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Chapter 12 : The Evolution of Antibiotic-Resistant Microbes in Foods and Host Ecosystems

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Abstract:

In the years between the introduction of antibiotic therapy and the mid-1970s, antibiotic-resistant bacteria were generally restricted to the hospital setting and epidemic diseases which were not major issues in much of the industrialized world. In this chapter, the development of tetracycline-resistant (Tc) fish pathogens and bacteria associated with aquaculture environments is discussed. Antibiotic residues may be found in a variety of foods produced around the world. Currently, unlabeled but high levels of cephalosporins (ceftiofur) are allowed in some foods. Rules exist which aim to minimize the level of antibiotic residues found in food products; however, not all foods are tested, nor is it clear that the standards required by farms in North America and Europe are followed when the food is produced for overseas consumption. The majority of the novel genes were mobile elements carrying antibiotic resistance and virulence genes. are normal inhabitants of the intestinal flora of most mammals, birds, and humans, as well as from soil, surface waters, plants, vegetables, raw foods such as milk and meat, and fermented meats such as Italian salami or raw sausage. Studies have shown that fish foods, even unlabeled ones, may contain antibiotic-resistant bacteria and/or antibiotic residues. This chapter also illustrates a few examples in which specific antibiotic resistance genes, regions of DNA, and/or plasmids have been found in bacteria from very different ecosystems, from different parts of the world, and in bacteria that are host species-specific.

Citation: Roberts M. 2009. The Evolution of Antibiotic-Resistant Microbes in Foods and Host Ecosystems, p 213-229. In Jaykus L, Wang H, Schlesinger L (ed), Food-Borne Microbes. ASM Press, Washington, DC. doi: 10.1128/9781555815479.ch12

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1. Aarestrup, F. M.,, Y. Agerso,, P. Gerner-Smidt,, M. Madsen, and, L. B. Jensen. 2000. Comparison of antimicrobial resistance pheno-types and resistance genes in Enterococcus faecalis and Enterococcus faecium from humans in the community, broilers, and pigs in Denmark. Diagn. Microbiol. Infect. Dis. 37:127137.
2. Aarestrup, F. M.,, P. Butaye, and, W. Witte. 2002. Nonhuman reservoirs of enterococci, p. 5599. In M. S. Gilmore,, D. B. Clewell,, P. Courvalin,, G. M. Dunny,, B. E. Murray, and, L. B. Rice (ed.), The Enterococci: Pathogenesis, Molecular Biology, and Antibiotic Resistance. ASM Press, Washington, DC.
3. Aarestrup, F. M.,, R. S. Hendriksen,, J. Lockett,, K. Gay,, K. Teates,, P. F. McDermott,, D. G. White,, H. Hasman,, G. Sorenen,, A. Bangtrakulonth,, S. Pornreongwong,, C. Puylsrikarn,, F. J. Angulo, and, P. Garner-Smidt. 2007. International spread of multidrug-resistant Salmonella Schwarzengrund in food products. Emerg. Infect. Dis. 13:726731.
4. Aarestrup, F. M.,, H. Kruse,, E. Tast,, A. M. Hammerum, and, L. B. Jensen. 2000. Associations between the use of antimicrobial agents for growth promotion and the occurrence of resistance among Enterococcus faecium from broilers and pigs in Denmark, Finland, and Norway. Microb. Drug Resist. 6:6370.
5. Akiba, T.,, L. Koyama,, Y. Ishiki,, S. Kimura, and, T. Rukushima. 1960. On the mechanism of the development of multiple-drug-resistant clones of Shigella. Jpn. J. Microbiol. 4:219227.
6. Anderson, A. A.,, J. Dugan,, L. Jones, and, D. Rockey. 2004. Stable chlamydial tetracycline resistance associated with a tet (C) resistance allele. Antimicrob. Agents Chemother. 48:39893995.
7. Aoki, T. 1988. Drug-resistant plasmids from fish pathogens. Microbiol. Sci. 5:219223.
8. Atkinson, B. A.,, A. Abu-Al-Jaibat, and, D. J. LeBlanc. 1997. Antibiotic resistance among enterococci isolated from clinical specimens between 1953 and 1954. Antimicrob. Agents Chemother. 41:15981600.
9. Bager, F.,, M. Madsen,, J. Christensen, and, F. M. Aarestrup. 1997. Avoparcin used as a growth promoter is associated with the occurrence of vancomycin-resistant Enterococcus faecium on Danish poultry and pig farms. Prev. Vet. Med. 31:95112.
10. Bates, J. 1997. Epidemiology of vancomycin-resistant enterococci in the community and the relevance of farm animals to human infection. J. Hosp. Infect. 37:507514.
11. Beltrametti, F.,, A. Consolandi,, L. Carrano,, F. Bagatin,, R. Rossi,, L. Leoni,, E. Zennaro,, E. Selva, and, F. Marinelli. 2007. Resistance to glycopeptide antibiotics in the teicoplanin producer is mediated by van gene homologue expression directing the synthesis of a modified cell wall peptidoglycan. Antimicrob. Agents Chemother. 51:11351141.
12. Bonomo, R. A.,, A. M. Hujer, and, K. M. Hujer. 2007. Integrons and superintegrons, p. 331338. In R. A. Bonomo and, M. Tolmasky (ed.), Enzyme-Mediated Resistance to Antibiotics: Mechanisms, Dissemination, and Prospects for Inhibition. ASM Press, Washington, DC.
13. Brazil, G.,, D. Curley,, F. Gannon, and, P. Smith. 1986. Persistence and acquisition of antibiotic resistance plasmids in Aeromonas salmonicida, p. 107114. In S. B. Levy and, R. P. Novick (ed.), Antibiotic Resistance Genes: Ecology, Transfer, and Expression. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
14. Brisson-Noel, A.,, M. Arthur, and, P. Courvalin. 1988. Evidence for natural gene transfer from gram-positive cocci to Escherichia coli. J. Bacteriol. 170:17391745.
15. Bush, K., and, P. A. Bradford. 2007. β-Lactamases: historical perspectives, p. 6779. In R. A. Bonomo and, M. Tolmasky (ed.), Enzyme-Mediated Resistance to Antibiotics: Mechanisms, Dissemination, and Prospects for Inhibition. ASM Press, Washington, DC.
16. Casas, C.,, E. C. Anderson,, K. K. Ojo,, I. Keith,, D. Whelan,, D. Rainnie, and, M. C. Roberts. 2005. Characterization of pRAS1-like plasmids from atypical North American psychrophilic Aeromonas salmonicida. FEMS Microbiol. Lett. 242:5963.
17. Chalkley, L. J., and, H. J. Koornhof. 1990. Intra- and inter-specific transformation of Streptococcus pneumoniae to penicillin resistance. J. Antimicrob. Chemother. 26:2128.
18. Chambers, P. A.,, P. S. Duggan,, J. Heritage, and, J. M. Forbes. 2002. The fate of antibiotic resistance marker genes in transgenic plant feed material fed to chickens. J. Antimicrob. Chemother. 49:161164.
19. Chapin, A.,, A. Rule,, K. Gibson,, T. Buckley, and, K. Schwab. 2005. Airborne multidrug-resistant bacteria isolated from a concentrated swine feeding operation. Environ. Health Perspect. 113:137142.
20. Chee-Sanford, J. C.,, R. I. Aminov,, I. J. Krapac,, N. Garrigues-Jeanjean, and, R. I. Mackie. 2001. Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities. Appl. Environ. Microbiol. 67:14941502.
21. Chopra, I., and, M. Roberts. 2001. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol. Mol. Biol. Rev. 65:232260.
22. Collignon, P., and, F. M. Aarestrup. 2007. Extended-spectrum β-lactamases, food, and cephalosporin use in food animals. Clin. Infect. Dis. 44:13911392.
23. Cousin, S. L., Jr.,, W. L. Whittington, and, M. C. Roberts. 2003. Acquired macrolide resistance genes in pathogenic Neisseria spp. isolated between 1940 and 1987. Antimicrob. Agents Chemother. 47:38773880.
24. Craig, M. L.,, R. Craigie,, M. Gellert, and, A. M. Lambowitz (ed.). 2002. Mobile DNA II. American Society for Microbiology, Washington, DC.
25. DePaola, A.,, P. A. Flynn,, R. M. McPhearson, and, S. B. Levy. 1988. Phenotypic and genotypic characterization of tetracyclineand oxytetracycline-resistant Aeromonas hydrophila from cultured channel catfish (Ictalurus punctatus) and their environments. Appl. Environ. Microbiol. 54:18611863.
26. deVries, J.,, M. Heine,, K. Harms, and, W. Wackernagel. 2003. Spread of recombinant DNA by roots and pollen of transgenic potato plants, identified by highly specific biomonitoring using natural transformation of an Acinetobacter sp. Appl. Environ. Microbiol. 69:44554462.
27. Doern, G. V.,, A. Brueggemann,, H. P. Holley, and, A. M. Rauch. 1996. Antimicrobial resistance of Streptococcus pneumoniae recovered from outpatients in the United States during the winter months of 1994 to 1995: results of a 30-center national surveillance study. Antimicrob. Agents Chemother. 40:12081213.
28. Donabedian, S. M.,, L. A. Thal,, E. Hershberger,, M. B. Perri,, J. W. Chow,, P. Bartlett,, R. Jones,, K. Joyce,, S. Rossiter,, K. Gay,, J. Johnson,, C. Mackinson,, E. DeBess,, J. Madden,, F. Angulo, and, M. J. Zervos. 2003. Molecular characterization of gentamicin-resistant enterococci in the United States: evidence of spread from animals to humans through food. J. Clin. Microbiol. 41:11091113.
29. Edlind, T. D. 1991. Protein synthesis as a target for antiprotozoal drugs, p. 569586. In G. Coombs and, M. North (ed.), Biochemical Protozoology. Taylor and Francis, London, England.
30. Emborg, H.,, A. K. Ersboll,, O. E. Heuer, and, H. C. Wegener. 2001. The effect of discontinuing the use of antimicrobial growth promoters on the productivity in the Danish broiler production. Prev. Vet. Med. 50:5370.
31. Falkow, S. 1977. Infectious Multiple Drug Resistance. Pion Limited, London, England.
32. Fey, P. D.,, T. J. Safranek,, M. E. Rupp,, E. F. Dunne,, E. Ribot,, P. C. Iwen,, P. A. Bradford,, F. J. Angulo, and, S. H. Hinrichs. 2000. Ceftriaxone-resistant salmonella infection acquired by a child from cattle. N. Engl. J. Med. 342:12421249.
33. Flannagan, S. E.,, J. W. Chow,, S. M. Donabedian,, W. J. Brown,, M. B. Perri,, M. J. Zervos,, Y. Ozawa, and, D. B. Clewell. 2003. Plasmid content of a vancomycin-resistant Enter-ococcus faecalis isolate from a patient also colonized by Staphylococcus aureus with a VanA phenotype. Antimicrob. Agents Chemother. 47:39543959.
34. Gambarotto, K.,, M. C. Ploy,, F. Dupron,, M. Giangiobbe, and, F. Denis. 2001. Occurrence of vancomycin-resistant enterococci in pork and poultry products from a cattle-rearing area of France. J. Clin. Microbiol. 39:23542355.
35. Gibbs, S. G.,, C. F. Green,, P. M. Tarwater, and, P. V. Scarpino. 2004. Airborne antibiotic resistant and nonresistant bacteria and fungi recovered from two swine herd confined animal feeding operations. J. Occup. Environ. Hyg. 1:699706.
36. Giraffa, G. 2002. Enterococci from foods. FEMS Microbiol. Rev. 26:163171.
37. Griffith, F. 1928. The significance of pneumococcal types. J. Hyg. 27:113159. [Reprint, J. Hyg. 64:129175, 1966.]
38. Hayes, J. R.,, L. L. English,, P. J. Carter,, T. Proescholdt,, K. Y. Lee,, D. D. Wagner, and, D. G. White. 2003. Prevalence and antimicrobial resistance of Enterococcus species isolated from retail meats. Appl. Environ. Microbiol. 69:71537160.
39. Herwig, R. P.,, J. P. Gray, and, D. P. Weston. 1997. Antibacterial resistant bacteria in surficial sediments near salmon net-cage farms in Puget Sound, Washington. Aquaculture 149:263283.
40. Holden, M. T. G.,, E. J. Feil,, J. A. Lindsay,, S. J. Peacock,, N. P. J. Day,, M. C. Enright,, T. J. Foster,, C. E. Moore,, L. Hurst,, R. Atkin,, A. Barron,, N. Bason,, S. D. Bentley,, C. Chillingworth,, T. Chillingworth,, C. Churcher,, L. Clark,, C. Corton,, A. Cronin,, J. Doggett,, L. Dowd,, T. Feltwell,, Z. Hance,, B. Harris,, H. Hauser,, S. Holroyd,, K. Jagels,, K. D. James,, N. Lennard,, A. Line,, R. Mayes,, S. Mould,, K. Mungall,, D. Ormond,, M. A. Quail,, E. Rabbinowitch,, K. Rutherford,, M. Sanders,, S. Sharp,, M. Simmonds,, K. Stevens,, S. Whitehead,, G. G. Barrell,, B. G. Spratt, and, J. Parkhill. 2004. Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc. Natl. Acad. Sci. USA 101:97869791.
41. Hughes, V. M., and, N. Datta. 1983. Conjugative plasmids in bacteria of the “pre-antibiotic” era. Nature 302:725726.
42. Institute of Medicine, Division of Health Promotion and Disease Prevention. 1998. Report of a Study. Human Health Risks With the Subtherapeutic Use of Penicillin or Tetracyclines in Animal Feed. National Academy Press, Washington, DC.
43. Jackson, C. R.,, P. J. Fedorka-Cray,, J. B. Barrett, and, S. R. Ladely. 2004. Effects of tylosin use on erythromycin resistance in enterococci isolated from swine. Appl. Environ. Microbiol. 70:42054210.
44. Jensen, L. B.,, Y. Agerso, and, G. Sengelov. 2002. Presence of erm genes among macrolide-resistant Gram-positive bacteria isolated from Danish farm soil. Environ. Int. 28:487491.
45. Jensen, L. B.,, A. M. Hammerum,, F. Bager, and, F. M. Aarestrup. 2002. Streptogramin resistance among Enterococcus faecium isolated from production animals in Denmark in 1997. Microb. Drug Resist. 8:369374.
46. Jones, C. S.,, D. J. Osborne, and, J. Stanley. 1992. Enterobacterial tetracycline resistance in relation to plasmid incompatibility. Mol. Cell. Probes 6:313317.
47. Kay, E.,, T. M. Vogel,, F. Bertolla,, R. Natlin, and, P. Simonet. 2002. In situ transfer of antibiotic resistance genes from transgenic (transplastomic) tobacco plants to bacteria. Appl. Environ. Microbiol. 68:33453351.
48. Kim, E. H., and, T. Aoki. 1994. The transposon-like structure of IS26-tetracycline, and kanamycin resistance determinant derived from transferable R plasmids of fish pathogen, Pasteurella piscicida. Microbiol. Immunol. 38:3138.
49. Klare, I.,, C. Konstabel,, G. Werner,, G. Huys,, V. Vankerckhoven,, G. Kahlmeter,, B. Hildebrandt,, S. Muller-Bertling,, W. Witte, and, H. Goossens. 2007. Antimicrobial susceptibilities of Lactobacillus, Pediococcus and Lactococcus human isolates and cultures intended for pro-biotic or nutritional use. J. Antimicrob. Chemother. 59:900912.
50. Lederberg, J. 1952. Cell genetics and hereditary symbiosis. Physiol. Rev. 32:403430.
51. Lester, C. H.,, N. Frimodt-Moller,, T. L. Sorensen,, D. L. Monnet, and, A. M. Hammerum. 2006. In vivo transfer of the vanA gene between Enterococcus faecium strains and the intestine of humans. Antimicrob. Agents Chemother. 50:596599.
52. Levy, S. B. 2002. The Antibiotic Paradox: How the Misuse of Antibiotics Destroys Their Curative Powers, 2nd ed. Plenum Press, New York, NY.
53. Livermore, D. M. 2002. Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: or worst nightmare? Clin. Infect. Dis. 34:634640.
54. Lu, K.,, R. Asano, and, J. Davies. 2004. Antimicrobial resistance gene delivery in animal feeds. Emerg. Infect. Dis. 10:679683.
55. Luna, V. A.,, S. Cousin,, W. L. Whittington, and, M. C. Roberts. 2000. Identification of the conjugative mef gene in clinical Acinetobacter junii and Neisseria gonorrhoeae isolates. Antimicrob. Agents Chemother. 44:25032506.
56. Luna, V. A.,, M. Heiken,, K. Judge,, C. Ulep,, C.,, N. Van Kirk,, H. Luis,, M. Bernardo,, J. Leitao, and, M. C. Roberts. 2002. Distribution of mef (A) in gram-positive bacteria from healthy Portuguese children. Antimicrob. Agents Chemother. 46:25132517.
57. Macovei, L., and, L. Zurek. 2006. Ecology of antibiotic resistance genes: characterization of enterococci from houseflies collected in food settings. Appl. Environ. Microbiol. 72:40284035.
58. Malbruny, B.,, A. Canu,, B. Bozdogan,, B. Fantin,, V. Zarrouk,, S. Dutka-Malen,, C. Feger, and, R. Leclercq. 2002. Resistance to quinupristin-dalfopristin due to mutations of L22 ribosomal protein in Staphylococcus aureus. Anti-microb. Agents Chemother. 46:22002207.
59. Malbruny, B.,, K. Nagai,, M. Coquemont,, B. Bozdogan,, A. T. Andrasevic,, H. Hupkova,, R. Leclercq, and, P. C. Appelbaum. 2002. Resistance to macrolides in clinical isolates of Streptococcus pyogenes due to ribosomal mutations. J. Antimicrob. Chemother. 49:935939.
60. Martel, A.,, L. A. Devriese,, A. Decostere, and, F. Haesebrouck. 2003. Presence of macrolide resistance genes in streptococci and enter-ococci isolated from pigs and pork carcasses. Int. J. Food Microbiol. 84:2732.
61. McClintock, B. 1950. The origin and behavior of mutable loci in maize. Proc. Natl. Acad. Sci. USA 36:344349.
62. McManus, P. S.,, V. O. Stockwell,, G. W. Sundin, and, A. L. Jones. 2002. Antibiotic use in plant agriculture. Annu. Rev. Phytopathol. 40:443465.
63. Mendez, B.,, C. Tachibana, and, S. B. Levy. 1980. Heterogeneity of tetracycline resistance determinants. Plasmid 3:99108.
64. Miranda, C. D.,, C. Kehrenberg,, C. Ulep,, S. Schwarz, and, M. C. Roberts. 2003. Diversity of tetracycline resistance genes in bacteria from Chilean salmon farms. Antimicrob. Agents Che-mother. 47:883888.
65. Nandi, S.,, J. J. Maurer,, C. Hofacre, and, A. O. Summers. 2004. Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter. Proc. Natl. Acad. Sci. USA 101:71187122.
66. National Research Council. 1999. The Use of Drugs in Food Animals: Benefits and Risks. National Academy Press, Washington, DC.
67. Novick, R. P. 1987. Plasmid incompatibility. Microbiol. Rev. 51:381395.
68. Ojo, K. K.,, C. Ulep,, N. Van Kirk,, H. Luis,, M. Bernardo,, J. Leitao, and, M. C. Roberts. 2004. The mef (A) gene predominates among seven macrolide resistance genes identified in gram-negative strains representing 13 genera, isolated from healthy Portuguese children. Antimicrob. Agents Chemother. 48:34513456.
69. Page, M. G. 2007. Resistance mediated by penicillin-binding proteins, p. 8199. In R. A. Bonomo and, M. Tolmasky (ed.), Enzyme-Mediated Resistance to Antibiotics: Mechanisms, Dissemination, and Prospects for Inhibition. ASM Press, Washington, DC.
70. Pang, Y.,, B. A. Brown,, V. A. Steingrube,, R. J. Wallace, Jr., and, M. C. Roberts. 1994. Tetracycline resistance determinants in Mycobacterium and Streptomyces species. Antimicrob. Agents Chemother. 38:14081412.
71. Rhodes, G.,, G. Huys,, J. Swings,, P. McGann,, M. Hiney,, P. Smith, and, R. W. Pickup. 2000. Distribution of oxytetracycline resistance plasmids between aeromonads in hospital and aquaculture environments: implication of Tn1721 in dissemination of the tetracycline resistance determinant Tet A. Appl. Environ. Microbiol. 66:38833890.
72. Rice, L. B. 2007. Conjugative transposons, p. 271284. In R. A. Bonomo and, M. Tolmasky (ed.). Enzyme-Mediated Resistance to Antibiotics: Mechanisms, Dissemination, and Prospects for Inhibition. ASM Press, Washington, DC.
73. Roberts, M. C. 1989. Plasmids of Neisseria gonorrhoeae and other Neisseria species. Rev. Clin. Microbiol. 2:S18S23.
74. Roberts, M. C. 1997. Genetic mobility and distribution of tetracycline resistance determinants. Ciba Found. Symp. 207:206218.
75. Roberts, M. C. 1998. Antibiotic resistance in oral/respiratory bacteria. Crit. Rev. Oral Biol. Med. 9:522540.
76. Roberts, M. C. 2002. Antibiotic toxicity, interactions and resistance development. Periodontology 2000. 28:280297.
77. Roberts, M. C. 2005. Update on acquired tetracycline resistance genes. FEMS Microbiol. Lett. 245:195203.
78. Roberts, M. C. 2006. Multidrug resistant genes associated with a 86 kb island in Acinetobacter baumannii. Trends Microbiol. 14:375378.
79. Roberts, M. C.,, B. Facinelli,, E. Giovanetti,, C. Casolari, and, P. E. Varaldo. 1996. Transferable erythromycin resistance in food isolates of Listeria. Appl. Environ. Microbiol. 62:269270.
80. Robicsek, A.,, G. A. Jacoby, and, D. C. Hooper. 2006. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect. Dis. 6:629640.
81. Rodríguez, C.,, L. Lang,, A. Wang,, K. Altendorf,, F. García, and, A. Lipski. 2006. Lettuce for human consumption collected in Costa Rica contains complex communities of culturable oxytetracycline- and gentamicin-resistant bacteria. Appl. Environ. Microbiol. 72:58705876.
82. Sapkota, A. R.,, K. K. Ojo,, M. C. Roberts, and, K. J. Schwab. 2006. Antibiotic resistance genes in multidrug-resistant Enterococcus spp. and Streptococcus spp. recovered from indoor air of a concentrated swine feeding operation. Lett. Appl. Microbiol. 43:534540.
83. Scarpino, P. V., and, H. Quinn. 1998. Bioaerosol distribution patterns adjacent to two swine-growing-finishing housed confinement units in the American Midwest. J. Aerosol Sci. 29:S553.
84. Schnabel, E. L., and, A. L. Jones. 1999. Distribution of tetracycline resistance genes and transposons among phylloplane bacteria in Michigan apple orchards. Appl. Environ. Microbiol. 65:48984907.
85. Sorum, H.,, M. C. Roberts, and, J. H. Crosa. 1992. Identification and cloning of a tetracycline resistance gene from the fish pathogen Vibrio salmonicida. Antimicrob. Agents Chemother. 36:611615.
86. Spratt, B. G.,, Q. Y. Zhang,, D. M. Jones,, A. Hutchison,, J. A. Brannigan, and, C. G. Dowson. 1989. Recruitment of a penicillin-binding protein gene from Neisseria flavescens during the emergence of penicillin resistance in Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 86:89888992.
87. Stokes, H. W., and, R. M. Hall. 1989. A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: integrons. Mol. Microbiol. 3:16691683.
88. Stokes, H. W.,, L. D. H. Elbourne, and, R. M. Hall. 2007. Tn1403, a multiple-antibiotic resistance transposon made up of three distinct transposons. Antimicrob. Agents Chemother. 51:18271829.
89. Summers, A. O. 2002. Generally overlooked fundamentals of bacterial genetics and ecology. Clin. Infect. Dis. 34:S85S92.
90. Thorne, P. S. 2007. Environmental health impacts of concentrated animal feeding operations: anticipating hazards—searching for solutions. Environ. Health Perspect. 115:296297.
91. Watanabe, T. 1963. Infective heredity of multiple drug resistance in bacteria. Bacteriol. Rev. 27:87115.
92. Waters, V. L. 2007. The dissemination of antibiotic resistance by bacterial conjugation, p. 285312. In R. A. Bonomo and, M. Tolmasky (ed.), Enzyme-Mediated Resistance to Antibiotics: Mechanisms, Dissemination, and Prospects for Inhibition. ASM Press, Washington, DC.
93. Webber, M. A., and, L. J. V. Piddock. 2003. The importance of efflux pumps in bacterial antibiotic resistance. J. Antimicrob. Chemother. 51:911.

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