1932

Abstract

The human food chain begins with upwards of 1,000 species of bacteria that inhabit the intestinal tracts of poultry and livestock. These intestinal denizens are responsible for the health and safety of a major protein source for humans. The use of antibiotics to treat animal diseases was followed by the surprising discovery that antibiotics enhanced food animal growth, and both led to six decades of antibiotic use that has shaped food animal management practices. Perhaps the greatest impact of antibiotic feeding in food animals has been as a selective force in the evolution of their intestinal bacteria, particularly by increasing the prevalence and diversity of antibiotic resistance genes. Future antibiotic use will likely be limited to prudent applications in both human and veterinary medicine. Improved knowledge of antibiotic effects, particularly of growth-promoting antibiotics, will help overcome the challenges of managing animal health and food safety.

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2014-09-08
2024-10-12
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Literature Cited

  1. Aarestrup FM, Kruse H, Tast E, Hammerum AM, Jensen LB. 1.  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. 6:63–70 [Google Scholar]
  2. Abreu MT. 2.  2010. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat. Rev. Immunol. 10:131–44 [Google Scholar]
  3. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J. 3.  2010. Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8:251–59 [Google Scholar]
  4. Allen HK, Levine UY, Looft T, Bandrick M, Casey TA. 4.  2013. Treatment, promotion, commotion: antibiotic alternatives in food-producing animals. Trends Microbiol. 21:114–19 [Google Scholar]
  5. Allen HK, Looft T, Bayles DO, Humphrey S, Levine UY. 5.  et al. 2011. Antibiotics in feed induce prophages in swine fecal microbiomes. mBio 2:e00260–11 [Google Scholar]
  6. Aminov RI. 6.  2009. The role of antibiotics and antibiotic resistance in nature. Environ. Microbiol. 11:2970–88 [Google Scholar]
  7. Aminov RI. 7.  2013. Biotic acts of antibiotics. Front. Microbiol. 4:241 [Google Scholar]
  8. Aminov RI, Mackie RI. 8.  2007. Evolution and ecology of antibiotic resistance genes. FEMS Microbiol. Lett. 271:147–61 [Google Scholar]
  9. Andersson DI. 9.  2003. Persistence of antibiotic resistant bacteria. Curr. Opin. Microbiol. 6:452–56 [Google Scholar]
  10. Andersson DI, Hughes D. 10.  2012. Evolution of antibiotic resistance at non-lethal drug concentrations. Drug Resist. Update 15:162–72 [Google Scholar]
  11. 11. Animal Health Inst 2012. Additives and Their Uses Bloomington, MN: The Animal Health Institute [Google Scholar]
  12. Baquero F. 12.  2001. Low-level antibacterial resistance: a gateway to clinical resistance. Drug Resist. Update 4:93–105 [Google Scholar]
  13. Barber RS, Braude R, Kon SK, Mitchell KG. 13.  1953. Antibiotics in the diet of the fattening pig. Br. J. Nutr. 7:306–19 [Google Scholar]
  14. Baron SF, Hylemon PB. 14.  1997. Biotransformation of bile acids, cholesterol, and steroid hormones. See 92 470–510
  15. Bearson BL, Allen HK, Brunelle BW, Lee IS, Casjens SR, Stanton TB. 15.  2014. The agricultural antibiotic carbadox induces phage-mediated gene transfer in Salmonella. Front. Microbiol. 552 [Google Scholar]
  16. Bearson SM, Allen HK, Bearson BL, Looft T, Brunelle BW. 16.  et al. 2013. Profiling the gastrointestinal microbiota in response to Salmonella: low versus high Salmonella shedding in the natural porcine host. Infect. Genet. Evol. 16:330–40 [Google Scholar]
  17. Boehr DD, Daigle DM, Wright GD. 17.  2004. Domain-domain interactions in the aminoglycoside antibiotic resistance enzyme AAC(6′)-APH(2′′). Biochemistry 43:9846–55 [Google Scholar]
  18. Brewer MT, Xiong N, Anderson KL, Carlson SA. 18.  2013. Effects of subtherapeutic concentrations of antimicrobials on gene acquisition events in Yersinia, Proteus, Shigella, and Salmonella recipient organisms in isolated ligated intestinal loops of swine. Am. J. Vet. Res. 74:1078–83 [Google Scholar]
  19. 19. Bristol Lab. Int 1960. Compositions for increasing efficiency of animal nurture. UK Patent No. 848925 A [Google Scholar]
  20. Brüssow H, Canchaya C, Hardt WD. 20.  2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68:560–602 [Google Scholar]
  21. Bryant MP. 21.  1959. Bacterial species of the rumen. Bacteriol. Rev. 23:125–53 [Google Scholar]
  22. Burrin D, Stoll B, Moore D. 22.  2013. Digestive physiology of the pig symposium: intestinal bile acid sensing is linked to key endocrine and metabolic signaling pathways. J. Anim. Sci. 91:1991–2000 [Google Scholar]
  23. Callaway T, Edrington TS, Anderson RC, Harvey RB, Genovese KJ. 23.  et al. 2008. Probiotics, prebiotics, and competitive exclusion for prophylaxis against bacterial disease. Anim. Health Res. Rev. 9:217–25 [Google Scholar]
  24. Callaway TR, Edrington TS, Rychlik JL, Genovese KJ, Poole TL. 24.  et al. 2003. Ionophores: their use as ruminant growth promotants and impact on food safety. Curr. Issues Intest. Microbiol. 4:43–51 [Google Scholar]
  25. Carpenter LE. 25.  1951. The effect of antibiotics and vitamin B12 on the growth of swine. Arch. Biochem. Biophys. 32:187–91 [Google Scholar]
  26. Chowdhury SR, King DE, Willing BP, Band MR, Beever JE. 26.  et al. 2007. Transcriptome profiling of the small intestinal epithelium in germfree versus conventional piglets. BMC Genomics 8:e215 [Google Scholar]
  27. Collinder E, Cardona ME, Kozakova H, Norin E, Stern S, Midtvedt T. 27.  2002. Biochemical intestinal parameters in pigs reared outdoors and indoors, and in germ-free pigs. J. Vet. Med. 49:203–9 [Google Scholar]
  28. Conway PL. 28.  1997. Development of intestinal microbiota. See 93 3–38
  29. Cotta MA, Russell JB. 29.  1997. Digestion of nitrogen in the rumen: a model for metabolism of nitrogen compounds in gastrointestinal environments. See 92 380–423
  30. Cryan JF, O’Mahony SM. 30.  2011. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol. Motil. 23:187–92 [Google Scholar]
  31. Danzeisen JL, Kim HB, Isaacson RE, Tu ZJ, Johnson TJ. 31.  2011. Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment. PLoS ONE 6:e27949 [Google Scholar]
  32. Davies J, Spiegelman GB, Yim G. 32.  2006. The world of subinhibitory antibiotic concentrations. Curr. Opin. Microbiol. 9:445–53 [Google Scholar]
  33. Derrien M, van Passel MW, van de Bovenkamp JH, Schipper RG, de Vos WM, Dekker J. 33.  2010. Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes 1:254–68 [Google Scholar]
  34. Dewhirst FE, Chien CC, Paster BJ, Ericson RL, Orcutt RP. 34.  et al. 1999. Phylogeny of the defined murine microbiota: altered Schaedler flora. Appl. Environ. Microbiol. 65:3287–92 [Google Scholar]
  35. Dibner JJ, Richards JD. 35.  2005. Antibiotic growth promoters in agriculture: history and mode of action. Poult. Sci. 84:634–43 [Google Scholar]
  36. Dumonceaux TJ, Hill JE, Hemmingsen SM, van Kessel AG. 36.  2006. Characterization of intestinal microbiota and response to dietary virginiamycin supplementation in the broiler chicken. Appl. Environ. Microbiol. 72:2815–23 [Google Scholar]
  37. Duncan SH, Richardson AJ, Kaul P, Holmes RP, Allison MJ, Stewart CS. 37.  2002. Oxalobacter formigenes and its potential role in human health. Appl. Environ. Microbiol. 68:3841–47 [Google Scholar]
  38. Dworkin J. 38.  2014. “The medium is the message”: Interspecies and interkingdom signaling by peptidoglycan and related bacterial glycans. Annu Rev. Microbiol. 68:137–54 [Google Scholar]
  39. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L. 39.  et al. 2005. Diversity of the human intestinal microbial flora. Science 308:1635–38 [Google Scholar]
  40. Elliott SD, Barnes EM. 40.  1959. Changes in serological type and antibiotic resistance of Lancefield group D streptococci in chickens receiving dietary chlortetracycline. J. Gen. Microbiol. 20:426–33 [Google Scholar]
  41. Engberg RM, Hedemann MS, Leser TD, Jensen BB. 41.  2000. Effect of zinc bacitracin and salinomycin on intestinal microflora and performance of broilers. Poult. Sci. 79:1311–19 [Google Scholar]
  42. Feighner SD, Dashkevicz MP. 42.  1987. Subtherapeutic levels of antibiotics in poultry feeds and their effects on weight gain, feed efficiency, and bacterial cholyltaurine hydrolase activity. Appl. Environ. Microbiol. 53:331–36 [Google Scholar]
  43. Feld L, Schjorring S, Hammer K, Licht TR, Danielsen M. 43.  et al. 2008. Selective pressure affects transfer and establishment of a Lactobacillus plantarum resistance plasmid in the gastrointestinal environment. J. Antimicrob. Chemother. 61:845–52 [Google Scholar]
  44. 44. Food Drug Admin 2012. Guidance for Industry: The Judicious Use of Medically Important Antimicrobial Drugs in Food-Producing Animals Washington, DC: U.S. Food Drug Admin. [Google Scholar]
  45. Forsberg CW, Cheng K-J, White BA. 45.  1997. Polysaccharide degradation in the rumen and large intestine. See 92 319–79
  46. Frye JG, Jackson CR. 46.  2013. Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from U.S. food animals. Front. Microbiol. 4:e135 [Google Scholar]
  47. Fuller R, Newland LGM, Briggs CAE, Braude R, Mitchell KG. 47.  1960. The normal intestinal flora of the pig. IV. The effect of dietary supplements of penicillin, chlortetracycline or copper sulphate on the faecal flora. J. Appl. Bacteriol. 23:195–205 [Google Scholar]
  48. Gaskins HR, Collier CT, Anderson DB. 48.  2002. Antibiotics as growth promotants: mode of action. Anim. Biotechnol. 13:29–42 [Google Scholar]
  49. Gaskins HR, Croix JA, Nakamura N, Nava GM. 49.  2008. Impact of the intestinal microbiota on the development of mucosal defense. Clin. Infect. Dis. 46:Suppl. 2S80–86 discussion S144–51 [Google Scholar]
  50. Gaze WH, Krone SM, Larsson DG, Li XZ, Robinson JA. 50.  et al. 2013. Influence of humans on evolution and mobilization of environmental antibiotic resistome. Emerg. Infect. Dis. 19:e120871 [Google Scholar]
  51. Goh EB, Yim G, Tsui W, McClure J, Surette MG, Davies J. 51.  2002. Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proc. Natl. Acad. Sci. USA 99:17025–30 [Google Scholar]
  52. Gong J, Forster RJ, Yu H, Chambers JR, Sabour PM. 52.  et al. 2002. Diversity and phylogenetic analysis of bacteria in the mucosa of chicken ceca and comparison with bacteria in the cecal lumen. FEMS Microbiol. Lett. 208:1–7 [Google Scholar]
  53. Gong J, Forster RJ, Yu H, Chambers JR, Wheatcroft R. 53.  et al. 2002. Molecular analysis of bacterial populations in the ileum of broiler chickens and comparison with bacteria in the cecum. FEMS Microbiol. Ecol. 41:171–79 [Google Scholar]
  54. Grenham S, Clarke G, Cryan JF, Dinan TG. 54.  2011. Brain-gut-microbe communication in health and disease. Front. Physiol. 2:94 [Google Scholar]
  55. Gustafson RH, Bowen RE. 55.  1997. Antibiotic use in animal agriculture. J. Appl. Microbiol. 83:531–41 [Google Scholar]
  56. Gustafsson A, Berstad A, Lund-Tonnesen S, Midtvedt T, Norin E. 56.  1999. The effect of faecal enema on five microflora-associated characteristics in patients with antibiotic-associated diarrhoea. Scand. J. Gastroenterol. 34:580–86 [Google Scholar]
  57. Hammond AC. 57.  1995. Leucaena toxicosis and its control in ruminants. J. Anim. Sci. 73:1487–92 [Google Scholar]
  58. Harvey MJ. 58.  1965. Animal feed composition and method of using same. US Patent No. 3185573 A [Google Scholar]
  59. Holdeman LV, Moore WEC. 59.  1975. Anaerobe Laboratory Manual Blacksburg, VA: Anaerobe Lab. Virginia Polytech. Inst. State Univ. [Google Scholar]
  60. Hooper LV. 60.  2004. Bacterial contributions to mammalian gut development. Trends Microbiol. 12:129–34 [Google Scholar]
  61. Hooper LV, Midtvedt T, Gordon JI. 61.  2002. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu. Rev. Nutr. 22:283–307 [Google Scholar]
  62. Hughes VM, Datta N. 62.  1983. Conjugative plasmids in bacteria of the ‘pre-antibiotic’ era. Nature 302:725–26 [Google Scholar]
  63. Hume ID. 63.  1997. Fermentation in the hindgut of mammals. See 92 84–115
  64. Hungate RE. 64.  1966. The Rumen and Its Microbes New York: Academic [Google Scholar]
  65. Isaacson R, Kim HB. 65.  2012. The intestinal microbiome of the pig. Anim. Health Res. Rev. 13:100–9 [Google Scholar]
  66. Jindal A, Kocherginskaya S, Mehboob A, Robert M, Mackie RI. 66.  et al. 2006. Antimicrobial use and resistance in swine waste treatment systems. Appl. Environ. Microbiol. 72:7813–20 [Google Scholar]
  67. Johansen CH, Bjerrum L, Pedersen K. 67.  2007. Impact of salinomycin on the intestinal microflora of broiler chickens. Acta Vet. Scand. 49:e30 [Google Scholar]
  68. Jørgensen KM, Wassermann T, Jensen , Hengzuang W, Molin S. 68.  et al. 2013. Sublethal ciprofloxacin treatment leads to rapid development of high-level ciprofloxacin resistance during long-term experimental evolution of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 57:4215–21 [Google Scholar]
  69. Jukes TH. 69.  1952. Animal and poultry feed containing aureomycin mash. US Patent No. 2619420 [Google Scholar]
  70. Jukes TH. 70.  1977. The history of the “antibiotic growth effect”. Fed. Proc. 36:2514–18 [Google Scholar]
  71. Keeney KM, Yurist-Doutsch S, Arrieta MC, Finlay BB. 71.  2014. Effects of antibiotics on human microbiota and subsequent disease. Annu Rev. Microbiol. 68217–35 [Google Scholar]
  72. Kien CL, Blauwiekel R, Bunn JY, Jetton TL, Frankel WL, Holst JJ. 72.  2007. Cecal infusion of butyrate increases intestinal cell proliferation in piglets. J. Nutr. 137:916–22 [Google Scholar]
  73. Kim HB, Borewicz K, White BA, Singer RS, Sreevatsan S. 73.  et al. 2012. Microbial shifts in the swine distal gut in response to the treatment with antimicrobial growth promoter, tylosin. Proc. Natl. Acad. Sci. USA 109:15485–90 [Google Scholar]
  74. Knapp CW, Dolfing J, Ehlert PA, Graham DW. 74.  2010. Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ. Sci. Technol. 44:580–87 [Google Scholar]
  75. Knarreborg A, Simon MA, Engberg RM, Jensen BB, Tannock GW. 75.  2002. Effects of dietary fat source and subtherapeutic levels of antibiotic on the bacterial community in the ileum of broiler chickens at various ages. Appl. Environ. Microbiol. 68:5918–24 [Google Scholar]
  76. Kohanski MA, DePristo MA, Collins JJ. 76.  2010. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol. Cell 37:311–20 [Google Scholar]
  77. Kohler B, Karch H, Schmidt H. 77.  2000. Antibacterials that are used as growth promoters in animal husbandry can affect the release of Shiga-toxin-2-converting bacteriophages and Shiga toxin 2 from Escherichia coli strains. Microbiology 146:1085–90 [Google Scholar]
  78. Krause DO, Nagaraja TG, Wright AD, Callaway TR. 78.  2013. Board-invited review: rumen microbiology; leading the way in microbial ecology. J. Anim. Sci. 91:331–41 [Google Scholar]
  79. Lagier JC, Armougom F, Million M, Hugon P, Pagnier I. 79.  et al. 2012. Microbial culturomics: paradigm shift in the human gut microbiome study. Clin. Microbiol. Infect. 18:1185–93 [Google Scholar]
  80. Lamendella R, Domingo JW, Ghosh S, Martinson J, Oerther DB. 80.  2011. Comparative fecal metagenomics unveils unique functional capacity of the swine gut. BMC Microbiol. 11:e103 [Google Scholar]
  81. Lawley TD, Bouley DM, Hoy YE, Gerke C, Relman DA, Monack DM. 81.  2008. Host transmission of Salmonella enterica serovar Typhimurium is controlled by virulence factors and indigenous intestinal microbiota. Infect. Immun. 76:403–16 [Google Scholar]
  82. Levine UY, Looft T, Allen HK, Stanton TB. 82.  2013. Butyrate-producing bacteria, including mucin degraders, from the swine intestinal tract. Appl. Environ. Microbiol. 79:3879–81 [Google Scholar]
  83. Levy SB, Marshall B. 83.  2004. Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med. 10:S122–29 [Google Scholar]
  84. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR. 84.  et al. 2008. Evolution of mammals and their gut microbes. Science 320:1647–51 [Google Scholar]
  85. Ley RE, Peterson DA, Gordon JI. 85.  2006. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–48 [Google Scholar]
  86. Linares JF, Gustafsson I, Baquero F, Martinez JL. 86.  2006. Antibiotics as intermicrobial signaling agents instead of weapons. Proc. Natl. Acad. Sci. USA 103:19484–89 [Google Scholar]
  87. Looft T, Allen HK, Cantarel BL, Levine UY, Bayles DO, Alt DP. 87.  2014. Bacteria, phages, and pigs: the effects of in-feed antibiotics on the microbiome at different gut locations. ISME J. 81566–76 [Google Scholar]
  88. Looft T, Johnson TA, Allen HK, Bayles DO, Alt DP. 88.  et al. 2012. In-feed antibiotic effects on the swine intestinal microbiome. Proc. Natl. Acad. Sci. USA 109:1691–96 [Google Scholar]
  89. Looft T, Levine UY, Stanton TB. 89.  2013. Cloacibacillus porcorum sp. nov., a mucin-degrading bacterium from the swine intestinal tract and emended description of the genus Cloacibacillus. Int. J. Syst. Evol. Microbiol. 63:1960–66 [Google Scholar]
  90. Louis P, Flint HJ. 90.  2009. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol. Lett. 294:1–8 [Google Scholar]
  91. Luecke RW, Thorp F Jr, Newland HW, McMillen WN. 91.  1951. The growth promoting effects of various antibiotics on pigs. J. Anim. Sci. 10:538–42 [Google Scholar]
  92. Mackie RI, White BA. 92.  1997. Gastrointestinal Microbiology 1 Gastrointestinal Ecosystems and Fermentations New York: Chapman & Hall [Google Scholar]
  93. Mackie RI, White BA, Isaacson RE. 93.  1997. Gastrointestinal Microbiology 2 Gastrointestinal Microbes and Host Interactions New York: Chapman & Hall [Google Scholar]
  94. Mahowald MA, Rey FE, Seedorf H, Turnbaugh PJ, Fulton RS. 94.  et al. 2009. Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc. Natl. Acad. Sci. USA 106:5859–64 [Google Scholar]
  95. Martinez JL. 95.  2012. Natural antibiotic resistance and contamination by antibiotic resistance determinants: the two ages in the evolution of resistance to antimicrobials. Front. Microbiol. 3:e1 [Google Scholar]
  96. Maurice CF, Haiser HJ, Turnbaugh PJ. 96.  2013. Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell 152:39–50 [Google Scholar]
  97. McFall-Ngai MJ. 97.  2014. The importance of microbes in animal development: lessons from the squid-vibrio symbiosis. Annu. Rev. Microbiol. 68:177–94 [Google Scholar]
  98. McFall-Ngai MJ, Hadfield MG, Bosch TC, Carey HV, Domazet-Loso T. 98.  et al. 2013. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 110:3229–36 [Google Scholar]
  99. Meessen-Pinard M, Sekulovic O, Fortier LC. 99.  2012. Evidence of in vivo prophage induction during Clostridium difficile infection. Appl. Environ. Microbiol. 78:7662–70 [Google Scholar]
  100. Midtvedt T. 100.  1989. Monitoring the functional state of the microflora. Recent Advances in Microbial Ecology T Hattori 515–19 Tokyo: Japan Sci. Soc. [Google Scholar]
  101. Midtvedt T, Lingaas E, Carlstedt-Duke B, Hoverstad T, Midtvedt AC. 101.  et al. 1990. Intestinal microbial conversion of cholesterol to coprostanol in man: influence of antibiotics. Acta Patholog. Microbiol. Immunol. Scand. 98:839–44 [Google Scholar]
  102. Modi SR, Lee HH, Spina CS, Collins JJ. 102.  2013. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499:219–22 [Google Scholar]
  103. Moore PR, Evenson A. 103.  et al. 1946. Use of Sulfasuxidine, streptothricin, and streptomycin in nutritional studies with the chick. J. Biol. Chem. 165:437–41 [Google Scholar]
  104. Nandi S, Maurer JJ, Hofacre C, Summers AO. 104.  2004. Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter. Proc. Natl. Acad. Sci. USA 101:7118–22 [Google Scholar]
  105. Niewold TA. 105.  2007. The nonantibiotic anti-inflammatory effect of antimicrobial growth promoters, the real mode of action? A hypothesis. Poult. Sci. 86:605–9 [Google Scholar]
  106. Norin KE. 106.  1997. Influence of antibiotics on some intestinal microflora associated characteristics. Anaerobe 3:145–48 [Google Scholar]
  107. Olsen GJ, Overbeek R, Larsen N, Marsh TL, McCaughey MJ. 107.  et al. 1992. The Ribosomal Database Project. Nucleic Acids Res. 20:Suppl.2199–200 [Google Scholar]
  108. Ott WH. 108.  1956. Penicillin in feed. US Patent No. 2753266 A [Google Scholar]
  109. Owens C, Broussard E, Surawicz C. 109.  2013. Fecal microbiota transplantation and donor standardization. Trends Microbiol. 21:443–45 [Google Scholar]
  110. Pabst R, Rothkotter HJ. 110.  1999. Postnatal development of lymphocyte subsets in different compartments of the small intestine of piglets. Vet. Immunol. Immunopathol. 72:167–73 [Google Scholar]
  111. Pasquale TR, Tan JS. 111.  2005. Nonantimicrobial effects of antibacterial agents. Clin. Infect. Dis. 40:127–35 [Google Scholar]
  112. Paterson DL. 112.  2004. “Collateral damage” from cephalosporin or quinolone antibiotic therapy. Clin. Infect. Dis. 38:Suppl. 4S341–45 [Google Scholar]
  113. Pérez-Cobas AE, Gosalbes MJ, Friedrichs A, Knecht H, Artacho A. 113.  et al. 2012. Gut microbiota disturbance during antibiotic therapy: a multi-omic approach. Gut 62:1591–601 [Google Scholar]
  114. Perron GG, Bell G, Quessy S. 114.  2008. Parallel evolution of multidrug-resistance in Salmonella enterica isolated from swine. FEMS Microbiol. Lett. 281:17–22 [Google Scholar]
  115. Perry JA, Wright GD. 115.  2013. The antibiotic resistance “mobilome”: searching for the link between environment and clinic. Front. Microbiol. 4:e138 [Google Scholar]
  116. 116. Pfizer 1954. Improvements in or relating to animal feed compositions. UK Patent No. 709348 A [Google Scholar]
  117. 117. Pfizer 1970. Animal feed composition. UK Patent No. 1180143 A [Google Scholar]
  118. Poppe C, Martin LC, Gyles CL, Reid-Smith R, Boerlin P. 118.  et al. 2005. Acquisition of resistance to extended-spectrum cephalosporins by Salmonella enterica subsp. enterica serovar Newport and Escherichia coli in the turkey poult intestinal tract. Appl. Environ. Microbiol. 71:1184–92 [Google Scholar]
  119. Pruden A. 119.  2013. Balancing water sustainability and public health goals in the face of growing concerns about antibiotic resistance. Environ. Sci. Technol. 48:5–14 [Google Scholar]
  120. Que JU, Casey SW, Hentges DJ. 120.  1986. Factors responsible for increased susceptibility of mice to intestinal colonization after treatment with streptomycin. Infect. Immun. 53:116–23 [Google Scholar]
  121. Que JU, Hentges DJ. 121.  1985. Effect of streptomycin administration on colonization resistance to Salmonella typhimurium in mice. Infect. Immun. 48:169–74 [Google Scholar]
  122. Rappe MS, Giovannoni SJ. 122.  2003. The uncultured microbial majority. Annu. Rev. Microbiol. 57:369–94 [Google Scholar]
  123. Raun A. 123.  1974. Antibiotics monensin and a204 for improving ruminant feed efficiency. US Patent No. 3839557 A [Google Scholar]
  124. Reeves AE, Koenigsknecht MJ, Bergin IL, Young VB. 124.  2012. Suppression of Clostridium difficile in the gastrointestinal tracts of germfree mice inoculated with a murine isolate from the family Lachnospiraceae. Infect. Immun. 80:3786–94 [Google Scholar]
  125. Rettedal E, Vilain S, Lindblom S, Lehnert K, Scofield C. 125.  et al. 2009. Alteration of the ileal microbiota of weanling piglets by the growth-promoting antibiotic chlortetracycline. Appl. Environ. Microbiol. 75:5489–95 [Google Scholar]
  126. Rhone Poulenc. 126.  1961. Compositions for the nutrition of animals. UK Patent No. 871285 A [Google Scholar]
  127. Rohlke F, Stollman N. 127.  2012. Fecal microbiota transplantation in relapsing Clostridium difficile infection. Therap. Adv. Gastroenterol. 5:403–20 [Google Scholar]
  128. Rubin TA, Gessert CE, Aas J, Bakken JS. 128.  2013. Fecal microbiome transplantation for recurrent Clostridium difficile infection: report on a case series. Anaerobe 19:22–26 [Google Scholar]
  129. Russell JB, Houlihan AJ. 129.  2003. Ionophore resistance of ruminal bacteria and its potential impact on human health. FEMS Microbiol. Rev. 27:65–74 [Google Scholar]
  130. Salyers A, Shoemaker N, Bonheyo G, Frias J. 130.  1999. Conjugative transposons: transmissible resistance islands. Pathogenicity Islands and Other Mobile Elements JB Kaper, J Hacker 331–46 Washington, DC: Am. Soc. Microbiol. [Google Scholar]
  131. Salyers AA, Amabile-Cuevas CF. 131.  1997. Why are antibiotic resistance genes so resistant to elimination?. Antimicrob. Agents Chemother. 41:2321–25 [Google Scholar]
  132. Savage DC. 132.  1977. Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol. 31:107–33 [Google Scholar]
  133. Schaedler RW, Dubs R, Costello R. 133.  1965. Association of germfree mice with bacteria isolated from normal mice. J. Exp. Med. 122:77–82 [Google Scholar]
  134. Shirkey TW, Siggers RH, Goldade BG, Marshall JK, Drew MD. 134.  et al. 2006. Effects of commensal bacteria on intestinal morphology and expression of proinflammatory cytokines in the gnotobiotic pig. Exp. Biol. Med. 231:1333–45 [Google Scholar]
  135. Shryock TR, Page SW. 135.  2006. Growth promotion uses of antimicrobial agents. Antimicrobial Therapies in Veterinary Medicine S Giguere, JF Prescott, JD Baggott, RD Walker, PM Dowling 389–404 Ames, IA: Blackwell [Google Scholar]
  136. Smith HW. 136.  1970. Effect of antibiotics on bacterial ecology in animals. Am. J. Clin. Nutr. 23:1472–79 [Google Scholar]
  137. Song B, Wang GR, Shoemaker NB, Salyers AA. 137.  2009. An unexpected effect of tetracycline concentration: growth phase-associated excision of the Bacteroides mobilizable transposon NBU1. J. Bacteriol. 191:1078–82 [Google Scholar]
  138. Stanton TB. 138.  2013. A call for antibiotic alternatives research. Trends Microbiol. 21:111–13 [Google Scholar]
  139. Stanton TB, Humphrey SB. 139.  2011. Persistence of antibiotic resistance: evaluation of a probiotic approach using antibiotic-sensitive Megasphaera elsdenii strains to prevent colonization of swine by antibiotic-resistant strains. Appl. Environ. Microbiol. 77:7158–66 [Google Scholar]
  140. Stanton TB, Humphrey SB, Scott KP, Flint HJ. 140.  2005. Hybrid tet genes and tet gene nomenclature: request for opinion. Antimicrob. Agents Chemother. 49:1265–66 [Google Scholar]
  141. Stanton TB, Humphrey SB, Sharma VK, Zuerner RL. 141.  2008. Collateral effects of antibiotics: carbadox and metronidazole induce VSH-1 and facilitate gene transfer among Brachyspira hyodysenteriae strains. Appl. Environ. Microbiol. 74:2950–56 [Google Scholar]
  142. Stanton TB, Humphrey SB, Stoffregen WC. 142.  2011. Chlortetracycline-resistant intestinal bacteria in organically-raised and feral swine. Appl. Environ. Microbiol. 77:7167–70 [Google Scholar]
  143. Stecher B, Hardt WD. 143.  2011. Mechanisms controlling pathogen colonization of the gut. Curr. Opin. Microbiol. 14:82–91 [Google Scholar]
  144. Stecher B, Robbiani R, Walker AW, Westendorf AM, Barthel M. 144.  et al. 2007. Salmonella enterica serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 5:2177–89 [Google Scholar]
  145. Sunkara LT, Achanta M, Schreiber NB, Bommineni YR, Dai G. 145.  et al. 2011. Butyrate enhances disease resistance of chickens by inducing antimicrobial host defense peptide gene expression. PLoS ONE 6:e27225 [Google Scholar]
  146. Tadesse DA, Zhao S, Tong E, Ayers S, Singh A. 146.  et al. 2012. Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950–2002. Emerg. Infect. Dis. 18:741–49 [Google Scholar]
  147. Tannock GW. 147.  1997. Modification of the normal microbiota by diet, stress, antimicrobial agents, and probiotics. See 93 434–65 [Google Scholar]
  148. Taschuk R, Griebel PJ. 148.  2012. Commensal microbiome effects on mucosal immune system development in the ruminant gastrointestinal tract. Anim. Health Res. Rev. 13:129–41 [Google Scholar]
  149. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. 149.  2007. The human microbiome project. Nature 449:804–10 [Google Scholar]
  150. Ubeda C, Pamer EG. 150.  2012. Antibiotics, microbiota, and immune defense. Trends Immunol. 33:459–66 [Google Scholar]
  151. van Hoek AHAM, Mayrhofer S, Domig KJ, Florez AB, Ammor MS. 151.  et al. 2008. Mosaic tetracycline resistance genes and their flanking regions in Bifidobacterium thermophilum and Lactobacillus johnsonii. Antimicrob. Agents Chemother. 52:248–52 [Google Scholar]
  152. Verhue WM. 152.  1978. Interaction of bacteriophage infection and low penicillin concentrations on the performance of yogurt cultures. Appl. Environ. Microbiol. 35:1145–49 [Google Scholar]
  153. Visek WJ. 153.  1978. The mode of growth promotion by antibiotic. J. Anim. Sci. 46:1447–69 [Google Scholar]
  154. Vispo C, Karasov WH. 154.  1997. The interaction of avian gut microbes and their host: an elusive symbiosis. See 92 116–55
  155. Wallace RJ. 155.  1994. Ruminal microbiology, biotechnology, and ruminant nutrition: progress and problems. J. Anim. Sci. 72:2992–3003 [Google Scholar]
  156. White BA, Lamed R, Bayer EA, Flint HJ. 156.  2014. Biomass utilization by gut microbiomes. Annu. Rev. Microbiol. 68279–96 [Google Scholar]
  157. Wiedenbeck J, Cohan FM. 157.  2011. Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol. Rev. 35:957–76 [Google Scholar]
  158. Willing BP, Russell SL, Finlay BB. 158.  2011. Shifting the balance: antibiotic effects on host-microbiota mutualism. Nat. Rev. Microbiol. 9:233–43 [Google Scholar]
  159. Wlodarska M, Finlay BB. 159.  2010. Host immune response to antibiotic perturbation of the microbiota. Mucosal Immunol. 3:100–3 [Google Scholar]
  160. 160. World Health Organ 2012. Critically important antimicrobials for human medicine Geneva: World Health Organ. [Google Scholar]
  161. Wozniak RA, Waldor MK. 161.  2010. Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat. Rev. Microbiol. 8:552–63 [Google Scholar]
  162. Yeoman CJ, Chia N, Jeraldo P, Sipos M, Goldenfeld ND, White BA. 162.  2012. The microbiome of the chicken gastrointestinal tract. Anim. Health Res. Rev. 13:89–99 [Google Scholar]
  163. Yim G, McClure J, Surette MG, Davies JE. 163.  2011. Modulation of Salmonella gene expression by subinhibitory concentrations of quinolones. J. Antibiot. (Tokyo) 64:73–78 [Google Scholar]
  164. Zoetendal EG, Raes J, van den Bogert B, Arumugam M, Booijink CC. 164.  et al. 2012. The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J. 6:1415–26 [Google Scholar]
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