1932

Abstract

Antimicrobial resistance (AMR) is a threat to animal and human health. Antimicrobial use has been identified as a major driver of AMR, and reductions in use are a focal point of interventions to reduce resistance. Accordingly, stakeholders in human health and livestock production have implemented antimicrobial stewardship programs aimed at reducing use. Thus far, these efforts have yielded variable impacts on AMR. Furthermore, scientific advances are prompting an expansion and more nuanced appreciation of the many nonantibiotic factors that drive AMR, as well as how these factors vary across systems, geographies, and contexts. Given these trends, we propose a framework to prioritize AMR interventions. We use this framework to evaluate the impact of interventions that focus on antimicrobial use. We conclude by suggesting that priorities be expanded to include greater consideration of host–microbial interactions that dictate AMR, as well as anthropogenic and environmental systems that promote dissemination of AMR.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-072020-080638
2021-02-15
2024-06-19
Loading full text...

Full text loading...

/deliver/fulltext/animal/9/1/annurev-animal-072020-080638.html?itemId=/content/journals/10.1146/annurev-animal-072020-080638&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    World Health Organ. 2019. Turning plans into action for antimicrobial resistance (AMR) Work. Pap. 2.0, Implement. Coord. World Health Organ. Geneva:
    [Google Scholar]
  2. 2. 
    World Organ. Anim. Health. 2020. Prudent and responsible use of antimicrobials https://www.oie.int/en/for-the-media/amr/prudent-and-responsible-use/
    [Google Scholar]
  3. 3. 
    White House. 2015. National Action Plan for Combating Antibiotic-Resistant Bacteria Washington, DC: Cent. Dis. Control
    [Google Scholar]
  4. 4. 
    World Health Organ. 2008. Joint FAO/WHO/OIE Expert Meeting on Critically Important Antimicrobials: Report of the FAO/WHO/OIE Expert Meeting, FAO Headquarters, Rome, 2630 November 2007 Rep., Anim. Prod. Health Div., Food Agric. Organ. World Health Organ. Rome:
    [Google Scholar]
  5. 5. 
    World Health Organ. 2017. WHO Guidelines on Use of Medically Important Antimicrobials in Food-Producing Animals Geneva: World Health Organ.
    [Google Scholar]
  6. 6. 
    D'Atri F, Arthur J, Blix HS, Hicks LA, Plachouras D et al. 2019. Targets for the reduction of antibiotic use in humans in the Transatlantic Taskforce on Antimicrobial Resistance (TATFAR) partner countries. Eurosurveillance 24:281800339
    [Google Scholar]
  7. 7. 
    Pan Am. Health Organ., Fla. Int. Univ. 2018. Recommendations for Implementing Antimicrobial Stewardship Programs in Latin America and the Caribbean: Manual for Public Health Decision-Makers Washington, DC: Pan Am. Health Organ., Fla. Int. Univ.
    [Google Scholar]
  8. 8. 
    World Health Organ. 2019. Antimicrobial Stewardship Programmes in Health-Care Facilities in Low- and Middle-Income Countries: A WHO Practical Toolkit Geneva: World Health Organ.
    [Google Scholar]
  9. 9. 
    Cent. Dis. Control Prev. 2019. The core elements of hospital antibiotic stewardship programs: 2019 Doc., Cent. Dis. Control Prev. Atlanta: https://www.cdc.gov/antibiotic-use/healthcare/pdfs/hospital-core-elements-H.pdf
    [Google Scholar]
  10. 10. 
    World Vet. Assoc. 2020. Global repository of available guidelines for responsible use of antimicrobials in animal health Doc., World Vet. Assoc. Brussels: http://worldvet.org/uploads/news/docs/list_of_available_guidelines_on_amu_-aug2019.pdf
    [Google Scholar]
  11. 11. 
    Am. Vet. Med. Assoc. 2020. Antimicrobial stewardship definition and core principles Resour., Am. Vet. Med. Assoc. Schaumburg, IL: https://www.avma.org/sites/default/files/resources/AntimicrobStewardshipDef_CorePrinciplesFlyer_052318.pdf
    [Google Scholar]
  12. 12. 
    Univ. Minn. 2020. Handbook of Antibiotic Stewardship in Companion Animal Veterinary Settings St. Paul: Univ. Minn 1st ed.
    [Google Scholar]
  13. 13. 
    Murphy CP, Carson C, Smith BA, Chapman B, Marrotte J et al. 2018. Factors potentially linked with the occurrence of antimicrobial resistance in selected bacteria from cattle, chickens and pigs: a scoping review of publications for use in modelling of antimicrobial resistance (IAM.AMR Project). Zoonoses Public Health 65:8957–71
    [Google Scholar]
  14. 14. 
    Vikesland P, Garner E, Gupta S, Kang S, Maile-Moskowitz A, Zhu N 2019. Differential drivers of antimicrobial resistance across the world. Acc. Chem. Res. 52:4916–24
    [Google Scholar]
  15. 15. 
    Rodríguez-Verdugo A, Gaut BS, Tenaillon O 2013. Evolution of Escherichia coli rifampicin resistance in an antibiotic-free environment during thermal stress. BMC Evol. Biol. 13:50
    [Google Scholar]
  16. 16. 
    Knöppel A, Näsvall J, Andersson DI 2017. Evolution of antibiotic resistance without antibiotic exposure. Antimicrob. Agents Chemother. 61:11e01495–17
    [Google Scholar]
  17. 17. 
    Collignon P, Beggs JJ, Walsh TR, Gandra S, Laxminarayan R 2018. Anthropological and socioeconomic factors contributing to global antimicrobial resistance: a univariate and multivariable analysis. Lancet Planet. Health 2:9e398–405
    [Google Scholar]
  18. 18. 
    Kakkar M, Chatterjee P, Chauhan AS, Grace D, Lindahl J et al. 2018. Antimicrobial resistance in South East Asia: time to ask the right questions. Glob. Health Action 11:11483637
    [Google Scholar]
  19. 19. 
    World Health Organ., Food Agric. Organ., World Organ. Anim. Health. 2020. Technical brief on water, sanitation, hygiene (WASH) and wastewater management to prevent infections and reduce the spread of antimicrobial resistance (AMR) Tech. Brief, World Health Organ. Geneva:
    [Google Scholar]
  20. 20. 
    Holmes AH, Moore LSP, Sundsfjord A, Steinbakk M, Regmi S et al. 2016. Understanding the mechanisms and drivers of antimicrobial resistance. Lancet 387:10014176–87
    [Google Scholar]
  21. 21. 
    Schechner V, Temkin E, Harbarth S, Carmeli Y, Schwaber MJ 2013. Epidemiological interpretation of studies examining the effect of antibiotic usage on resistance. Clin. Microbiol. Rev. 26:2289–307
    [Google Scholar]
  22. 22. 
    Singer RS, Ward MP, Maldonado G 2006. Can landscape ecology untangle the complexity of antibiotic resistance. Nat. Rev. Microbiol. 4:12943–52
    [Google Scholar]
  23. 23. 
    Singer RS, Reid-Smith R, Sischo WM 2006. Stakeholder position paper: epidemiological perspectives on antibiotic use in animals. Prev. Vet. Med. 73:2–3153–61
    [Google Scholar]
  24. 24. 
    Essack SY, Sartorius B. 2018. Global antibiotic resistance: of contagion, confounders, and the COM-B model. Lancet Planet. Health 2:9e376–77
    [Google Scholar]
  25. 25. 
    Blommaert A, Marais C, Hens N, Coenen S, Muller A et al. 2014. Determinants of between-country differences in ambulatory antibiotic use and antibiotic resistance in Europe: a longitudinal observational study. J. Antimicrob. Chemother. 69:2535–47
    [Google Scholar]
  26. 26. 
    Hernandez-Santiago V, Davey PG, Nathwani D, Marwick CA, Guthrie B 2019. Changes in resistance among coliform bacteraemia associated with a primary care antimicrobial stewardship intervention: a population-based interrupted time series study. PLOS Med 16:6e1002825
    [Google Scholar]
  27. 27. 
    Hammond A, Stuijfzand B, Avison MB, Hay AD 2020. Antimicrobial resistance associations with national primary care antibiotic stewardship policy: primary care-based, multilevel analytic study. PLOS ONE 15:5e0232903
    [Google Scholar]
  28. 28. 
    Pouwels KB, Freeman R, Muller-Pebody B, Rooney G, Henderson KL et al. 2018. Association between use of different antibiotics and trimethoprim resistance: going beyond the obvious crude association. J. Antimicrob. Chemother. 73:61700–7
    [Google Scholar]
  29. 29. 
    Sundqvist M, Geli P, Andersson DI, Sjölund-Karlsson M, Runehagen A et al. 2010. Little evidence for reversibility of trimethoprim resistance after a drastic reduction in trimethoprim use. J. Antimicrob. Chemother. 65:2350–60
    [Google Scholar]
  30. 30. 
    Hurd HS, Doores S, Hayes D, Mathew A, Maurer J et al. 2004. Public health consequences of macrolide use in food animals: a deterministic risk assessment. J. Food Prot. 67:5980–92
    [Google Scholar]
  31. 31. 
    Mughini-Gras L, Dorado-García A, van Duijkeren E, van den Bunt G, Dierikx CM et al. 2019. Attributable sources of community-acquired carriage of Escherichia coli containing β-lactam antibiotic resistance genes: a population-based modelling study. Lancet Planet. Health 3:8e357–69
    [Google Scholar]
  32. 32. 
    O'Connor AM, Auvermann BW, Dzikamunhenga RS, Glanville JM, Higgins JPT et al. 2017. Updated systematic review: associations between proximity to animal feeding operations and health of individuals in nearby communities. Syst. Rev. 6:186
    [Google Scholar]
  33. 33. 
    Bueno I, Williams-Nguyen J, Hwang H, Sargeant JM, Nault AJ, Singer RS 2018. Systematic review: impact of point sources on antibiotic-resistant bacteria in the natural environment. Zoonoses Public Health 65:1e162–84
    [Google Scholar]
  34. 34. 
    Bonten MJM, Mevius D. 2015. Less evidence for an important role of food-producing animals as source of antibiotic resistance in humans. Clin. Infect. Dis. 60:121867
    [Google Scholar]
  35. 35. 
    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 1:8e316–27
    [Google Scholar]
  36. 36. 
    Bennani H, Mateus A, Mays N, Eastmure E, Stärk KDC, Häsler B 2020. Overview of evidence of antimicrobial use and antimicrobial resistance in the food chain. Antibiotics 9:249
    [Google Scholar]
  37. 37. 
    Singer RS, Williams-Nguyen J. 2014. Human health impacts of antibiotic use in agriculture: a push for improved causal inference. Curr. Opin. Microbiol. 19:1–8
    [Google Scholar]
  38. 38. 
    van Bunnik BAD, Woolhouse MEJ 2017. Modelling the impact of curtailing antibiotic usage in food animals on antibiotic resistance in humans. R. Soc. Open Sci. 4:4161067
    [Google Scholar]
  39. 39. 
    Singer RS, Ruegg PL, Bauman DE 2017. Quantitative risk assessment of antimicrobial-resistant foodborne infections in humans due to recombinant bovine somatotropin usage in dairy cows. J. Food Prot. 80:71099–116
    [Google Scholar]
  40. 40. 
    Hurd HS, Vaughn MB, Holtkamp D, Dickson J, Warnick L 2010. Quantitative risk from fluoroquinolone-resistant Salmonella and Campylobacter due to treatment of dairy heifers with enrofloxacin for bovine respiratory disease. Foodborne Pathog. Dis. 7:111305–22
    [Google Scholar]
  41. 41. 
    Knight GM, Davies NG, Colijn C, Coll F, Donker T et al. 2019. Mathematical modelling for antibiotic resistance control policy: Do we know enough. BMC Infect. Dis. 19:1011
    [Google Scholar]
  42. 42. 
    Landers TF, Cohen B, Wittum TE, Larson EL 2012. A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Rep 127:14–22
    [Google Scholar]
  43. 43. 
    Katwyk SRV, Grimshaw JM, Nkangu M, Nagi R, Mendelson M et al. 2019. Government policy interventions to reduce human antimicrobial use: a systematic review and evidence map. PLOS Med 16:6e1002819
    [Google Scholar]
  44. 44. 
    Agersø Y, Aarestrup FM. 2013. Voluntary ban on cephalosporin use in Danish pig production has effectively reduced extended-spectrum cephalosporinase-producing Escherichia coli in slaughter pigs. J. Antimicrob. Chemother. 68:3569–72
    [Google Scholar]
  45. 45. 
    van den Bogaard AE, Bruinsma N, Stobberingh EE 2000. The effect of banning avoparcin on VRE carriage in The Netherlands. J. Antimicrob. Chemother. 46:1146–48
    [Google Scholar]
  46. 46. 
    Benedict KM, Gow SP, McAllister TA, Booker CW, Hannon SJ et al. 2015. Antimicrobial resistance in Escherichia coli recovered from feedlot cattle and associations with antimicrobial use. PLOS ONE 10:12e0143995
    [Google Scholar]
  47. 47. 
    Morley PS, Dargatz DA, Hyatt DR, Dewell GA, Patterson JG et al. 2011. Effects of restricted antimicrobial exposure on antimicrobial resistance in fecal Escherichia coli from feedlot cattle. Foodborne Pathog. Dis. 8:187–98
    [Google Scholar]
  48. 48. 
    Aarestrup FM, Seyfarth AM, Emborg H-D, Pedersen K, Hendriksen RS, Bager F 2001. Effect of abolishment of the use of antimicrobial agents for growth promotion on occurrence of antimicrobial resistance in fecal enterococci from food animals in Denmark. Antimicrob. Agents Chemother. 45:72054–59
    [Google Scholar]
  49. 49. 
    Noyes NR, Benedict KM, Gow SP, Waldner CL, Reid-Smith RJ et al. 2016. Modelling considerations in the analysis of associations between antimicrobial use and resistance in beef feedlot cattle. Epidemiol. Infect. 144:61313–29
    [Google Scholar]
  50. 50. 
    Pouwels KB, Batra R, Patel A, Edgeworth JD, Robotham JV, Smieszek T 2017. Will co-trimoxazole resistance rates ever go down? Resistance rates remain high despite decades of reduced co-trimoxazole consumption. J. Glob. Antimicrob. Resist. 11:71–74
    [Google Scholar]
  51. 51. 
    Zawack K, Li M, Booth JG, Love W, Lanzas C, Gröhn YT 2016. Monitoring antimicrobial resistance in the food supply chain and its implications for FDA policy initiatives. Antimicrob. Agents Chemother. 60:95302–11
    [Google Scholar]
  52. 52. 
    MacLean RC, Vogwill T. 2014. Limits to compensatory adaptation and the persistence of antibiotic resistance in pathogenic bacteria. Evol. Med. Public Health 2015:14–12
    [Google Scholar]
  53. 53. 
    Lamrabet O, Martin M, Lenski RE, Schneider D 2019. Changes in intrinsic antibiotic susceptibility during a long-term evolution experiment with Escherichia coli. mBio 10:2e00189–19
    [Google Scholar]
  54. 54. 
    Willmann M, El-Hadidi M, Huson DH, Schütz M, Weidenmaier C et al. 2015. Antibiotic selection pressure determination through sequence-based metagenomics. Antimicrob. Agents Chemother. 59:127335–45
    [Google Scholar]
  55. 55. 
    Zaura E, Brandt BW, Teixeira de Mattos MJ, Buijs MJ, Caspers MPM et al. 2015. Same exposure but two radically different responses to antibiotics: resilience of the salivary microbiome versus long-term microbial shifts in feces. mBio 6:6e01693–15
    [Google Scholar]
  56. 56. 
    Raymond F, Ouameur AA, Déraspe M, Iqbal N, Gingras H et al. 2016. The initial state of the human gut microbiome determines its reshaping by antibiotics. ISME J 10:3707–20
    [Google Scholar]
  57. 57. 
    Willmann M, Vehreschild MJGT, Biehl LM, Vogel W, Dörfel D et al. 2019. Distinct impact of antibiotics on the gut microbiome and resistome: a longitudinal multicenter cohort study. BMC Biol 17:76
    [Google Scholar]
  58. 58. 
    Ng KM, Aranda-Díaz A, Tropini C, Frankel MR, Van Treuren W et al. 2019. Recovery of the gut microbiota after antibiotics depends on host diet, community context, and environmental reservoirs. Cell Host Microbe 26:5650–65.e4
    [Google Scholar]
  59. 59. 
    World Health Organ. 2003. Impacts of Antimicrobial Growth Promoter Termination in Denmark: The WHO International Review Panel's Evaluation of the Termination of the Use of Antimicrobial Growth Promoters in Denmark: Foulum, Denmark 6–9 November 2002 Geneva: World Health Organ.
    [Google Scholar]
  60. 60. 
    Natl. Acad. Sci. Eng. Med. 2018. Understanding the Economics of Microbial Threats: Proceedings of a Workshop Washington, DC: Natl. Acad. Press
    [Google Scholar]
  61. 61. 
    Laxminarayan R, Boeckel TV, Teillant A 2015. The economic costs of withdrawing antimicrobial growth promoters from the livestock sector Pap., Food Agric. Fish. Pap., Organ. Econ. Co-op. Dev., Paris
    [Google Scholar]
  62. 62. 
    Xiao Y, Li L. 2013. Legislation of clinical antibiotic use in China. Lancet Infect. Dis. 13:3189–91
    [Google Scholar]
  63. 63. 
    Chen J, Wang Y, Chen X, Hesketh T 2020. Widespread illegal sales of antibiotics in Chinese pharmacies—a nationwide cross-sectional study. Antimicrob. Resist. Infect. Control 9:12
    [Google Scholar]
  64. 64. 
    Collignon P, Athukorala P, Senanayake S, Khan F 2015. Antimicrobial resistance: the major contribution of poor governance and corruption to this growing problem. PLOS ONE 10:3e0116746
    [Google Scholar]
  65. 65. 
    Teixeira Rodrigues A, Roque F, Falcão A, Figueiras A, Herdeiro MT 2013. Understanding physician antibiotic prescribing behaviour: a systematic review of qualitative studies. Int. J. Antimicrob. Agents 41:3203–12
    [Google Scholar]
  66. 66. 
    Lago A, Godden SM. 2018. Use of rapid culture systems to guide clinical mastitis treatment decisions. Vet. Clin. N. Am. Food Anim. Pract. 34:3389–412
    [Google Scholar]
  67. 67. 
    Rowe SM, Godden SM, Nydam DV, Gorden PJ, Lago A et al. 2020. Randomized controlled non-inferiority trial investigating the effect of 2 selective dry-cow therapy protocols on antibiotic use at dry-off and dry period intramammary infection dynamics. J. Dairy Sci. 103:76473–92
    [Google Scholar]
  68. 68. 
    Rowe SM, Godden SM, Nydam DV, Gorden PJ, Lago A et al. 2020. Randomized controlled trial investigating the effect of 2 selective dry-cow therapy protocols on udder health and performance in the subsequent lactation. J. Dairy Sci. 103:76493–503
    [Google Scholar]
  69. 69. 
    Singer AC, Xu Q, Keller VDJ 2019. Translating antibiotic prescribing into antibiotic resistance in the environment: a hazard characterisation case study. PLOS ONE 14:9e0221568
    [Google Scholar]
  70. 70. 
    Baclet N, Ficheur G, Alfandari S, Ferret L, Senneville E et al. 2017. Explicit definitions of potentially inappropriate prescriptions of antibiotics in older patients: a compilation derived from a systematic review. Int. J. Antimicrob. Agents 50:5640–48
    [Google Scholar]
  71. 71. 
    Tarrant C, Krockow EM, Nakkawita WMID, Bolscher M, Colman AM et al. 2020. Moral and contextual dimensions of “inappropriate” antibiotic prescribing in secondary care: a three-country interview study. Front. Sociol. 5:7
    [Google Scholar]
  72. 72. 
    Kirchhelle C. 2018. Pharming animals: a global history of antibiotics in food production (1935–2017). Palgrave Commun 4:96
    [Google Scholar]
  73. 73. 
    McEwen SA, Angulo FJ, Collignon PJ, Conly J 2017. Potential unintended consequences associated with restrictions on antimicrobial use in food-producing animals. See Reference 5:61–64
    [Google Scholar]
  74. 74. 
    Smith JA. 2011. Experiences with drug-free broiler production. Poult. Sci. 90:112670–78
    [Google Scholar]
  75. 75. 
    Singer RS, Porter LJ, Thomson DU, Gage M, Beaudoin A, Wishnie JK 2019. Raising animals without antibiotics: U.S. producer and veterinarian experiences and opinions. Front. Vet. Sci. 6:452
    [Google Scholar]
  76. 76. 
    Gaucher M-L, Quessy S, Letellier A, Arsenault J, Boulianne M 2015. Impact of a drug-free program on broiler chicken growth performances, gut health, Clostridium perfringens and Campylobacter jejuni occurrences at the farm level. Poult. Sci. 94:81791–801
    [Google Scholar]
  77. 77. 
    Karavolias J, Salois MJ, Baker KT, Watkins K 2018. Raised without antibiotics: impact on animal welfare and implications for food policy. Transl. Anim. Sci. 2:4337–48
    [Google Scholar]
  78. 78. 
    Salois MJ, Cady RA, Heskett EA 2016. The environmental and economic impact of withdrawing antibiotics from US broiler production. J. Food Distrib. Res. 47:179–80
    [Google Scholar]
  79. 79. 
    Wierup M. 2001. The Swedish experience of the 1986 year ban of antimicrobial growth promoters, with special reference to animal health, disease prevention, productivity, and usage of antimicrobials. Microb. Drug Resist. 7:2183–90
    [Google Scholar]
  80. 80. 
    Casewell M, Friis C, Marco E, McMullin P, Phillips I 2003. The European ban on growth-promoting antibiotics and emerging consequences for human and animal health. J. Antimicrob. Chemother. 52:2159–61
    [Google Scholar]
  81. 81. 
    Cogliani C, Goossens H, Greko C 2011. Restricting antimicrobial use in food animals: lessons from Europe: Banning nonessential antibiotic uses in food animals is intended to reduce pools of resistance genes. Microbe Mag 6:6274–79
    [Google Scholar]
  82. 82. 
    Speksnijder DC, Mevius DJ, Bruschke CJM, Wagenaar JA 2015. Reduction of veterinary antimicrobial use in the Netherlands. The Dutch success model. Zoonoses Public Health 62:Suppl. 179–87
    [Google Scholar]
  83. 83. 
    Begemann S, Perkins E, Hoyweghen IV, Christley R, Watkins F 2018. How political cultures produce different antibiotic policies in agriculture: a historical comparative case study between the United Kingdom and Sweden. Sociol. Rural. 58:4765–85
    [Google Scholar]
  84. 84. 
    Krockow EM, Tarrant C. 2019. The international dimensions of antimicrobial resistance: Contextual factors shape distinct ethical challenges in South Africa, Sri Lanka and the United Kingdom. Bioethics 33:7756–65
    [Google Scholar]
  85. 85. 
    Davey P, Marwick CA, Scott CL, Charani E, McNeil K et al. 2017. Interventions to improve antibiotic prescribing practices for hospital inpatients. Cochrane Database Syst. Rev. 2:CD003543
    [Google Scholar]
  86. 86. 
    Schuts EC, Hulscher MEJL, Mouton JW, Verduin CM, Stuart JWTC et al. 2016. Current evidence on hospital antimicrobial stewardship objectives: a systematic review and meta-analysis. Lancet Infect. Dis. 16:7847–56
    [Google Scholar]
  87. 87. 
    Kim JW, Chung J, Choi S-H, Jang HJ, Hong S-B et al. 2012. Early use of imipenem/cilastatin and vancomycin followed by de-escalation versus conventional antimicrobials without de-escalation for patients with hospital-acquired pneumonia in a medical ICU: a randomized clinical trial. Crit. Care 16:1R28
    [Google Scholar]
  88. 88. 
    Leone M, Bechis C, Baumstarck K, Lefrant J-Y, Albanèse J et al. 2014. De-escalation versus continuation of empirical antimicrobial treatment in severe sepsis: a multicenter non-blinded randomized noninferiority trial. Intensive Care Med 40:101399–408
    [Google Scholar]
  89. 89. 
    Balinskaite V, Bou-Antoun S, Johnson AP, Holmes A, Aylin P 2019. An assessment of potential unintended consequences following a national antimicrobial stewardship program in England: an interrupted time series analysis. Clin. Infect. Dis. 69:2233–42
    [Google Scholar]
  90. 90. 
    Keenan JD, Bailey RL, West SK, Arzika AM, Hart J et al. 2018. Azithromycin to reduce childhood mortality in Sub-Saharan Africa. N. Engl. J. Med. 378:171583–92
    [Google Scholar]
  91. 91. 
    Keenan JD, Arzika AM, Maliki R, Boubacar N, Elh Adamou S et al. 2019. MORDOR II: persistence of benefit of azithromycin for childhood mortality. N. Engl. J. Med. 380:232207–14
    [Google Scholar]
  92. 92. 
    Arzika AM, Maliki R, Boubacar N, Kane S, Cotter SY et al. 2019. Biannual mass azithromycin distributions and malaria parasitemia in pre-school children in Niger: a cluster-randomized, placebo-controlled trial. PLOS Med 16:6e1002835
    [Google Scholar]
  93. 93. 
    Doan T, Arzika AM, Hinterwirth A, Maliki R, Zhong L et al. 2019. Macrolide resistance in MORDOR I: a cluster-randomized trial in Niger. N. Engl. J. Med. 380:232271–73
    [Google Scholar]
  94. 94. 
    O'Connor AM, Hu D, Totton SC, Scott N, Winder CB et al. 2019. A systematic review and network meta-analysis of injectable antibiotic options for the control of bovine respiratory disease in the first 45 days post arrival at the feedlot. Anim. Health Res. Rev. 20:2163–81
    [Google Scholar]
  95. 95. 
    Scott HM, Acuff G, Bergeron G, Bourassa MW, Gill J et al. 2019. Critically important antibiotics: criteria and approaches for measuring and reducing their use in food animal agriculture. Ann. N.Y. Acad. Sci. 1441:18–16
    [Google Scholar]
  96. 96. 
    O'Connor AM, Hu D, Totton SC, Scott N, Winder CB et al. 2019. A systematic review and network meta-analysis of bacterial and viral vaccines, administered at or near arrival at the feedlot, for control of bovine respiratory disease in beef cattle. Anim. Health Res. Rev. 20:2143–62
    [Google Scholar]
  97. 97. 
    Sargeant JM, Deb B, Bergevin MD, Churchill K, Dawkins K et al. 2019. Efficacy of bacterial vaccines to prevent respiratory disease in swine: a systematic review and network meta-analysis. Anim. Health Res. Rev. 20:2274–90
    [Google Scholar]
  98. 98. 
    Sargeant JM, Bergevin MD, Churchill K, Dawkins K, Deb B et al. 2019. The efficacy of litter management strategies to prevent morbidity and mortality in broiler chickens: a systematic review and network meta-analysis. Anim. Health Res. Rev. 20:2247–62
    [Google Scholar]
  99. 99. 
    Winder CB, Sargeant JM, Hu D, Wang C, Kelton DF et al. 2019. Comparative efficacy of teat sealants given prepartum for prevention of intramammary infections and clinical mastitis: a systematic review and network meta-analysis. Anim. Health Res. Rev. 20:2182–98
    [Google Scholar]
  100. 100. 
    Olesen SW, Barnett ML, MacFadden DR, Brownstein JS, Hernández-Díaz S et al. 2018. The distribution of antibiotic use and its association with antibiotic resistance. eLife 7:e39435
    [Google Scholar]
  101. 101. 
    Wang Y, Lu J, Engelstädter J, Zhang S, Ding P et al. 2020. Non-antibiotic pharmaceuticals enhance the transmission of exogenous antibiotic resistance genes through bacterial transformation. ISME J 14:2179–96
    [Google Scholar]
  102. 102. 
    Yelin I, Flett KB, Merakou C, Mehrotra P, Stam J et al. 2019. Genomic and epidemiological evidence of bacterial transmission from probiotic capsule to blood in ICU patients. Nat. Med. 25:111728–32
    [Google Scholar]
  103. 103. 
    Kahn LH, Bergeron G, Bourassa MW, De Vegt B, Gill J et al. 2019. From farm management to bacteriophage therapy: strategies to reduce antibiotic use in animal agriculture. Ann. N.Y. Acad. Sci. 1441:131–39
    [Google Scholar]
  104. 104. 
    Czaplewski L, Bax R, Clokie M, Dawson M, Fairhead H et al. 2016. Alternatives to antibiotics—a pipeline portfolio review. Lancet Infect. Dis. 16:2239–51
    [Google Scholar]
  105. 105. 
    Banerji A, Jahne M, Herrmann M, Brinkman N, Keely S 2019. Bringing community ecology to bear on the issue of antimicrobial resistance. Front. Microbiol. 10:2626
    [Google Scholar]
  106. 106. 
    Gordillo Altamirano FL, Barr JJ 2019. Phage therapy in the postantibiotic era. Clin. Microbiol. Rev. 32:e00066–18
    [Google Scholar]
  107. 107. 
    Klümper U, Recker M, Zhang L, Yin X, Zhang T et al. 2019. Selection for antimicrobial resistance is reduced when embedded in a natural microbial community. ISME J 13:122927–37
    [Google Scholar]
  108. 108. 
    Vrancianu CO, Popa LI, Bleotu C, Chifiriuc MC 2020. Targeting plasmids to limit acquisition and transmission of antimicrobial resistance. Front. Microbiol. 11:761
    [Google Scholar]
  109. 109. 
    Relman DA, Lipsitch M. 2018. Microbiome as a tool and a target in the effort to address antimicrobial resistance. PNAS 115:5112902–10
    [Google Scholar]
  110. 110. 
    Schulfer A, Blaser MJ. 2015. Risks of antibiotic exposures early in life on the developing microbiome. PLOS Pathog 11:7e1004903
    [Google Scholar]
  111. 111. 
    Arrieta M-C, Stiemsma LT, Dimitriu PA, Thorson L, Russell S et al. 2015. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci. Transl. Med. 7:307307ra152
    [Google Scholar]
  112. 112. 
    Mitre E, Susi A, Kropp LE, Schwartz DJ, Gorman GH, Nylund CM 2018. Association between use of acid-suppressive medications and antibiotics during infancy and allergic diseases in early childhood. JAMA Pediatr 172:6e180315
    [Google Scholar]
  113. 113. 
    Benoun JM, Labuda JC, McSorley SJ 2016. Collateral damage: detrimental effect of antibiotics on the development of protective immune memory. mBio 7:6e01520–16
    [Google Scholar]
  114. 114. 
    Oh JZ, Ravindran R, Chassaing B, Carvalho FA, Maddur MS et al. 2014. TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity 41:3478–92
    [Google Scholar]
  115. 115. 
    Ober RA, Thissen JB, Jaing CJ, Cino-Ozuna AG, Rowland RRR, Niederwerder MC 2017. Increased microbiome diversity at the time of infection is associated with improved growth rates of pigs after co-infection with porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2). Vet. Microbiol. 208:203–11
    [Google Scholar]
  116. 116. 
    Ruczizka U, Metzler-Zebeli B, Unterweger C, Mann E, Schwarz L et al. 2019. Early parenteral administration of ceftiofur has gender-specific short- and long-term effects on the fecal microbiota and growth in pigs from the suckling to growing phase. Animals 10:117
    [Google Scholar]
  117. 117. 
    Correa-Fiz F, Gonçalves dos Santos JM, Illas F, Aragon V 2019. Antimicrobial removal on piglets promotes health and higher bacterial diversity in the nasal microbiota. Sci. Rep. 9:16545
    [Google Scholar]
  118. 118. 
    Shahi F, Redeker K, Chong J 2019. Rethinking antimicrobial stewardship paradigms in the context of the gut microbiome. JAC Antimicrob. Resist. 1:1dlz015
    [Google Scholar]
  119. 119. 
    Nathwani D, Varghese D, Stephens J, Ansari W, Martin S, Charbonneau C 2019. Value of hospital antimicrobial stewardship programs (ASPs): a systematic review. Antimicrob. Resist. Infect. Control. 8:35
    [Google Scholar]
  120. 120. 
    Dik J-WH, Hendrix R, Poelman R, Niesters HG, Postma MJ et al. 2016. Measuring the impact of antimicrobial stewardship programs. Expert Rev. Anti-Infect. Ther. 14:6569–75
    [Google Scholar]
  121. 121. 
    Smith MJ, Gerber JS, Hersh AL 2015. Inpatient antimicrobial stewardship in pediatrics: a systematic review. J. Pediatr. Infect. Dis. Soc. 4:4e127–35
    [Google Scholar]
  122. 122. 
    McGregor JC, Weekes E, Forrest GN, Standiford HC, Perencevich EN et al. 2006. Impact of a computerized clinical decision support system on reducing inappropriate antimicrobial use: a randomized controlled trial. J. Am. Med. Inform. Assoc. 13:4378–84
    [Google Scholar]
  123. 123. 
    Scott RD, Slayton RB, Lessa FC, Baggs J, Culler SD et al. 2019. Assessing the social cost and benefits of a national requirement establishing antibiotic stewardship programs to prevent Clostridioides difficile infection in US hospitals. Antimicrob. Resist. Infect. Control 8:17
    [Google Scholar]
  124. 124. 
    Berge ACB, Moore DA, Besser TE, Sischo WM 2009. Targeting therapy to minimize antimicrobial use in preweaned calves: effects on health, growth, and treatment costs. J. Dairy Sci. 92:94707–14
    [Google Scholar]
  125. 125. 
    Weese JS, Giguère S, Guardabassi L, Morley PS, Papich M et al. 2015. ACVIM consensus statement on therapeutic antimicrobial use in animals and antimicrobial resistance. J. Vet. Intern. Med. 29:2487–98
    [Google Scholar]
  126. 126. 
    Gomez DE, Arroyo LG, Poljak Z, Viel L, Weese JS 2017. Implementation of an algorithm for selection of antimicrobial therapy for diarrhoeic calves: impact on antimicrobial treatment rates, health and faecal microbiota. Vet. J. 226:15–25
    [Google Scholar]
  127. 127. 
    Roope LSJ, Smith RD, Pouwels KB, Buchanan J, Abel L et al. 2019. The challenge of antimicrobial resistance: What economics can contribute. Science 364:6435eaau4679
    [Google Scholar]
  128. 128. 
    Murphy D, Ricci A, Auce Z, Beechinor JG, Bergendahl H et al. 2017. 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 (RONAFA). EFSA J 15:14666
    [Google Scholar]
  129. 129. 
    Hoelzer K, Bielke L, Blake DP, Cox E, Cutting SM et al. 2018. Vaccines as alternatives to antibiotics for food producing animals. Part 1: challenges and needs. Vet. Res. 49:64
    [Google Scholar]
  130. 130. 
    Hoelzer K, Bielke L, Blake DP, Cox E, Cutting SM et al. 2018. Vaccines as alternatives to antibiotics for food producing animals. Part 2: new approaches and potential solutions. Vet. Res. 49:70
    [Google Scholar]
  131. 131. 
    Kurt T, Wong N, Fowler H, Gay C, Lillehoj H et al. 2019. Strategic priorities for research on antibiotic alternatives in animal agriculture—results from an expert workshop. Front. Vet. Sci. 6:429
    [Google Scholar]
  132. 132. 
    Pres. Advis. Counc. Combat. Antibiot. Resist. Bact. 2017. Recommendations for incentivizing the development of vaccines, diagnostics, and therapeutics to combat antibiotic-resistance Rep., US Dep Health Hum. Serv. Washington, DC:
    [Google Scholar]
  133. 133. 
    World Health Organ. 2020. Global Antimicrobial Resistance Surveillance System (GLASS): country participation https://www.who.int/glass/country-participation/en/#enrolment
    [Google Scholar]
  134. 134. 
    Simjee S, McDermott P, Trott DJ, Chuanchuen R 2018. Present and future surveillance of antimicrobial resistance in animals: principles and practices. Microbiol. Spectr. 6:4 https://doi.org/10.1128/microbiolspec.ARBA-0028–2017
    [Crossref] [Google Scholar]
  135. 135. 
    Schrijver R, Stijntjes M, Rodríguez-Baño J, Tacconelli E, Babu Rajendran N, Voss A 2018. Review of antimicrobial resistance surveillance programmes in livestock and meat in EU with focus on humans. Clin. Microbiol. Infect. 24:6577–90
    [Google Scholar]
  136. 136. 
    Donado‐Godoy P, Castellanos R, León M, Arevalo A, Clavijo V et al. 2015. The establishment of the Colombian Integrated Program for Antimicrobial Resistance Surveillance (COIPARS): a pilot project on poultry farms, slaughterhouses and retail market. Zoonoses Public Health 62:Suppl. 158–69
    [Google Scholar]
  137. 137. 
    Schnall J, Rajkhowa A, Ikuta K, Rao P, Moore CE 2019. Surveillance and monitoring of antimicrobial resistance: limitations and lessons from the GRAM project. BMC Med 17:176
    [Google Scholar]
  138. 138. 
    Roberts RM, Smith GW, Bazer FW, Cibelli J, Seidel GE et al. 2009. Research priorities. Farm animal research in crisis. Science 324:5926468–69
    [Google Scholar]
  139. 139. 
    Found. Food Agric. Res. 2019. FFAR launches international consortium for antimicrobial stewardship in agriculture. News Jan. 20. https://foundationfar.org/2019/01/30/ffar-launches-international-consortium-for-antimicrobial-stewardship-in-agriculture/
    [Google Scholar]
  140. 140. 
    Natl. Inst. Allergy Infect. Dis. 2016. New public-private partnership will combat antimicrobial resistance. NIAID Funding News Aug. 24. https://www.niaid.nih.gov/grants-contracts/partnership-combats-antimicrobial-resistance
    [Google Scholar]
  141. 141. 
    Littmann J, Viens AM. 2015. The ethical significance of antimicrobial resistance. Public Health Ethics 8:3209–24
    [Google Scholar]
  142. 142. 
    Blanquart F. 2019. Evolutionary epidemiology models to predict the dynamics of antibiotic resistance. Evol. Appl. 12:3365–83
    [Google Scholar]
  143. 143. 
    Collignon P, Beggs JJ. 2019. Socioeconomic enablers for contagion: factors impelling the antimicrobial resistance epidemic. Antibiotics 8:386
    [Google Scholar]
  144. 144. 
    Hiltunen T, Virta M, Laine A-L 2017. Antibiotic resistance in the wild: an eco-evolutionary perspective. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372:171220160039
    [Google Scholar]
  145. 145. 
    Baquero F, Coque TM, de la Cruz F 2011. Ecology and evolution as targets: the need for novel eco-evo drugs and strategies to fight antibiotic resistance. Antimicrob. Agents Chemother. 55:83649–60
    [Google Scholar]
  146. 146. 
    Ghaly TM, Gillings MR. 2018. Mobile DNAs as ecologically and evolutionarily independent units of life. Trends Microbiol 26:11904–12
    [Google Scholar]
  147. 147. 
    Maltas J, Krasnick B, Wood KB 2020. Using selection by nonantibiotic stressors to sensitize bacteria to antibiotics. Mol. Biol. Evol. 37:51394–406
    [Google Scholar]
/content/journals/10.1146/annurev-animal-072020-080638
Loading
/content/journals/10.1146/annurev-animal-072020-080638
Loading

Data & Media loading...

  • 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