Y, Wang Y, Walsh TR, Yi L-X, Zhang R, et al. 2016.. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. . Lancet Infect. Dis. 16:(2):16168
    [Google Scholar]
  32. 31. 
    Matsunaga N, Hayakawa K. 2018.. Estimating the impact of antimicrobial resistance. . Lancet Glob. Heal. 6:(9):e93435
    [Google Scholar]
  33. 32. 
    Minist. Agric. For. Fisheries (MAFF). 2015.. Sales amounts and sales volumes (active substance) of antibiotics, synthetic antibacterials, antihelmintics and antiprotozoals. Rep., Natl. Vet. Assay Lab., Kokubunji, Japan:. http://www.maff.go.jp/nval/iyakutou/hanbaidaka/attach/pdf/h27-koukinzai_re.pdf
    [Google Scholar]
  34. 33. 
    Naylor NR, Atun R, Zhu N, Kulasabanathan K, Silva S, et al. 2018.. Estimating the burden of antimicrobial resistance: a systematic literature review. . Antimicrob. Resist. Infect. Control 7:(1):58
    [Google Scholar]
  35. 34. 
    O'Neill J. 2014.. Antimicrobial resistance: tackling a crisis for the health and wealth of nations. Rev. Pap., Rev. Antimicrob. Resist., London:. https://amr-review.org/sites/default/files/AMR%20Review%20Paper%20-%20Tackling%20a%20crisis%20for%20the%20health%20and%20wealth%20of%20nations_1.pdf
    [Google Scholar]
  36. 35. 
    O'Neill J. 2016.. Tackling drug-resistant infections globally: final report and recommendations. Rev. Pap., Rev. Antimicrob. Resist., London:. https://amr-review.org/sites/default/files/160518_Final%20paper_with%20cover.pdf
    [Google Scholar]
  37. 36. 
    OECD. 2018.. Stemming the Superbug Tide: Just a Few Dollars More. Paris:: OECD
    [Google Scholar]
  38. 37. 
    OIE (World Organ. Animal Health). 2017.. Global action to alleviate the threat of antimicrobial resistance: progress and opportunities for future activities under the “One Health” initiative considering. Rep., OIE, Paris:. http://www.oie.int/fileadmin/Home/eng/Our_scientific_expertise/docs/pdf/AMR/A_AMR_RESO_2017.pdf
    [Google Scholar]
  39. 38. 
    OIE (World Organ. Animal Health). 2017.. OIE annual report on antimicrobial agents intended for use in animals: better understanding of the global situation. Rep., OIE, Paris:. https://www.oie.int/fileadmin/Home/eng/Our_scientific_expertise/docs/pdf/AMR/Annual_Report_AMR_2.pdf
    [Google Scholar]
  40. 39. 
    Pesti GM, Amato SV, Minear LR. 1985.. Water consumption of broiler chickens under commercial conditions. . Poult. Sci. 64:(5):8038
    [Google Scholar]
  41. 40. 
    Pires SM, Christensen J. 2017.. Source attribution of Campylobacter infections in Denmark. Tech. Rep., Natl. Food Inst. Tech., Univ. Denmark, Lyngby:. https://orbit.dtu.dk/files/145802383/Report_Source_Attribution_Campylobacter_FINAL.pdf
    [Google Scholar]
  42. 41. 
    Plumb DC. 1999.. Veterinary Drug Handbook. White Bear Lake, MN:: Pharma Vet. , 3rd ed..
    [Google Scholar]
  43. 42. 
    QIA. 2019.. Establishment of monitoring system for livestock antibiotics for livestock in 2012: antibiotic use and antibiotic resistance monitoring. Rep., QIA, Gimcheon, Korea:. http://lib.qia.go.kr/LibtechUpload/Book/B20140306-2.pdf
    [Google Scholar]
  44. 43. 
    Roberts RR, Hota B, Ahmad I, Scott RD II, Foster SD, et al. 2009.. Hospital and societal costs of antimicrobial‐resistant infections in a Chicago teaching hospital: implications for antibiotic stewardship. . Clin. Infect. Dis. 49:(8):117584
    [Google Scholar]
  45. 44. 
    Scott AM, Beller E, Glasziou P, Clark J, Ranakusuma RW, et al. 2018.. Is antimicrobial administration to food animals a direct threat to human health? A rapid systematic review. . Int. J. Antimicrob. Agents 52:(3):31623
    [Google Scholar]
  46. 45. 
    Stewardson A, Fankhauser C, De Angelis G, Rohner P, Safran E, et al. 2013.. Burden of bloodstream infection caused by extended-spectrum β-lactamase–producing enterobacteriaceae determined using multistate modeling at a Swiss university hospital and a nationwide predictive model. . Infect. Control Hosp. Epidemiol. 34:(2):13343
    [Google Scholar]
  47. 46. 
    Stewardson AJ, Allignol A, Beyersmann J, Graves N, Schumacher M, et al. 2016.. The health and economic burden of bloodstream infections caused by antimicrobial-susceptible and non-susceptible Enterobacteriaceae and Staphylococcusaureus in European hospitals, 2010 and 2011: a multicentre retrospective cohort study. . Euro Surveill. 21:(33). https://doi.org/10.2807/1560-7917.es.2016.21.33.30319
    [Crossref] [Google Scholar]
  48. 47. 
    Tang KL, Caffrey NP, Nóbrega DB, Cork SC, Ronksley PE, et al. 2017.. Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: a systematic review and meta-analysis. . Lancet Planet. Health 1:(8):e31627
    [Google Scholar]
  49. 48. 
    Taylor J, Hafner M, Yerushalmi E, Smith R, Bellasio J, et al. 2014.. Estimating economic costs of antimicrobial resistance: model and results. Rep., RAND Eur., Cambridge, UK:. https://www.rand.org/pubs/research_reports/RR911.html
    [Google Scholar]
  50. 49. 
    Temkin E, Fallach N, Almagor J, Gladstone BP, Tacconelli E, et al. 2018.. Estimating the number of infections caused by antibiotic-resistant Escherichia coli and Klebsiellapneumoniae in 2014: a modelling study. . Lancet Glob. Health 6:(9):e96979
    [Google Scholar]
  51. 50. 
    Thorpe KE, Joski P, Johnston KJ. 2018.. Antibiotic-resistant infection treatment costs have doubled since 2002, now exceeding $2 billion annually. . Health Aff. 37:(4):66269
    [Google Scholar]
  52. 51. 
    US FDA (Food Drug Adm.). 2015.. Veterinary feed directive. . Fed. Regist. 80:(106):3170835
    [Google Scholar]
  53. 52. 
    US FDA (Food Drug Adm.), DHHS (Dep. Health Hum. Serv.). 2000.. Enrofloxacin for poultry; opportunity for hearing. . Fed. Regist. 65: FR 64954
    [Google Scholar]
  54. 53. 
    US GAO (Gov. Account. Off.). 2011.. Antibiotic resistance: agencies have made limited progress addressing antibiotic use in animals. GAO-11-801, Comm. Rules, House Represent., Washington, DC:. https://www.gao.gov/assets/330/323090.pdf
    [Google Scholar]
  55. 54. 
    Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, et al. 2015.. Global trends in antimicrobial use in food animals. . PNAS 112:(18):564954
    [Google Scholar]
  56. 55. 
    Wallinga D. 2018.. Better bacon why it's high time the US pork industry stopped pigging out on antibiotics. Issue Brief, June 6, NRDC, New York:. https://www.nrdc.org/resources/better-bacon-why-its-high-time-us-pork-industry-stopped-pigging-out-antibiotics
    [Google Scholar]
  57. 56. 
    Wallinga D, Roach S. 2018.. Antibiotic consumption in U.S. pork, beef, and turkey industries vastly outstrips comparable industries in Europe, and the U.S. chicken industry. Issue Brief, Nov. 13, NRDC, New York:. https://www.nrdc.org/resources/antibiotic-consumption-us-pork-beef-and-turkey-industries-vastly-outstrips-comparable
    [Google Scholar]
  58. 57. 
    Walsh TR, Wu Y. 2016.. China bans colistin as a feed additive for animals. . Lancet Infect. Dis. 16:(10):11023
    [Google Scholar]
  59. 58. 
    Wardyn SE, Stegger M, Price LB, Smith TC. 2018.. Whole-genome analysis of recurrent Staphylococcusaureus t571/st398 infection in farmer, Iowa, USA. . Emerg. Infect. Dis. 24:(1):15354
    [Google Scholar]
  60. 59. 
    Webb HE, Angulo FJ, Granier SA, Scott HM, Loneragan GH. 2017.. Illustrative examples of probable transfer of resistance determinants from food animals to humans: streptothricins, glycopeptides, and colistin. . F1000Res. 6::1805
    [Google Scholar]
  61. 60. 
    WHO (World Health Organ.). 2014.. Antimicrobial resistance: global report on surveillance. Rep., WHO, Geneva. http://apps.who.int/iris/bitstream/handle/10665/112642/9789241564748_eng.pdf;jsessionid=C08C60691635B5D4635DB3D050DB403C?sequence=1
    [Google Scholar]
  62. 61. 
    WHO (World Health Organ.). 2019.. Global Antimicrobial Resistance Surveillance System (GLASS) report: early implementation 2017–2018. Rep., WHO, Geneva:. https://www.who.int/glass/resources/publications/early-implementation-report/en/
    [Google Scholar]
  63. 62. 
    WHO (World Health Organ.). 2019.. WHO guidelines on use of medically important antimicrobials in food-producing animals. Rep., WHO, Geneva:. https://apps.who.int/iris/bitstream/handle/10665/258970/9789241550130-eng.pdf?sequence=1
    [Google Scholar]
  64. 63. 
    Woolhouse MEJ, Ward MJ. 2013.. Sources of antimicrobial resistance. . Science 341:(6153):146061
    [Google Scholar]
  65. 64. 
    World Bank. 2017.. Drug-resistant infections: a threat to our economic future. Fin. Rep., World Bank, Washington, DC:. http://documents.worldbank.org/curated/en/323311493396993758/pdf/final-report.pdf
    [Google Scholar]
  66. 65. 
    Wozniak TM, Barnsbee L, Lee XJ, Pacella RE. 2019.. Using the best available data to estimate the cost of antimicrobial resistance: a systematic review. . Antimicrob. Resist. Infect. Control 8:(1):26
    [Google Scholar]
  67. 66. 
    Zhang Q-Q, Ying G-G, Pan C-G, Liu Y-S, Zhao J-L. 2015.. Comprehensive evaluation of antibiotics emission and fate in the river basins of China: source analysis, multimedia modeling, and linkage to bacterial resistance. . Environ. Sci. Technol. 49:(11):677282
    [Google Scholar]
/content/journals/10.1146/annurev-publhealth-040218-043954
Loading
/content/journals/10.1146/annurev-publhealth-040218-043954
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error