Antibiotics in agriculture and the risk to human health: How worried should we be?

Evolutionary Applications

Volumn 8, Issue 3, 2015, Pages 240-247

  Chang, Qiuzhi ^a   Wang, Weike ^a   Regev Yochay, Gili ^b,c   Lipsitch, Marc ^a   Hanage, William P ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b SHEBA MEDICAL CENTER   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Enterococcus; Staphylococcus aureus; Agriculture; Antibiotic resistance; Food; Resistance transfer

Indexed keywords

EID: 84925333020     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12185     Document Type: Article

References (62)

1. Aarestrup, F. M. 1999. Association between the consumption of antimicrobial agents in animal husbandry and the occurrence of resistant bacteria among food animals. International Journal of Antimicrobial Agents 12:279-285.
2. Aarestrup, F. M., P. Ahrens, M. Madsen, L. V. Pallesen, R. L. Poulsen, and H. Westh 1996. Glycopeptide susceptibility among Danish Enterococcus faecium and Enterococcus faecalis isolates of animal and human origin and PCR identification of genes within the vana cluster. Antimicrobial Agents and Chemotherapy 40:1938-1940.
3. Aarestrup, F. M., A. M. Seyfarth, H. D. Emborg, K. Pedersen, R. S. Hendriksen, and F. Bager 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. Antimicrobial Agents and Chemotherapy 45:2054-2059.
4. Anderson, S. A., R. W. Yeaton Woo, and L. M. Crawford 2001. Risk assessment of the impact on human health of resistant Campylobacter jejuni from fluoroquinolone use in beef cattle. Food Control 12:13-25.
5. Armand-Lefevre, L., R. Ruimy, and A. Andremont 2005. Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls, and pigs. Emerging Infectious Diseases 11:711-714.
6. Baker-Austin, C., M. S. Wright, R. Stepanauskas, and J. V. McArthur 2006. Co-selection of antibiotic and metal resistance. Trends in Microbiology 14:176-182.
7. Bartholomew, M. J., K. Hollinger, and D. Vose 2003. Characterizing the risk of antimicrobial use in food animals: fluoroquinolone-resistant campylobacter from consumption of chicken. In M. E. Torrence, and R. E. Isaacson, eds. Microbial Food Safety in Animal Agriculture: Current Topics pp. 293-301. Iowa State Press, Ames, IA.
8. Bebrone, C. 2007. Metallo-beta-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily. Biochemical Pharmacology 74:1686-1701.
9. Bonten, M. J., R. Willems, and R. A. Weinstein 2001. Vancomycin-resistant Enterococci: why are they here, and where do they come from? The Lancet Infectious Diseases 1:314-325.
10. Bowler, L. D., Q. Y. Zhang, J. Y. Riou, and B. G. Spratt 1994. Interspecies recombination between the penA genes of Neisseria meningitidis and commensal Neisseria species during the emergence of penicillin resistance in N. meningitidis: natural events and laboratory simulation. Journal of Bacteriology 176:333-337.
11. Centers for Disease Control and Prevention. 2013. Antibiotic Resistance Threats in the United States, 2013. http://www.cdc.gov/drugresistance/threat-report-2013/ (accessed on 6 March 2014).
12. Claycamp, H. G. 2006. Rapid benefit-risk assessments: no escape from expert judgments in risk management. Risk Analysis 26:147-156; discussion 157-161.
13. Coffey, T. J., C. G. Dowson, M. Daniels, and B. G. Spratt 1993. Horizontal spread of an altered penicillin-binding protein 2B gene between Streptococcus pneumoniae and Streptococcus oralis. FEMS Microbiology Letters 110:335-339.
14. Cox, L. A., and D. A. Popken 2006. Quantifying potential human health impacts of animal antibiotic use: Enrofloxacin and Macrolides in chickens. Risk Analysis 26:135-146.
15. Dowson, C. G., T. J. Coffey, C. Kell, and R. A. Whiley 1993. Evolution of penicillin resistance in Streptococcus pneumoniae; the role of Streptococcus mitis in the formation of a low affinity PBP2B in S. pneumoniae. Molecular Microbiology 9:635-643.
16. Engberg, J., F. M. Aarestrup, D. E. Taylor, P. Gerner-Smidt, and I. Nachamkin 2001. Quinolone and macrolide resistance in Campylobacter jejuni and C. Coli: resistance mechanisms and trends in human isolates. Emerging Infectious Diseases 7:24-34.
17. Fan, J., M. Shu, G. Zhang, W. Zhou, Y. Jiang, Y. Zhu, G. Chen et al. 2009. Biogeography and virulence of Staphylococcus aureus. PLoS ONE 4:e6216.
18. Fitzgerald, J. R. 2012. Livestock-associated Staphylococcus aureus: origin, evolution and public health threat. Trends in Microbiology 20:192-198.
19. Graveland, H., J. A. Wagenaar, K. Bergs, H. Heesterbeek, and D. Heederik 2011. Persistence of livestock associated MRSA CC398 in humans is dependent on intensity of animal contact. PLoS ONE 6:e16830.
20. Gupta, A., J. M. Nelson, T. J. Barrett, R. V. Tauxe, S. P. Rossiter, C. R. Friedman, K. W. Joyce et al. 2004. Antimicrobial resistance among Campylobacter strains, United States, 1997-2001. Emerging Infectious Diseases 10:1102-1109.
21. Hall, B. G., S. J. Salipante, and M. Barlow 2004. Independent origins of subgroup Bl + B2 and subgroup B3 metallo-beta-lactamases. Journal of Molecular Evolution 59:133-141.
22. Handwerger, S., B. Raucher, D. Altarac, J. Monka, S. Marchione, K. V. Singh, B. E. Murray et al. 1993. Nosocomial outbreak due to Enterococcus faecium highly resistant to vancomycin, penicillin, and gentamicin. Clinical Infectious Diseases 16:750-755.
23. Harrison, E. M., G. K. Paterson, M. T. G. Holden, J. Larsen, M. Stegger, A. R. Larsen, A. Petersen et al. 2013. Whole genome sequencing identifies zoonotic transmission of MRSA isolates with the novel mecA homologue mecC. EMBO Molecular Medicine 5:509-515.
24. Hasman, H., and F. M. Aarestrup 2002. tcrB, a gene conferring transferable copper resistance in Enterococcus faecium: occurrence, transferability, and linkage to macrolide and glycopeptide resistance. Antimicrobial Agents and Chemotherapy 46:1410-1416.
25. Hollis, A., and Z. Ahmed 2013. Preserving antibiotics, rationally. The New England Journal of Medicine 369:2474-2476.
26. Humphrey, T. J., F. Jørgensen, J. A. Frost, H. Wadda, G. Domingue, N. C. Elviss, D. J. Griggs et al. 2005. Prevalence and subtypes of ciprofloxacin-resistant Campylobacter spp. in commercial poultry flocks before, during, and after treatment with fluoroquinolones. Antimicrobial Agents and Chemotherapy 49:690-698.
27. IOM, Institute of Medicine. 1988. Human Health Risks with the Subtherapeutic Use of Penicillin Or Tetracyclines in Animal Feed. Committee on Human Health Risk Assessment of Using Subtherapeutic Antibiotics in Animal Feeds. National Academy Press, Washington, DC.
28. Jensen, L. B., A. M. Hammerum, R. L. Poulsen, and H. Westh 1999. Vancomycin-resistant Enterococcus faecium strains with highly similar pulsed-field gel electrophoresis patterns containing similar Tn1546-like elements isolated from a hospitalized patient and pigs in Denmark. Antimicrobial Agents and Chemotherapy 43:724-725.
29. Kennedy, D. 2013. Time to deal with antibiotics. Science 342:777.
30. Kos, V. N., C. A. Desjardins, A. Griggs, G. Cerqueira, A. Van Tonder, M. T. G. Holden, P. Godfrey et al. 2012. Comparative genomics of vancomycin-resistant Staphylococcus aureus strains and their positions within the clade most commonly associated with methicillin-resistant S. aureus hospital-acquired infection in the United States. mBio 3:e00112-12.
31. Lebreton, F., W. van Schaik, A. M. McGuire, P. Godfrey, A. Griggs, V. Mazumdar, J. Corander et al. 2013. Emergence of epidemic multidrug-resistant Enterococcus faecium from animal and commensal strains. mBio 4:e00534-13.
32. Levy, S. B. 1997. Antibiotic resistance: an ecological imbalance. Ciba Foundation Symposium 207:1-9; discussion 9-14.
33. Limbago, B. M., A. J. Kallen, W. Zhu, P. Eggers, L. K. McDougal, and V. S. Albrecht 2014. Report of the 13th vancomycin-resistant Staphylococcus aureus isolate from the United States. Journal of Clinical Microbiology 52:998-1002.
34. Lipsitch, M., R. S. Singer, and B. R. Levin 2002. Antibiotics in agriculture: when is it time to close the barn door? Proceedings of the National Academy of Sciences of the United States of America 99:5752-5754.
35. Marshall, B. M., and S. B. Levy 2011. Food animals and antimicrobials: impacts on human health. Clinical Microbiology Reviews 24:718-733.
36. McEwen, S. A. 2012. Quantitative human health risk assessments of antimicrobial use in animals and selection of resistance: a review of publicly available reports. Revue Scientifique et Technique (International Office of Epizootics) 31:261-276.
37. Mellon, M., C. Benbrook, and K. L. Benbrook 2001. Hogging it: estimates of antimicrobial abuse in livestock. Union of Concerned Scientists, UCS Publications, Cambridge, MA.
38. Nannapaneni, R., I. Hanning, K. C. Wiggins, R. P. Story, S. C. Ricke, and M. G. Johnson 2009. Ciprofloxacin-resistant Campylobacter persists in raw retail chicken after the fluoroquinolone ban. Food Additives & Contaminants Part A, Chemistry, Analysis, Control, Exposure & Risk Assessment 26:1348-1353.
39. Noble, W. C., Z. Virani, and R. G. Cree 1992. Co-transfer of vancomycin and other resistance genes from Enterococcus faecalis NCTC 12201 to Staphylococcus aureus. FEMS Microbiology Letters 72:195-198.
40. Noto, M. J., P. M. Fox, and G. L. Archer 2008. Spontaneous deletion of the methicillin resistance determinant, mecA, partially compensates for the fitness cost associated with high-level vancomycin resistance in Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 52:1221-1229.
41. Paarlberg, R. 2010. Food Politics: What Everyone Needs to Know. Oxford University Press, New York, NY.
42. Pantosti, A., M. Del Grosso, S. Tagliabue, A. Macrì, and A. Caprioli 1999. Decrease of vancomycin-resistant enterococci in poultry meat after avoparcin ban. Lancet 354:741-742.
43. Perron, G. G., S. Quessy, and G. Bell 2008. A reservoir of drug-resistant pathogenic bacteria in asymptomatic hosts. PLoS ONE 3:e3749.
44. Phillips, I. 2007. Withdrawal of growth-promoting antibiotics in Europe and its effects in relation to human health. International Journal of Antimicrobial Agents 30:101-107.
45. Phillips, I., M. Casewell, T. Cox, B. De Groot, C. Friis, R. Jones, C. Nightingale et al. 2004. Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. The Journal of Antimicrobial Chemotherapy 53:28-52.
46. Price, L. B., L. G. Lackey, R. Vailes, and E. Silbergeld 2007. The persistence of fluoroquinolone-resistant Campylobacter in poultry production. Environmental Health Perspectives 115:1035-1039.
47. Pugh, D. M. 2002. The EU precautionary bans of animal feed additive antibiotics. Toxicology Letters 128:35-44.
48. Scallan, E., R. M. Hoekstra, F. J. Angulo, R. T. Tauxe, M. A. Widdowson, S. L. Roy, J. L. Jones, and P. M. Griffin 2011. Foodborne Illness Acquired in the United States - Major Pathogens. Emerging Infectious Diseases. 17:7-15.
49. Shepheard, M. A., V. M. Fleming, T. R. Connor, J. Corander, E. J. Feil, C. Fraser, and W. P. Hanage 2013. Historical zoonoses and other changes in host tropism of Staphylococcus aureus, identified by phylogenetic analysis of a population dataset. PLoS ONE 8:e62369.
50. 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.
51. Smith, D. L., A. D. Harris, J. A. Johnson, E. K. Silbergeld, and J. Glenn Morris 2002. Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. Proceedings of the National Academy of Sciences of the United States of America 99:6434-6439.
52. Spoor, L. E., P. R. McAdam, L. A. Weinert, A. Rambaut, H. Hasman, F. M. Aarestrup, A. M. Kearns et al. 2013. Livestock origin for a human pandemic clone of community-associated methicillin-resistant Staphylococcus aureus. mBio 4:00356-13.
53. Stepanauskas, R., T. C. Glenn, C. H. Jagoe, R. C. Tuckfield, A. H. Lindell, and J. V. McArthur 2005. Elevated microbial tolerance to metals and antibiotics in metal-contaminated industrial environments. Environmental Science & Technology 39:3671-3678.
54. The Pew Commission on Industrial Farm Animal Production, 2008. Putting Meat on the Table: Industrial Farm Animal Production in America. The Pew Commission on Industrial Farm Animal Production. http://www.pewtrusts.org/en/research-and-analysis/reports/2008/04/29/putting-meat-on-the-table-industrial-farm-animal-production-in-america (accessed on 6 March 2014).
55. Travers, K., and M. Barza 2002. Morbidity of infections caused by antimicrobial-resistant bacteria. Clinical Infectious Diseases 34(Suppl 3):S131-S134.
56. Van der Mee-Marquet, N., P. François, A.-S. Domelier-Valentin, F. Coulomb, C. Decreux, C. Hombrock-Allet, O. Lehiani et al. 2011. Emergence of unusual bloodstream infections associated with pig-borne-like Staphylococcus aureus ST398 in France. Clinical Infectious Diseases 52:152-153.
57. Wang, Y., C. Wu, Q. Zhang, J. Qi, H. Liu, Y. Wang, T. He et al. 2012. Identification of New Delhi metallo-β-lactamase 1 in Acinetobacter lwoffii of food animal origin. PLoS ONE 7:e37152.
58. Weinert, L. A., J. J. Welch, M. A. Suchard, P. Lemey, A. Rambaut, and J. R. Fitzgerald 2012. Molecular dating of human-to-bovid host jumps by Staphylococcus aureus reveals an association with the spread of domestication. Biology Letters 8:829-832.
59. Willems, R. J. L., J. Top, M. van Santen, D. A. Robinson, T. M. Coque, F. Baquero, H. Grundmann et al. 2005. Global spread of vancomycin-resistant Enterococcus faecium from distinct nosocomial genetic complex. Emerging Infectious Diseases 11:821-828.
60. Willems, R. J. L., W. P. Hanage, D. E. Bessen, and E. J. Feil 2011. Population biology of gram-positive pathogens: high-risk clones for dissemination of antibiotic resistance. FEMS Microbiology Reviews 35:872-900.
61. Witte, W. 1998. Medical consequences of antibiotic use in agriculture. Science 279:996-997.
62. Woodford, N., A.-M. A. Adebiyi, M.-F. I. Palepou, and B. D. Cookson 1998. Diversity of vanA glycopeptide resistance elements in Enterococci from humans and nonhuman sources. Antimicrobial Agents and Chemotherapy 42:502-508.