Learning from agriculture: Understanding low-dose antimicrobials as drivers of resistome expansion

Frontiers in Microbiology

Volumn 5, Issue JUN, 2014, Pages

  You, Yaqi ^a   Silbergeld, Ellen K ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Agriculture; Antimicrobials; Environmental pollution; Metals; Microbiome; Mobilome; Resistome

Indexed keywords

EID: 84905171346     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00284     Document Type: Review

References (115)

1. Aarestrup, F. M., Seyfarth, A. M., Emborg, H. D., Pedersen, K., Hendriksen, R. S., and 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, 2054-2059. doi: 10.1128/AAC.45.7.2054-2059.2001
2. Agerso, Y., Wulff, G., Vaclavik, E., Halling-Sorensen, B., and Jensen, L. B. (2006). Effect of tetracycline residues in pig manure slurry on tetracycline-resistant bacteria and resistance gene tet(M) in soil microcosms. Environ. Int. 32, 876-882. doi: 10.1016/j.envint.2006.05.008
3. Allen, H. K., Donato, J., Wang, H. H., Cloud-Hansen, K. A., Davies, J., and Handelsman, J. (2010). Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8, 251-259. doi: 10.1038/nrmicro2312
4. Allen, H. K., Looft, T., Bayles, D. O., Humphrey, S., Levine, U. Y., Alt, D., et al. (2011). Antibiotics in feed induce prophages in swine fecal microbiomes. MBio 2, e00260-e00211. doi: 10.1128/mBio.00260-11
5. Amachawadi, R. G., Scott, H. M., Alvarado, C. A., Mainini, T. R., Vinasco, J., Drouillard, J. S., et al. (2013). Occurrence of the transferable copper resistance gene tcrB among fecal enterococci of US feedlot cattle fed copper-supplemented diets. Appl. Environ. Microb. 79, 4369-4375. doi: 10.1128/AEM.00503-13
6. Andersson, D. I., and Hughes, D. (2010). Antibiotic resistance and its cost: is it possible to reverse resistance? Nat. Rev. Microbiol. 8, 260-271. doi: 10.1038/nrmicro2319
7. Andrews, R. E. Jr., Johnson, W. S., Guard, A. R., and Marvin, J. D. (2004). Survival of enterococci and Tn916-like conjugative transposons in soil. Can. J. Microbiol. 50, 957-966. doi: 10.1139/w04-090
8. Arriola, C. S. (2011). Antimicrobial Resistant Bacteria and Use of Antimicrobials in Pig Farming in Peru. Ph.D. thesis, Johns Hopkins University.
9. Ashbolt, N. J., Amézquita, A., Backhaus, T., Borriello, P., Brandt, K. K., Collignon, P., et al. (2013). Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environ. Health Perspec. 121, 993-1001. doi: 10.1289/ehp.1206316
10. Baker-Austin, C., Wright, M. S., Stepanauskas, R., and McArthur, J. V. (2006). Co-selection of antibiotic and metal resistance. Trends Microbiol. 14, 176-182. doi: 10.1016/j.tim.2006.02.006
11. Baquero, F., Martinez, J. L., and Cantón, R. (2008). Antibiotics and antibiotic resistance in water environments. Curr. Opin. Biotech. 19, 260-265. doi: 10.1016/j.copbio.2008.05.006
12. Bass, L., Liebert, C. A., Lee, M. D., Summers, A. O., White, D. G., Thayer, S. G., et al. (1999). Incidence and characterization of integrons, genetic elements mediating multiple-drug resistance, in avian Escherichia coli. Antimicrob. Agents Chemother. 43, 2925-2929.
13. Beaber, J. W., Hochhut, B., and Waldor, M. K. (2003). SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427, 72-74. doi: 10.1038/nature02241
14. Bearson, B. L., Allen, H. K., Brunelle, B. W., Lee, I., Casjens, S. R., and Stanton, T. B. (2014). The agricultural antibiotic carbadox induces phage-mediated gene transfer in Salmonella. Front. Microbiol. 5:52. doi: 10.3389/fmicb.2014.00052
15. Binh, C. T. T., Heuer, H., Kaupenjohann, M., and Smalla, K. (2008). Piggery manure used for soil fertilization is a reservoir for transferable antibiotic resistance plasmids. FEMS Microbiol. Ecol. 66, 25-37. doi: 10.1111/j.1574-6941.2008.00526.x
16. Byrne-Bailey, K. G., Gaze, W. H., Zhang, L., Kay, P., Boxall, A., Hawkey, P. M., et al. (2011). Integron prevalence and diversity in manured soil. Appl. Environ. Microb. 77, 684-687. doi: 10.1128/AEM.01425-10
17. Cavaco, L. M., Hasman, H., and Aarestrup, F. M. (2011). Zinc resistance of Staphylococcus aureus of animal origin is strongly associated with methicillin resistance. Vet. Microbiol. 150, 344-348. doi: 10.1016/j.vetmic.2011.02.014
18. Cheng, W., Chen, H., Su, C., and Yan, S. (2013). Abundance and persistence of antibiotic resistance genes in livestock farms: a comprehensive investigation in eastern China. Environ. Int. 61, 1-7. doi: 10.1016/j.envint.2013.08.023
19. Cressman, M. D., Yu, Z., Nelson, M. C., Moeller, S. J., Lilburn, M. S., and Zerby, H. N. (2010). Interrelations between the microbiotas in the litter and in the intestines of commercial broiler chickens. Appl. Environ. Microbiol. 76, 6572-6582. doi: 10.1128/AEM.00180-10
20. Danzeisen, J. L., Kim, H. B., Isaacson, R. E., Tu, Z. J., and Johnson, T. J. (2011). Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment. PLoS ONE 6:e27949. doi: 10.1371/journal.pone.0027949
21. Davis, M. F., Silbergeld, E., Price, L. B., and Liu, C. M.-H. (2011). An ecological perspective on U.S. industrial poultry production: the role of anthropogenic ecosystems on the emergence of drug-resistant bacteria from agricultural environments. Curr. Opin. Microbiol. 14, 244-250. doi: 10.1016/j.mib.2011.04.003
22. D'Costa, V. M., Griffiths, E., and Wright, G. D. (2007). Expanding the soil antibiotic resistome: exploring environmental diversity. Curr. Opin. Microbiol. 10, 481-489. doi: 10.1016/j.mib.2007.08.009
23. D'Costa, V. M., McGrann, K. M., Hughes, D. W., and Wright, G. D. (2006). Sampling the antibiotic resistome. Science 311, 374-377. doi: 10.1126/science.1120800
24. Engster, H. M., Marvil, D., and Stewart-Brown, B. (2002). The effect of withdrawing growth promoting antibiotics from broiler chickens: a long-term commercial industry study. J. Appl. Poult. Res. 11, 431-436. doi: 10.1093/japr/11.4.431
25. FDA. (U.S. Food and Drug Administration). (2011). 2011 Summary Report on Antimicrobials Sold or Distributed for Use in Food-Producing Animals.
26. Forsberg, K. J., Reyes, A., Wang, B., Selleck, E. M., Sommer, M. O., and Dantas, G. (2012). The shared antibiotic resistome of soil bacteria and human pathogens. Science 337, 1107-1111. doi: 10.1126/science.1220761
27. Frost, L. S., Leplae, R., Summers, A. O., and Toussaint, A. (2005). Mobile genetic elements: the agents of open source evolution. Nat. Rev. Microbiol. 3, 722-732. doi: 10.1038/nrmicro1235
28. Furtula, V., Farrell, E. G., Diarrassouba, F., Rempel, H., Pritchard, J., and Diarra, M. S. (2009). Veterinary pharmaceuticals and antibiotic resistance of Escherichia coli isolates in poultry litter from commercial farms and controlled feeding trials. Poult. Sci. 89, 180-188. doi: 10.3382/ps.2009-00198
29. Garbarino, J. R., Bednar, A. J., Rutherford, D. W., Beyer, R. S., and Wershaw, R. L. (2003). Environmental fate of roxarsone in poultry litter. I. Degradation of roxarsone during composting. Environ. Sci. Technol. 37, 1509-1514. doi: 10.1021/es026219q
30. Gaze, W. H., Krone, S. M., Larsson, D. G. J., Li, X.-Z., Robinson, J. A., Simonet, P., et al. (2013). Influence of humans on evolution and mobilization of environmental antibiotic resistome. Emerg. Infect. Dis. 19, e120871. doi: 10.3201/eid1907.120871
31. Gerba, C. P., and Smith, J. E. (2005). Sources of pathogenic microorganisms and their fate during land application of wastes. J. Environ. Qual. 34, 42-48. doi: 10.2134/jeq2005.0042
32. Ghosh, S., and LaPara, T. M. (2007). The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME J. 1, 191-203. doi: 10.1038/ismej.2007.31
33. Gillings, M. R. (2013). Evolutionary consequences of antibiotic use for the resistome, mobilome and microbial pangenome. Front. Microbiol. 4:4. doi: 10.3389/fmicb.2013.00004
34. Graham, J. P., Boland, J. J., and Silbergeld, E. (2007). Growth promoting antibiotics in food animal production: an economic analysis. Public Health Rep. 122, 79-87.
35. Graham, J. P., Evans, S. L., Price, L. B., and Silbergeld, E. (2009a). Fate of antimicrobial-resistant enterococci and staphylococci and resistance determinants in stored poultry litter. Environ. Res. 109, 682-689. doi: 10.1016/j.envres.2009.05.005
36. Graham, J. P., Silbergeld, E., Price, L. B., Evans, S. L., and Graczyk, T. K. (2009b). Antibiotic resistant enterococci and staphylococci isolated from flies collected near confined poultry feeding operations. Sci. Total Environ. 407, 2701-2710. doi: 10.1016/j.scitotenv.2008.11.056
37. Graham, J. P., Leibler, J. H., Price, L. B., Otte, J. M., Pfeiffer, D. U., Tiensin, T., et al. (2008). The animal-human interface and infectious disease in industrial food animal production: rethinking biosecurity and biocontainment. Public Health Rep. 123, 282-299.
38. Graham, J. P., and Nachman, K. E. (2010). Managing waste from confined animal feeding operations in the United States: the need for sanitary reform. J. Water Health 8, 646-670. doi: 10.2166/wh.2010.075
39. Gullberg, E., Cao, S., Berg, O. G., Ilbäck, C., Sandegren, L., Hughes, D., et al. (2011). Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog. 7:e1002158. doi: 10.1371/journal.ppat.1002158
40. Gupta, G., and Charles, S. (1999). Trace elements in soils fertilized with poultry litter. Poult. Sci. 78, 1695-1698. doi: 10.1093/ps/78.12.1695
41. Halling-Sørensen, B., Sengeløv, G., and Tjørnelund, J. (2002). Toxicity of tetracyclines and tetracycline degradation products to environmentally relevant bacteria, including selected tetracycline-resistant bacteria. Arch. Environ. Con. Tox. 42, 263-271. doi: 10.1007/s00244-001-0017-2
42. Hammerum, A. M. (2012). Enterococci of animal origin and their significance for public health. Clin. Microbiol. Infect. 18, 619-625. doi: 10.1111/j.1469-0691.2012.03829.x
43. Hamscher, G., Pawelzick, H. T., and Höper, H. (2005). Different behavior of tetracyclines and sulfonamides in sandy soils after repeated fertilization with liquid manure. Environ. Toxicol. Chem. 24, 861-868. doi: 10.1897/04-182R.1
44. Hasman, H., and Aarestrup, F. M. (2002). tcrB, a gene conferring transferable copper resistance in Enterococcus faecium: occurrence, transferability, and linkage to macrolide and glycopeptide resistance. Antimicrob. Agents Chemother. 46, 1410-1416. doi: 10.1128/AAC.46.5.1410-1416.2002
45. Heuer, H., Focks, A., Lamshöft, M., Smalla, K., Matthies, M., and Spiteller, M. (2008). Fate of sulfadiazine administered to pigs and its quantitative effect on the dynamics of bacterial resistance genes in manure and manured soil. Soil Biol. Biochem. 40, 1892-1900. doi: 10.1016/j.soilbio.2008.03.014
46. Heuer, H., Schmitt, H., and Smalla, K. (2011). Antibiotic resistance gene spread due to manure application on agricultural fields. Curr. Opin. Microbiol. 14, 236-243. doi: 10.1016/j.mib.2011.04.009
47. Jackson, B. P., Bertsch, P. M., Cabrera, M. L., Camberato, J. J., Camberato, J. J., Seaman, J. C., et al. (2003). Trace element speciation in poultry litter. J. Environ. Qual. 32, 535-540. doi: 10.2134/jeq2003.5350
48. Jakobsen, L., Spangholm, D. J., Pedersen, K., Jensen, L. B., Emborg, H.-D., Agersø, Y., et al. (2010). Broiler chickens, broiler chicken meat, pigs and pork as sources of ExPEC related virulence genes and resistance in Escherichia coli isolates from community-dwelling humans and UTI patients. Int. J. Food Microbiol. 142, 264-272. doi: 10.1016/j.ijfoodmicro.2010.06.025
49. Jones, B. A., Grace, D., Kock, R., Alonso, S., Rushton, J., Said, M. Y., et al. (2013). Zoonosis emergence linked to agricultural intensification and environmental change. Proc. Natl. Acad. Sci. U.S.A. 110, 8399-8404. doi: 10.1073/pnas.1208059110
50. Joseph, S. W., Hayes, J. R., English, L. L., Carr, L. E., and Wagner, D. D. (2001). Implications of multiple antimicrobial-resistant enterococci associated with the poultry environment. Food Addit. Contam. 18, 1118-1123. doi: 10.1080/02652030110051275
51. Jukes, T. H. (1972). Antibiotics in animal feeds and animal production. Bioscience 22, 526-534. doi: 10.2307/1296312
52. Kav, A. B., Sasson, G., Jami, E., Doron-Faigenboim, A., Benhar, I., and Mizrahi, I. (2012). Insights into the bovine rumen plasmidome. Proc. Natl. Acad. Sci. U.S.A. 109, 5452-5457. doi: 10.1073/pnas.1116410109
53. Kemper, N. (2008). Veterinary antibiotics in the aquatic and terrestrial environment. Ecol. Indic. 8, 1-13. doi: 10.1016/j.ecolind.2007.06.002
54. Kim, H. B., Borewicz, K., White, B. A., Singer, R. S., Sreevatsan, S., Tu, Z. J., et al. (2012). Microbial shifts in the swine distal gut in response to the treatment with antimicrobial growth promoter, tylosin. Proc. Natl. Acad. Sci. U.S.A. 109, 15485-15490. doi: 10.1073/pnas.1205147109
55. Knapp, C. W., Dolfing, J., Ehlert, P. A. I., and Graham, D. W. (2010). Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ. Sci. Technol. 44, 580-587. doi: 10.1021/es901221x
56. Knapp, C. W., Engemann, C. A., Hanson, M. L., Keen, P. L., Hall, K. J., and Graham, D. W. (2008). Indirect evidence of transposon-mediated selection of antibiotic resistance genes in aquatic systems at low-level oxytetracycline exposures. Environ. Sci. Technol. 42, 5348-5353. doi: 10.1021/es703199g
57. Kohanski, M. A., DePristo, M. A., and Collins, J. J. (2010). Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol. Cell 37, 311-320. doi: 10.1016/j.molcel.2010.01.003
58. Kumar, K., Gupta, S. C., Chander, Y., and Singh, A. K. (2005). Antibiotic use in agriculture and its impact on the terrestrial environment. Adv. Agron. 87, 1-54. doi: 10.1016/S0065-2113(05)87001-4
59. Leibler, J. H., Otte, J., Roland-Holst, D., Pfeiffer, D. U., Magalhaes, R. S., Rushton, J., et al. (2009). Industrial food animal production and global health risks: exploring the ecosystems and economics of avian influenza. Ecohealth 6, 58-70. doi: 10.1007/s10393-009-0226-0
60. Leverstein-van Hall, M. A., Dierikx, C. M., Cohen Stuart, J., Voets, G. M., van den Munckhof, M. P., van Essen-Zandbergen, A., et al. (2011). Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin. Microbiol. Infect. 17, 873-880. doi: 10.1111/j.1469-0691.2011.03497.x
61. Levin, B. R., Perrot, V., and Walker, N. (2000). Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154, 985-997.
62. Looft, T., Johnson, T. A., Allen, H. K., Bayles, D. O., Alt, D. P., Stedtfeld, R. D., et al. (2012). In-feed antibiotic effects on the swine intestinal microbiome. Proc. Natl. Acad. Sci. U.S.A. 109, 1691-1696. doi: 10.1073/pnas.1120238109
63. Lorenz, M. G., and Wackernagel, W. (1994). Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Rev. 58, 563-602.
64. Martinez, J. L. (2009). Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ. Pollut. 157, 2893-2902. doi: 10.1016/j.envpol.2009.05.051
65. McKinney, C. W., Loftin, K. A., Meyer, M. T., Davis, J. G., and Pruden, A. (2010). tet and sul antibiotic resistance genes in livestock lagoons of various operation type, configuration, and antibiotic occurrence. Environ. Sci. Technol. 44, 6102-6109. doi: 10.1021/es9038165
66. Nandi, S., Maurer, J. J., Hofacre, C., and Summers, A. O. (2004). Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter. Proc. Natl. Acad. Sci. U.S.A. 101, 7118-7122. doi: 10.1073/pnas.0306466101
67. Novo, A., Andre, S., Viana, P., Nunes, O. C., and Manaia, C. M. (2013). Antibiotic resistance, antimicrobial residues and bacterial community composition in urban wastewater. Water Res. 47, 1875-1887. doi: 10.1016/j.watres.2013.01.010
68. Peak, N., Knapp, C. W., Yang, R. K., Hanfelt, M. M., Smith, M. S., Aga, D. S., et al. (2007). Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environ. Microbiol. 9, 143-151. doi: 10.1111/j.1462-2920.2006.01123.x
69. Pei, R., Kim, S.-C., Carlson, K. H., and Pruden, A. (2006). Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Res. 40, 2427-2435. doi: 10.1016/j.watres.2006.04.017
70. Perry, J. A., and Wright, G. D. (2013). The antibiotic resistance mobilome: searching for the link between environment and clinic. Front. Microbiol. 4:138. doi: 10.3389/fmicb.2013.00138
71. Pontiroli, A., Ceccherini, M.-T., Poté, J., Wildi, W., Kay, E., Nannipieri, P., et al. (2010). Long-term persistence and bacterial transformation potential of transplastomic plant DNA in soil. Res. Microbiol. 161, 326-334. doi: 10.1016/j.resmic.2010.04.009
72. Price, L. B., Stegger, M., Hasman, H., Aziz, M., Larsen, J., Andersen, P. S., et al. (2012). Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio 3, e00305-e00311. doi: 10.1128/mBio.00305-11
73. Pruden, A., Pei, R., Storteboom, H., and Carlson, K. H. (2006). Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ. Sci. Technol. 40, 7445-7450. doi: 10.1021/es060413l
74. Qu, A., Brulc, J. M., Wilson, M. K., Law, B. F., Theoret, J. R., Joens, L. A., et al. (2008). Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. PLoS ONE 3:e2945. doi: 10.1371/journal.pone.0002945
75. Raes, J., and Bork, P. (2008). Molecular eco-systems biology: towards an understanding of community function. Nat. Rev. Microbiol. 6, 693-699. doi: 10.1038/nrmicro1935
76. Rozen, D. E., McGee, L., Levin, B. R., and Klugman, K. P. (2007). Fitness costs of fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 51, 412-416. doi: 10.1128/AAC.01161-06
77. Rutherford, D. W., Bednar, A. J., Garbarino, J. R., Needham, R., Staver, K. W., and Wershaw, R. L. (2003). Environmental fate of roxarsone in poultry litter. Part II. Mobility of arsenic in soils amended with poultry litter. Environ. Sci. Technol. 37, 1515-1520. doi: 10.1021/es026222+
78. Sapkota, A. R., Lefferts, L. Y., McKenzie, S., and Walker, P. (2007). What do we feed to food-production animals? A review of animal feed ingredients and their potential impacts on human health. Environ. Health Perspect. 115, 663-670. doi: 10.1289/ehp.9760
79. Sarmah, A. K., Meyer, M. T., and Boxall, A. B. A. (2006). A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65, 725-759. doi: 10.1016/j.chemosphere.2006.03.026
80. Schentag, J. J., Klugman, K. P., Yu, V. L., Adelman, M. H., Wilton, G. J., Chiou, C. C., et al. (2007). Streptococcus pneumoniae bacteraemia: pharmacodynamic correlations with outcome and macrolide resistance-a controlled study. Int. J. Antimicrob. Agents 30, 264-269. doi: 10.1016/j.ijantimicag.2007.04.013
81. Sengelov, G., Agerso, Y., Halling-Sorensen, B., Baloda, S. B., Andersen, J. S., and Jensen, L. B. (2003). Bacterial antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry. Environ. Int. 28, 587-595. doi: 10.1016/S0160-4120(02)00084-3
82. Shade, A., Caporaso, J. G., Handelsman, J., Knight, R., and Fierer, N. (2013). A meta-analysis of changes in bacterial and archaeal communities with time. ISME J. 7, 1493-1506. doi: 10.1038/ismej.2013.54
83. Shanmugasundaram, R., Lilburn, M. S., and Selvaraj, R. K. (2011). Effect of recycled litter on immune cells in the cecal tonsils of chickens. Poult. Sci. 91, 95-100. doi: 10.3382/ps.2011-01800
84. Siefert, J. L. (2009). Defining the mobilome. Methods Mol. Biol. 532, 13-27. doi: 10.1007/978-1-60327-853-9_2
85. Silbergeld, E., Graham, J., and Price, L. B. (2008). Industrial food animal production, antimicrobial resistance, and human health. Annu. Rev. Public Health 29, 151-169. doi: 10.1146/annurev.publhealth.29.020907.090904
86. Silveira, E., Freitas, A. R., Antunes, P., Barros, M., Campos, J., Coque, T. M., et al. (2014). Co-transfer of resistance to high concentrations of copper and first- line antibiotics among Enterococcus from different origins (humans, animals, the environment and foods) and clonal lineages. J. Antimicrob. Chemother. 69, 899-906. doi: 10.1093/jac/dkt479
87. Singer, R. S., Ward, M. P., and Maldonado, G. (2006). Can landscape ecology untangle the complexity of antibiotic resistance? Nat. Rev. Microbiol. 4, 943-952. doi: 10.1038/nrmicro1553
88. Skurnik, D., Ruimy, R., Ready, D., Ruppe, E., Bernede-Bauduin, C., Djossou, F., et al. (2010). Is exposure to mercury a driving force for the carriage of antibiotic resistance genes? J. Med. Microbiol. 59, 804-807. doi: 10.1099/jmm.0.017665-0
89. Smet, A., Rasschaert, G., Martel, A., Persoons, D., Dewulf, J., Butaye, P., et al. (2011). In situ ESBL conjugation from avian to human Escherichia coli during cefotaxime administration. J. Appl. Microbiol. 110, 541-549. doi: 10.1111/j.1365-2672.2010.04907.x
90. Smith, M. S., Yang, R. K., Knapp, C. W., Niu, Y., Peak, N., Hanfelt, M. M., et al. (2004). Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR. Appl. Environ. Microb. 70, 7372-7377. doi: 10.1128/AEM.70.12.7372-7377.2004
91. Starr, M. P., and Reynolds, D. M. (1951). Streptomycin resistance of coliform bacteria from turkeys fed streptomycin. Am. J. Public Health Nations Health 41, 1375-1380. doi: 10.2105/AJPH.41.11_Pt_1.1375
92. Stepanauskas, R., Glenn, T. C., Jagoe, C. H., Tuckfield, R. C., Lindell, A. H., King, C. J., et al. (2006). Coselection for microbial resistance to metals and antibiotics in freshwater microcosms. Environ. Microbiol. 8, 1510-1514. doi: 10.1111/j.1462-2920.2006.01091.x
93. Stine, O. C., Johnson, J. A., Keefer-Norris, A., Perry, K. L., Tigno, J., Qaiyumi, S., et al. (2007). Widespread distribution of tetracycline resistance genes in a confined animal feeding facility. Int. J. Antimicrob. Agents 29, 348-352. doi: 10.1016/j.ijantimicag.2006.11.015
94. Stokstad, E. L. R., and Jukes, T. H 1958-1959 Studies of the growth-promoting effect of antibiotics in chicks on a purified diet. Antibiot. Ann. 6, 998-1002.
95. Stolz, J. F., Perera, E., Kilonzo, B., Kail, B., Crable, B., Fisher, E., et al. (2007). Biotransformation of 3-nitro-4-hydroxybenzene arsonic acid (roxarsone) and release of inorganic arsenic by Clostridium species. Environ. Sci. Tech. 41, 818-823. doi: 10.1021/es061802i
96. Storteboom, H. N., Kim, S.-C., Doesken, K. C., Carlson, K. H., Davis, J. G., and Pruden, A. (2007). Response of antibiotics and resistance genes to high-intensity and low-intensity manure management. J. Environ. Qual. 36, 1695-1703. doi: 10.2134/jeq2007.0006
97. Teuber, M. (2001). Veterinary use and antibiotic resistance. Curr. Opin. Microbiol. 4, 493-499. doi: 10.1016/S1369-5274(00)00241-1
98. Tolls, J. (2001). Sorption of veterinary pharmaceuticals in soils: a review. Environ. Sci. Technol. 35, 3397-3406. doi: 10.1021/es0003021
99. Tuckfield, R. C., and McArthur, J. V. (2008). Spatial analysis of antibiotic resistance along metal contaminated streams. Microb. Ecol. 55, 595-607. doi: 10.1007/s00248-007-9303-5
100. Vandenberg, L. N. (2014). Low-dose effects of hormones and endocrine disruptors. Vitam. Horm. 94, 129-165. doi: 10.1016/B978-0-12-800095-3.00005-5
101. van Elsas, J. D., Turner, S., and Bailey, M. J. (2003). Horizontal gene transfer in the phytosphere. New Phytol. 157, 525-537. doi: 10.1046/j.1469-8137.2003.00697.x
102. van Loo, I., Huijsdens, X., and Tiemersma, E. (2007). Emergence of methicillin-resistant Staphylococcus aureus of animal origin in humans. Emerg. Infect. Dis. 13, 1834-1839. doi: 10.3201/eid1312.070384
103. Volkova, V. V., Bailey, R. H., and Wills, R. W. (2009). Salmonella in broiler litter and properties of soil at farm location. PLoS ONE 4:e6403. doi: 10.1371/journal.pone.0006403
104. Waters, A. E., Contente-Cuomo, T., Buchhagen, J., Liu, C. M., Watson, L., Pearce, K., et al. (2011). Multidrug-Resistant Staphylococcus aureus in US meat and poultry. Clin. Infect. Dis. 52, 1227-1230. doi: 10.1093/cid/cir181
105. Wegener, H. C. (2003). Antibiotics in animal feed and their role in resistance development. Curr. Opin. Microbiol. 6, 439-445. doi: 10.1016/j.mib.2003.09.009
106. Wei, S., Morrison, M., and Yu, Z. (2013). Bacterial census of poultry intestinal microbiome. Poult. Sci. 92, 671-683. doi: 10.3382/ps.2012-02822
107. Wozniak, R. A. F., and Waldor, M. K. (2010). Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat. Rev. Microbiol. 8, 552-563. doi: 10.1038/nrmicro2382
108. Wright, G. D. (2007). The antibiotic resistome: the nexus of chemical and genetic diversity. Nat. Rev. Microbiol. 5, 175-186. doi: 10.1038/nrmicro1614
109. Wu, N., Qiao, M., Zhang, B., Cheng, W.-D., and Zhu, Y.-G. (2010). Abundance and diversity of tetracycline resistance genes in soils adjacent to representative swine feedlots in China. Environ. Sci. Technol. 44, 6933-6939. doi: 10.1021/es1007802
110. You, Y., Hilpert, M., and Ward, M. J. (2012). Detection of a common and persistent tet(L)-carrying plasmid in chicken-waste-impacted farm soil. Appl. Environ. Microb. 78, 3203-3213. doi: 10.1128/AEM.07763-11
111. You, Y., Hilpert, M., and Ward, M. J. (2013). Identification of Tet45, a tetracycline efflux pump, from a poultry-litter-exposed soil isolate and persistence of tet(45) in the soil. J. Antimicrob. Chemother. 68, 1962-1969. doi: 10.1093/jac/dkt127
112. Zhang, X.-X., Zhang, T., and Fang, H. H. P. (2009). Antibiotic resistance genes in water environment. Appl. Microbiol. Biotechnol. 82, 397-414. doi: 10.1007/s00253-008-1829-z
113. Zhou, W., Wang, Y., and Lin, J. (2012). Functional cloning and characterization of antibiotic resistance genes from the chicken gut microbiome. Appl. Environ. Microb. 78, 3028-3032. doi: 10.1128/AEM.06920-11
114. Zhu, Y.-G., Johnson, T. A., Su, J.-Q., Qiao, M., Guo, G.-X., Guo, F., et al. (2013). Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc. Natl. Acad. Sci. U.S.A. 110, 3435-3440. doi: 10.1073/pnas.1222743110
115. Zinsstag, J., Schelling, E., Waltner-Toews, D., and Tanner, M. (2011). From one medicine to one health and systemic approaches to health and well-being. Prev. Vet. Med. 101, 148-156. doi: 10.1016/j.prevetmed.2010.07.003