Skip to main content
Log in

Antibiotic Usage in Animals

Impact on Bacterial Resistance and Public Health

  • Leading Article
  • Published:
Drugs Aims and scope Submit manuscript

Abstract

Antibiotic use whether for therapy or prevention of bacterial diseases, or as performance enhancers will result in antibiotic resistant micro-organisms, not only among pathogens but also among bacteria of the endogenous microflora of animals. The extent to which antibiotic use in animals will contribute to the antibiotic resistance in humans is still under much debate. In addition to the veterinary use of antibiotics, the use of these agents as antimicrobial growth promoters (AGP) greatly influences the prevalence of resistance in animal bacteria and a poses risk factor for the emergence of antibiotic resistance in human pathogens. Antibiotic resistant bacteria such as Escherichia coli, Salmonella spp., Campylobacter spp. and enterococci from animals can colonise or infect the human population via contact (occupational exposure) or via the food chain. Moreover, resistance genes can be transferred from bacteria of animals to human pathogens in the intestinal flora of humans.

In humans, the control of resistance is based on hygienic measures: prevention of cross contamination and a decrease in the usage of antibiotics. In food animals housed closely together, hygienic measures, such as prevention of oral-faecal contact, are not feasible. Therefore, diminishing the need for antibiotics is the only possible way of controlling resistance in large groups of animals. This can be achieved by improvement of animal husbandry systems, feed composition and eradication of or vaccination against infectious diseases. Moreover, abolishing the use of antibiotics as feed additives for growth promotion in animals bred as a food source for humans would decrease the use of antibiotics in animals on a worldwide scale by nearly 50%. This would not only diminish the public health risk of dissemination of resistant bacteria or resistant genes from animals to humans, but would also be of major importance in maintaining the efficacy of antibiotics in veterinary medicine.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Murray BE. New aspects of antimicrobial resistance and the resulting therapeutic dilemmas. J Infect Dis 1991; 163(6): 1184–94

    Article  PubMed  CAS  Google Scholar 

  2. Neu HC. The crisis in antibiotic resistance. Science 1992; 257(5073): 1064–73

    Article  PubMed  CAS  Google Scholar 

  3. Wise R, Hart T, Cars O, et al. Antimicrobial resistance is a major threat to public health. BMJ 1998; 317: 609–10

    Article  PubMed  CAS  Google Scholar 

  4. Murray BE. Problems and dilemmas of antimicrobial resistance. Pharmacotherapy 1992; 12: 86s-93s

    Google Scholar 

  5. Murray BE. Can antibiotic resistance be controlled? N Engl J Med 1994; 330(17): 1229–30

    Article  PubMed  CAS  Google Scholar 

  6. De Craene A, Viaene J. Economics effects of technology in agriculture. Do performance enhancers for animals benefit consumers? Report University of Gent, Belgium, Faculty of Agricultural Sciences, Department of Agro-Marketing 1992; 162

  7. Rosen GD. Antibacterials in poultry and pig nutrition. In: Wallace RJ, Chesson A, editors. Biotechnology in animal feeds and feeding. Weinheim: VCH Verlagsgesellschaft mbH, 1995; 47: 143–72

    Article  Google Scholar 

  8. CEAS. The impact of animal husbandry in the European Community of the use of growth promoters in animal feeds. Brussels E.C., 1991 Feb; 1,2: 319

    Google Scholar 

  9. Thomke S, Elwinger K. Growth promotants in feeding pigs and poultry. II. Mode of action of antibiotic growth promotants. Ann Zootech 1998; 47(3): 153–67

    Article  CAS  Google Scholar 

  10. Forbes M, Park JY. Growth of germ-free and conventional chicks: effect of diet, dietary penicillin and bacterial environment. J Nutr 1959; 69: 78–84

    Google Scholar 

  11. Frost AJ. In:Woolcock JB, editor. Microbiology of animals and animal products. Antibiotics and animal production. Amsterdam: Elsevier, 1997: 181–94

    Google Scholar 

  12. Thomke S, Elwinger K. Growth promoters in feeding pigs and poultry. III. Alternatives to antibiotic growth promoters. Ann Zootech 1998; 47(4): 245–71

    Article  CAS  Google Scholar 

  13. Jukes TH. The history of the ‘antibiotic growth effect’. Fed Proc 1977; 36(11): 2514–8

    PubMed  CAS  Google Scholar 

  14. Jukes TH. The present status and background of antibiotics in the feeding of domestic animals. Ann N Y Acad Sci 1971; 182: 362–79

    Article  PubMed  CAS  Google Scholar 

  15. Prescott JF, Baggot JD. Antimicrobial therapy in veterinary medicine. Ames, Iowa State University Press: 1993

  16. Devriese LA, Daube G, Hommez J, et al. In vitro susceptibility of Clostridium perfringens isolated from farm animals to growth-enhancing antibiotics. J Appl Bacteriol 1993; 75(1): 55–7

    Article  PubMed  CAS  Google Scholar 

  17. Dutta GN, Devriese LA. Susceptibility of fecal streptococci of poultry origin to nine growth-promoting agents. Appl Environ Microbiol 1982; 44(4): 832–7

    PubMed  CAS  Google Scholar 

  18. SOU. Antimicrobial Feed Additives. Report from the commission on antimicrobial feed additives. Stockholm, 1997: 132

  19. Aarestrup FM, Bager F, Jensen NE, et al. Surveillance of antimicrobial resistance in bacteria isolated from food animals to antimicrobial growth promoters and related therapeutic agents in Denmark. APMIS 1998; 106: 606–22

    Article  PubMed  CAS  Google Scholar 

  20. Wierup M. Preventive methods replace antibiotic growth promoters: ten years experience from Sweden. APUA Newsletter 1998; 16: 1–4

    Google Scholar 

  21. van den Bogaard AE, London N, Driessen C, et al. The effect of antimicrobial growth promoters on the resistance in faecal indicator bacteria of pigs [abstract]. Proceedings of the 38th Interscience Conference on Antimicrobial Agents and Chemotherapy; 1998 Sep 24–7; San Diego: 1998; C-077

  22. Witte W. Impact of antibiotic use in animal feeding on resistance of bacterial pathogens in humans. In: Proceedings of: Antibiotic resistance, origins, evolution, selection and spread. Ciba Found Symp 1997; 207: 61–71

  23. Swann MM. Joint Committee on the use of antibiotics in animal husbandry and veterinary medicine. London: Her Majesty’s Stationary Office, 1969

    Google Scholar 

  24. van den Bogaard AE, Stobberingh EE. Time to ban all antibiotics as animal growth-promoting agents? [letter]. Lancet 1996; 348(9027): 619, 1454–6

    PubMed  Google Scholar 

  25. Chopra I, Hodgson J, Metcalf B, et al. The search for antimicrobial agents effective against bacteria resistant to multiple antibiotics. Antimicrob Agents Chemother 1997; 41(3): 497–503

    PubMed  CAS  Google Scholar 

  26. Jones RN, Marshall SA, Erwin ME. Antimicrobial activity and spectrum of SCH27899 (Ziracin®) tested against Gram-positive species including recommendations for routine susceptibility testing methods and quality control. Diagn Microbiol Infect Dis 1999; 34: 103–10

    Article  PubMed  CAS  Google Scholar 

  27. Cook RR. Antimicrobial resistance-use in veterinary and human medicine. J Antimicrob Chemother 1997; 39(3): 435

    Article  PubMed  CAS  Google Scholar 

  28. van den Bogaard AE. Antimicrobial resistance — relation to human and animal exposure to antibiotics [letter]. J Antimicrob Chemother 1997; 40(3): 453–4

    Article  PubMed  Google Scholar 

  29. de Neeling AJ, van Klingeren B, Harteloh PPM. Het gebruik van antibiotica en het optreden van resistentie. Volks-gezondheid Toekomst Verkenning, 1995–2010. RIVM 1993: 658–62

  30. Emersen AM. Control of the spread of resistance. In: Greenwood D, editor. Antimicrobial chemotherapy. Oxford: Oxford University Press, 1995

    Google Scholar 

  31. Miller DJS. Present state and heads in the use of veterinary drugs. In: Proceedings of Euroresidue II conference, Veldhoven, The Netherlands; 1993 May 3–5

  32. Prescott JF. Antibiotics: Miracle drugs or pig food? Can Vet J 1997; 38(12): 763–6

    PubMed  CAS  Google Scholar 

  33. Levy SB. Multidrug resistance — a sign of the times. N Engl J Med 1998; 338(19): 1376–8

    Article  PubMed  CAS  Google Scholar 

  34. DANMAP, 1995. Consumption of antimicrobial agents and occurence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. 1997; DANMAP No. 1

  35. Reynolds P. Glycopeptide antibiotics: pharmacokinetics, spectrum of activity, resistance patterns. Hosp Formulary 1990; 25: 537–44

    CAS  Google Scholar 

  36. Arthur M, Courvalin P. Genetics and mechanisms of glycopeptide resistance in enterococci. Antimicrob Agents Chemother 1993; 37(8): 1563–71

    Article  PubMed  CAS  Google Scholar 

  37. Arthur M, Reynolds P, Courvalin P. Glycopeptide resistance in enterococci. Trends Microbiol 1996; 4(10): 401–7

    Article  PubMed  CAS  Google Scholar 

  38. Leclercq R, Derlot E, Weber M, et al. Transferable vancomycin and teicoplanin resistance in Enterococcus faecium. Antimicrob Agents Chemother 1989; 33(1): 10–5

    Article  PubMed  CAS  Google Scholar 

  39. Quintiliani Jr R, Courvalin P. Conjugal transfer of the vancomycin resistance determinant vanB between enterococci involves the movement of large genetic elements from chromosome to chromosome. FEMS Microbiol Lett 1994; 119(3): 359–63

    Article  PubMed  CAS  Google Scholar 

  40. Quintiliani Jr R, Courvalin P. Characterization of Tnl547, a composite transposon flanked by the IS16 and IS256-like elements, that confers vancomycin resistance in Enterococcus faecalis BM 4281. Gene 1996; 172(1): 1–8

    Article  PubMed  CAS  Google Scholar 

  41. Woodford N, Jones BL, Baccus Z, et al. Linkage of vancomycin and high-level gentamicin resistance genes on the same plasmid in a clinical isolate of Enterococcus faecalis. J Antimicrob Chemother 1995; 35(1): 179–84

    Article  PubMed  CAS  Google Scholar 

  42. Noble WC, Virani Z, Cree RG. Co-transfer of vancomycin and other resistance genes from Enterococcus faecalis NCTC 12201 to Staphylococcus aureus. FEMS Microbiol Lett 1992; 72(2): 195–8

    Article  PubMed  CAS  Google Scholar 

  43. Devriese LA, Ieven M, Grossens H, et al. Presence of vanco-mycin-resistant enterococci in farm and pet animals. Antimicrob Agents Chemother 1996; 40(10): 2285–7

    PubMed  CAS  Google Scholar 

  44. Bates J, Jordens JZ, Griffiths DT. Farm animals as a putative reservoir for vancomycin-resistant enterococcal infection in man. J Antimicrob Chemother 1994; 34(4): 507–14

    Article  PubMed  CAS  Google Scholar 

  45. Klare I, Heier H, Claus H, et al. VanA-mediated high-level glycopeptide resistance in Enterococcus faecium.from animal husbandry. FEMS Microbiol Lett 1995; 125(2–3): 165–71

    Article  PubMed  CAS  Google Scholar 

  46. Coque TM, Tomako JF, Ricke SC, et al. Vancomycin-resistant enterococci from nosocomial, community, and animal sources in the United States. Antimicrob Agents Chemother 1996; 40(11): 2605–9

    PubMed  Google Scholar 

  47. Greko C, Lindblad J. Vancomycin sensitivity of enterococci from Swedish poultry and pigs. Proceedings of Symposium Food Associated Pathogens; 1996 May 6–8; Department of Food Hygiene, SLU, Uppsala, Sweden

  48. Patel R, Uhl JR, Kohner P, et al. Multiplex PCR detection of vanA, vanB, vanC-1, and vanC-2/3 genes in enterococci. J Clin Microbiol 1997; 35(3): 703–7

    PubMed  CAS  Google Scholar 

  49. Woodford N. Glycopeptide-resistant enterococci: a decade of experience. J Med Microbiol 1998; 47: 849–62

    Article  PubMed  CAS  Google Scholar 

  50. Cormican MG, Johnson DM, Jones RN. Activity of the quinupristin-dalfopristin combination (RP-59500; Synercid) tested against vancomycin-resistant Enterococcus species. Diagn Microbiol Infect Dis 1996; 24(1): 59–60

    Article  PubMed  CAS  Google Scholar 

  51. Putnam SD, Jones RN, Johnson DM, et al. In vitro antimicrobial activity and MIC quality control guidelines of RPR 106972 (RPR 112808/RPR106950): a novel orally administered streptogramin combination. Diagn Microbiol Infect Dis 1997; 28(3): 139–47

    Article  PubMed  CAS  Google Scholar 

  52. Leclercq R, Courvalin P. Bacterial resistance to macrolide, lincosamide, and streptogramin antibiotics by target modification. Antimicrob Agents Chemother 1991; 35(7): 1267–72

    Article  PubMed  CAS  Google Scholar 

  53. Leclercq R, Courvalin P. Intrinsic and unusual resistance to macrolide, lincosamide, and streptogramin antibiotics in bacteria. Antimicrob Agents Chemother 1991; 35(7): 1273–6

    Article  PubMed  CAS  Google Scholar 

  54. Rende Fournier R, Leclercq R, Galimand M, et al. Identification of the satA gene encoding a streptogramin A acetyltransferase in Enterococcus faecium. BM 4145. Antimicrob Agents Chemother 1993; 37(10): 2119–5

    Article  PubMed  CAS  Google Scholar 

  55. Jensen L, Hammerum AM, Aarestrup FM, et al. Occurence of satA and vgb genes in streptogramin-resistant Enterococcus faecium. isolates of animal and human origins in the Netherlands. Antimicrob Agents Chemother 1998; 42: 3330–1

    PubMed  CAS  Google Scholar 

  56. Weisblum B. Erythromycin resistance by ribosome modification. Antimicrob Agents Chemother 1995; 39: 577–608

    Article  PubMed  CAS  Google Scholar 

  57. ElSolh N, Allignet J. Staphylococcal resistance to streptogramins and related antibiotics. Drug Resist Update 1998; 1(3): 169–75

    Article  CAS  Google Scholar 

  58. Poyart-Salmeron C, Carlier C, Trieu-Cuot P, et al. Transferable plasmid-mediated antibiotic resistance in Listeria monocytogenes. Lancet 1990; 335(8703): 1422–6

    Article  PubMed  CAS  Google Scholar 

  59. Doucet-Populaire F, Trieu-Cuot P, Dosbaa I, et al. Inducible transfer of conjugative transposon Tnl545 from Enterococcus faecalis to Listeria monocytogenes in the digestive tracts of gnotobiotic mice. Antimicrob Agents Chemother 1991; 35(1): 185–7

    Article  PubMed  CAS  Google Scholar 

  60. Wolf H. Avilamycin, an inhibitor of the 30S ribosomal subunits function. FEBS Lett 1973; 36(2): 181–6

    Article  PubMed  CAS  Google Scholar 

  61. Aarestrup FM. Association between decreased susceptibility to a new antibiotic for treatment of human diseases, everninomycin (SCH 27899), and resistance to an antibiotic used for growth promotion in animals, avilamycin. Microb Drug Resist Mech Epidemiol Dis 1998; 4: 137–41

    Article  CAS  Google Scholar 

  62. Prescott JF, Sivendra R, Barnum DA. The use of bacitracin in the prevention and treatment of experimentally-induced necrotic enteritis in the chicken. Can Vet J 1978; 19(7): 181–3

    PubMed  CAS  Google Scholar 

  63. Wicker DL, Isgrigg WN, Trammel JH. The control and prevention for necrotic enteritis in broilers with zinc bacitracin. Poultry Sci 1977; 56: 1229–31

    Article  CAS  Google Scholar 

  64. Weidema WF, van den Bogaard AE. Whole gut irrigation and antimicrobial prophylaxis in elective colorectal surgery. Neth J Surg 1984; 5: 1–108

    Google Scholar 

  65. O’Donovan CA, Fan-Havard P, Tecson-Tumang FT, et al. Enteric eradication of vancomycin-resistant Enterococcus faecium with oral bacitracin. Diagn Microbiol Infect Dis 1994; 18(2): 105–9

    Article  PubMed  Google Scholar 

  66. Chia JK, Nakata MM, Park SS, et al. Use of bacitracin therapy for infection due to vancomycin-resistant Enterococcus faecium. Clin Infect Dis 1995; 21(6): 1520

    Article  PubMed  CAS  Google Scholar 

  67. Cain BD, Norton PJ, Eubanks W, et al. Amplification of the bacA gene confers bacitracin resistance to Escherichia coli. J Bacteriol 1993; 175(12): 3784–9

    PubMed  CAS  Google Scholar 

  68. Allen NE, Hobbs Jr JN. Induction of vancomycin resistance in Enterococcus faecium by non-glycopeptide antibiotics. FEMS Microbiol Lett 1995; 132(1–2): 107–4

    Article  PubMed  CAS  Google Scholar 

  69. Lai MH, Kirsch DR. Induction signals for vancomycin resistance encoded by the vanA gene cluster in Enterococcus faecium. Antimicrob Agents Chemother 1996; 40(7): 1645–8

    PubMed  CAS  Google Scholar 

  70. Walton JR. The effect of zinc bacitracin on the susceptibility of selected Gram-negative and Gram-positive bacteria to therapeutic antibiotics. Zentralbl Veterinar Med B 1978; 25(4): 329–1

    Article  CAS  Google Scholar 

  71. Walton JR, Wheeler JE. Loss of resistance to the tetracyclines from porcine Escherichia coli in contact with dietary bacitracin methylene disalicylate. Zentralbl Veterinarmed B 1987; 34(3): 161–4

    PubMed  CAS  Google Scholar 

  72. Walton JR. The effect of dietary zinc bacitracin on the resistance status of intestinal Escherichia coli and enterococci from broiler chickens. Zentralbl Veterinar Med B 1984; 31(1): 1–8

    Article  CAS  Google Scholar 

  73. Gedek B. Factors influencing multiple resistance in enteric bacteria in animals. Proceedings of ten years on from Swann; London: 1981 Oct 5–6: 111–26

    Google Scholar 

  74. Huber G. Monomycin and related phosporus containing antibiotics. In: Hahn FE, editor. Antibiotics. New York: Springer Verlag, 1979: 135–53

    Google Scholar 

  75. Dealy J, Moeller MW. Influence of bambermycins on Salmonella infection and antibiotic resistance in swine. J Anim Sci 1976; 42(5): 1331–6

    PubMed  CAS  Google Scholar 

  76. Dealy J, Moeller MW. Effect of bambermycins on Escherichia coli and antibiotic resistance in calves. J Anim Sci 1977; 45(6): 1239–42

    PubMed  CAS  Google Scholar 

  77. Dealy J, Moeller MW. Influence of bambermycins on Salmonella infection and antibiotic resistance in calves. J Anim Sci 1977; 44(5): 734–8

    PubMed  CAS  Google Scholar 

  78. Corpet DE. The effect of bambermycin, carbadox, chlortetra-cycline and olaquindox on antibiotic resistance in intestinal coliforms: a new animal model. Ann Microbiol Paris 1984; 135a(2): 329–9

    PubMed  CAS  Google Scholar 

  79. Sepulchre M. Flavomycine: inhibition de l’antibioresistance chez les enterobacteries. Bulletin Mensuel de la Societé Vétérinaire Practique de France 1979; 63 199–225

  80. George BA, Fagerberg DJ, Quarles CL, et al. Effect of bambermycins on quantity, prevalence, duration, and antimicrobial resistance of Salmonella typhimurium in experimentally infected broiler chickens. Am J Vet Res 1982; 43: 299–303

    PubMed  CAS  Google Scholar 

  81. George BA, Fagerberg DJ. Effect of bambermycins, in vitro, on plassmid-mediated antimicrobial resistance. Am J Vet Res 1984; 45: 2336–41

    PubMed  CAS  Google Scholar 

  82. Pohl P, Laub Kupersztejn R, Thomas J, et al. Effects de la flavomycine et de quelques agents antiparasitaires sur une souche colibacillaire hébergeant divers facteurs-R. Ann Méd Vét 1975; 119: 51–7

    CAS  Google Scholar 

  83. Devriese LA. Sensitivity of staphylococci from farm animals to antibacterial agents used for growth promotion and therapy: a ten-year study. Ann Res Vet 1980; 11(4): 399–408

    CAS  Google Scholar 

  84. Ohmae K, Yonezawa S, Terakado N. R plasmid with carbadox resistance from Escherichia coli of porcine origin. Antimicrob Agents Chemother 1981; 19(1): 86–90

    Article  PubMed  CAS  Google Scholar 

  85. Ohmae K, Yonezawa S, Terakado N. Epizootiological studies on R plasmid with carbadox resistance. Nippon Juigaku Zasshi 1983; 45(2): 165–70

    Article  PubMed  CAS  Google Scholar 

  86. Quelette M, Nicas M, Kundig C. Antimicrobial multidrug resistance. Int J Antimicrob Agents 1997; 8(3): 179–87

    Article  Google Scholar 

  87. Cohen SP, Hachler H, Levy SB. Genetic and functional analysis of the multiple antibiotic resistance (mar) locus in Escherichia coli. J Bacteriol 1993; 175(5): 1484–92

    PubMed  CAS  Google Scholar 

  88. Hartmann FA, Trostle SS, Klohnen AA. Isolation of methicillin-resistant Staphylococcus aureus from a postoperative wound infection in a horse. J Am Vet Med Assoc 1997; 211(5): 590–2

    PubMed  CAS  Google Scholar 

  89. Tomlin J, Pead MJ, Lloyd DH, et al. Methicillin-resistant Staphylococcus aureus infections in 11 dogs. Vet Rec 1999; 144: 60–4

    Article  PubMed  CAS  Google Scholar 

  90. Courvalin P. Transfer of antibiotic resistance genes between Gram-positive and Gram-negative bacteria. Antimicrob Agents Chemother 1994; 38(7): 1447–51

    Article  PubMed  CAS  Google Scholar 

  91. Brisson-Noel A, Arthur M, Courvalin P. Evidence of natural gene transfer from Gram-positive cocci to Escherichia coli. J Bacteriol 1988; 170: 1739–45

    PubMed  CAS  Google Scholar 

  92. Doucet-Populaire F, Trieu-Cuot P, Andremont A, et al. Conjugal transfer of plasmid DNA from Enterococcus faecalis to Escherichia coli in digestive tracts of gnotobiotic mice. Antimicrob Agents Chemother 1992; 36(2): 502–4

    Article  PubMed  CAS  Google Scholar 

  93. Biavasco F, Giovanetti E, Miele A, et al. In vitro conjugative transfer of VanA vancomycin resistance between Enterococci and Listeriae of different species. Eur J Clin Microbiol Infect Dis 1996; 15(1): 50–9

    Article  PubMed  CAS  Google Scholar 

  94. Franklin A, Mollby R. Concurrent transfer and recombination between plasmids encoding for heat-stable enterotoxin and drug resistance in porcine enterotoxigenic Escherichia coli. Med Microbiol Immunol Berl 1983; 172(3): 137–47

    Article  PubMed  CAS  Google Scholar 

  95. Mullany P, Wilks M, Taba of chali S. Transfer of macrolide-lincosamide-streptogramin B (MLS) resistance in Clostridium difficile is linked to a gene homologous with toxin A and is mediated by a conjungative tansposon, Tn 5398. J Antimicrobial Chemother 1995; 35: 305–15

    Article  CAS  Google Scholar 

  96. Lester SC, del Pilar-Pla M, Wang F, et al. The carriage of Escherichia coli resistant to antimicrobial agents by healthy children in Boston, in Caracas, Venezuela, and in Qin Pu, China. N Engl J Med 1990; 323(5): 285–9

    Article  PubMed  CAS  Google Scholar 

  97. Van den Bogaard AE, London N, Driessen C, et al. Fluoro-quinolone usage in animals and resistance in human faecal E. coli [abstract]. 37th International Conference on Antimicrobial Agents and Chemotherapy; 1997 Sep 24–7; Toronto, C-137

  98. Linton AH, Hinton MH, Al Chalaby ZA. Monitoring for antibiotic resistance in enterococci consequent upon feeding growth promoters active against gram-positive bacteria. J Vet Pharmacol Ther 1985; 8(1): 62–70

    Article  PubMed  CAS  Google Scholar 

  99. Thal LA, Welton LA, Perri MB, et al. Antimicrobial resistance in enterococci isolated from turkeys fed virginiamycin [abstract]. Proceedings of 36th International Conference on Antimicrobial Agents and Chemotherapy; 1996 Sep 15–18; New Orleans

  100. Linton AH, Hedges AJ, Bennet PM. Monitoring for the development of antimicrobial resistance during the use of olaquindox as a feed additive on commercial pig farms. J Appl Bacteriol 1988; 64: 311–27

    Article  PubMed  CAS  Google Scholar 

  101. Mills KW, Kelly BL. Antibiotic susceptibilities of swine Salmonella isolates from 1979 to 1983. Am J Vet Res 1986; 47(11): 2349–50

    PubMed  CAS  Google Scholar 

  102. Hedges AJ, Linton AH. Olaquindox resistance in the coliform flora of pigs and their environment: an ecological study. J Appl Bacteriol 1988; 64(5): 429–3

    Article  PubMed  CAS  Google Scholar 

  103. McDonald LC, Kuehnert MJ, Tenover FC, et al. Vancomycin-resistant enterococci outside the health-care setting: prevalence, sources, and public health implications. Emerg Infect Dis 1997; 3(3): 311–7

    Article  PubMed  CAS  Google Scholar 

  104. van den Braak N, van Belkum A, van Keulen M, et al. Molecular characterization of vancomycin-resistant enterococci from hospitalized patients and poultry products in the Nethrelands. J Clin Microbiol 1998; 36: 1927–32

    PubMed  Google Scholar 

  105. van den Bogaard AE, Jensen LB, Stobberingh EE. Vancomycin-resistant enterococci in turkeys and fanners [letter]. N Engl J Med 1997; 337(21): 1558–9

    Article  PubMed  Google Scholar 

  106. van den Bogaard AE, Mertens P, London NH, et al. High prevalence of colonization with vancomycin- and pristinamycin-resistant enterococci in healthy humans and pigs in The Netherlands: is the addition of antibiotics to animal feeds to blame? [letter]. J Antimicrob Chemother 1997; 40(3): 454–6

    Article  PubMed  Google Scholar 

  107. Tast E, Honkanen-Buzalski T, Mannerkorpi P. Tylosin and spiramycin as feed additives: influence on the efficacy of therapeutic macrolides. Report of the Ministry of Agriculture and Forestry of Finland, Julkaisuja, May 1997

  108. Antimicrobial Growth Promoters. Committee on Antimicrobial Growth Promoters. Health Council of the Netherlands, 1998; No. 1998/15E, Rijswijk, The Netherlands

  109. Van den Bogaard A, London N, Driessen C, et al. Prevalence of resistant faecal bacteria in turkeys, turkey farmers and turkey slaughterers [abstract]. 36th International Conference on Antimicrobial Agents and Chemotherapy; 1996 Sep 15–8; New Orleans; C-163

  110. Bager F, Madsen M, Christensen J, et al. 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 1997; 31(1–2): 95–112

    Article  PubMed  CAS  Google Scholar 

  111. Bezanson GS, Khakhria R, Bollegraaf E. Nosocomial outbreak caused by antibiotic-resistant strain of Salmonella typhimurium acquired from dairy cattle. Can Med Assoc J 1983; 128(4): 426–7

    PubMed  CAS  Google Scholar 

  112. Holmberg SD, Osterholm MT, Senger KA, et al. Drug-resistant Salmonella from animals fed antimicrobials. N Engl J Med 1984; 311(10): 617–22

    Article  PubMed  CAS  Google Scholar 

  113. Mishu B, Griffin PM, Tauxe RV, et al. Salmonella enteritidis gastroenteritis transmitted by intact chicken eggs. Ann Intern Med 1991; 115(3): 190–4

    PubMed  CAS  Google Scholar 

  114. Spika JS, Waterman SH, Hoo GW, et al. Chloramphenicol-resistant Salmonella newport traced through hamburger to dairy farms: a major persisting source of human salmonellosis in California. N Engl J Med 1987; 316(10): 565–70

    Article  PubMed  CAS  Google Scholar 

  115. Datta N, Hughes VM. Plasmids of the same Inc groups in Enterobacteria before and after the medical use of antibiotics. Nature 1983; 306(5943): 616–7

    Article  PubMed  CAS  Google Scholar 

  116. Deleener J, Haeebaert K. Enquête sur la role joué dans propagation de Salmonella et Shigella par les porteurs de germes dans l’industrie de la viande. Med Mal Infect 1980; 10: 394–8

    Article  Google Scholar 

  117. Wray C. Medical impact of antimicrobial use in food animal production: scenarios and risk assessment Salmonella and E. coli in England and Wales. Proceedings of the WHO Meeting on the Usage of Quinolones in Animals. 1997 Oct 13–7; Berlin

  118. Manten A, Guinée PA, Kampelmacher EH, et al. An elevenyear study of drug resistance in Salmonella in the Netherlands. Bull World Health Organ 1971; 45(1): 85–93

    PubMed  CAS  Google Scholar 

  119. Voogd CE, Guinée PA, Manten A, et al. Incidence of resistance to tetracycline, chloramphenicol and ampicillin among Salmonella species isolated in The Netherlands in 1965 and 1966. Antonie van Leeuwenhoek 1968; 34(3): 357–64

    Article  PubMed  CAS  Google Scholar 

  120. Voogd CE, Guinee PA, Manten A, et al. Incidence of resistance to tetracycline, chloramphenicol and ampicillin among Salmonella species isolated in the Netherlands in 1967 and 1968. Antonie van Leeuwenhoek 1970; 36(2): 297–304

    Article  PubMed  CAS  Google Scholar 

  121. Voogd CE, van Leeuwen WJ, Guinee PA, et al. Incidence of resistance to ampicillin, chloramphenicol, kanamycin and tetracycline among Salmonella species isolated in the Netherlands in 1972, 1973 and 1974. Antonie van Leeuwenhoek 1977; 43(3-4): 269–81

    Article  PubMed  CAS  Google Scholar 

  122. van Leeuwen WJ, Voogd C, Guinée PA, et al. Incidence of resistance to ampicillin, chloramphenicol, kanamycin, tetracycline and trimethoprim of Salmonella strains isolated in The Netherlands during 1975–1980. Antonie van Leeuwenhoek 1982; 48(1): 85–96

    Article  PubMed  Google Scholar 

  123. Cherubin CE. Epidemiological assessments of antibiotic resistance in Salmonella. In: Steel JH, Beran GW, editors. CRC Handbook series in zoonoses. Boca Raton (FL): CRC Press Inc, 1984: 173–200

    Google Scholar 

  124. National Academy of Sciences. Committee to study the human health aspects of subtherapeutic antibiotic use in animal feeds. Washington, DC: National Press, 1980

    Google Scholar 

  125. Threlfall EJ, Frost JA, Ward LR, et al. Epidemic in cattle and humans of Salmonella typhimurium DT 104 with chromosomally integrated multiple drug resistance [see comments]. Vet Rec 1994; 134(22): 577

    Article  PubMed  CAS  Google Scholar 

  126. Threlfall EJ, Frost JA, Ward LR, et al. Increasing spectrum of resistance in multiresistant Salmonella typhimurium [letter]. Lancet 1996; 347(9007): 1053–4

    Article  PubMed  CAS  Google Scholar 

  127. Endtz HP, Ruijs GT, van Klingeren B, et al. Quinolone resistance in campylobacter isolated from man and poultry following the introduction of fluoroquinolones in veterinary medicine. J Antimicrob Chemother 1991; 27(2): 199–208

    Article  PubMed  CAS  Google Scholar 

  128. Jacobs-Reitsma WF, Kan CA, Bolder NM. The introduction of quinolone resistance in Campylobacter bacteria in broilers by quinolone treatment. Lett Applied Microbiol 1994; 19(4): 228–31

    Article  CAS  Google Scholar 

  129. Gaunt PN, Piddock LJ. Ciprofloxacin-resistant Campylobacter spp. in humans: an epidemiological and laboratory study. J Antimicrob Chemother 1996; 37(4): 747–57

    Article  PubMed  CAS  Google Scholar 

  130. Perez Trallero E, Zigortrga C, Cilla G, et al. Animal origin of the antibiotic resistance of human pathogenic Yersinia enterocolitica [letter]. Scand J Infect Dis 1988; 20(5): 572–3

    Google Scholar 

  131. van der Waaij D. Colonization resistance of the digestive tract: clinical consequences and implications. J Antimicrob Chemother 1982; 10(4): 263–70

    Article  PubMed  Google Scholar 

  132. Vollaard EJ, Clasener HA. Colonization resistance. Antimicrob Agents Chemother 1994; 38(3): 409–14

    Article  PubMed  CAS  Google Scholar 

  133. Vollaard EJ, Clasener HA, van Saene HK, et al. Effect on colonization resistance: an important criterion in selecting antibiotics. DICP 1990; 24(1): 60–6

    PubMed  CAS  Google Scholar 

  134. Barrow PA, Smith HW, Tucker JF. The effect of feeding diets containing avoparcin on the excretion of salmonellas by chickens experimentally infected with natural sources of salmonella organisms. J Hyg Lond 1984; 93(3): 439–4

    Article  PubMed  CAS  Google Scholar 

  135. Barrow PA. Further observations on the effect of feeding diets containing avoparcin on the excretion of salmonellas by experimentally infected chickens. Epidemiol Infect 1989; 102 239–52

    Google Scholar 

  136. Gustafson RH, Beck JR, Kohbland JD. The influence of Avoparcin on the establishment of Salmonella in chickens. Zentralbl Veterinär Med B 1981; 29: 119–28

    Article  Google Scholar 

  137. Abou Youssef MH, DiCuollo CJ, Miller CR, et al. Influence of a sub-therapeutic level of virginiamycin in feed on the incidence and persistence of Salmonella typhimurium in experimentally infected swine. J Anim Sci 1979; 49(1): 128–33

    PubMed  CAS  Google Scholar 

  138. Abou Youssef MH, DiCuollo CJ, Free SM, et al. The influence of a feed additive level of virginiamycin on the course of an experimentally induced Salmonella typhimurium. infection in broilers. Poult Sci 1983; 62(1): 30–7

    Article  PubMed  CAS  Google Scholar 

  139. Matthes S, Leuchtenberger WG, Loliger HC. Effect of antibiotic feed additives on the intestinal flora and the persistence of salmonellae in chickens. Dtsch Tierarztl Wochenschr 1982; 89(1): 19–22

    PubMed  CAS  Google Scholar 

  140. Smith HW, Tucker JF. The effect of feeding diets containing permitted antibiotics on the faecal excretion of Salmonella typhimurium. by experimentally infected chickens. J Hyg Lond 1975; 75(2): 293–301

    Article  PubMed  CAS  Google Scholar 

  141. Smith HW, Tucker JF. The effect of antimicrobial feed additives on the colonization of the alimentary tract of chickens by Salmonella typhimurium. JHyg Lond 1978; 80(2): 217–31

    Article  CAS  Google Scholar 

  142. Ford AM, Fagerberg DJ, Quarles CL, et al. Influence of salinomycin on incidence, shedding, and antimicrobial resistance of Salmonella typhimurium. in experimentally infected broiler chicks. Poult Sci 1981; 60(11): 2441–53

    Article  PubMed  CAS  Google Scholar 

  143. Corpet DE. Antibiotic resistance from food [letter]. N Engl J Med 1988; 318(18): 1206–7

    PubMed  CAS  Google Scholar 

  144. Nijsten R, London N, van den Bogaard A, et al. Resistance in faecal Escherichia coli isolated from pigfarmers and abattoir workers. Epidemiol Infect 1994; 113(1): 45–52

    Article  PubMed  CAS  Google Scholar 

  145. Nijsten R, London N, van den Bogaard A, et al. Antibiotic resistance among Escherichia coli isolated from faecal samples of pig farmers and pigs. J Antimicrob Chemother 1996; 37(6): 1131–40

    Article  PubMed  CAS  Google Scholar 

  146. Edlund C, Barkholt L, OlssonLiljequist B, et al. Effect of van-comycin on intestinal flora of patients who previously received antimicrobial therapy. Clin Infect Dis 1997; 25: 729–32

    Article  PubMed  CAS  Google Scholar 

  147. van der Auwera P, Pensart N, Korten V, et al. Influence of oral glycopeptides on the faecal flora of human volunteers: selection of highly glucopeptide resistant enterococci. J Infect Dis 1996; 173(5): 1129–36

    Article  PubMed  Google Scholar 

  148. Quednau M, Ahme S, Petersson AC, et al. Antibiotic-resistant strains of Enterococcus isolated from Swedish and Danish retailed chicken and pork. J Applied Microbiol 1998; 84(6): 1163–70

    Article  CAS  Google Scholar 

  149. Schouten MA, Voss A, Hoogkamp-Korstanje JAA. Carnivorous humans, but not from vegetarians [letter]. Lancet 1997; 349: 1258

    Article  PubMed  CAS  Google Scholar 

  150. Levy SB, FitzGerald GB, Macone AB. Spread of antibiotic-resistant plasmids from chicken to chicken and from chicken to man. Nature 1976; 260(5546): 40–2

    Article  PubMed  CAS  Google Scholar 

  151. Levy SB, FitzGerald GB, Macone AB. Changes in intestinal flora of farm personnel after introduction of a tetracycline-supplemented feed on a farm. N Engl J Med 1976; 295(11): 583–8

    Article  PubMed  CAS  Google Scholar 

  152. Nikolich MP, Hong G, Shoemaker NB, et al. Evidence for natural horizontal transfer of tetQ between bacteria that normally colonize humans and bacteria that normally colonize livestock. Appl Environ Microbiol 1994; 60(9): 3255–60

    PubMed  CAS  Google Scholar 

  153. Shoemaker NB, Wang GR, Salyers AA. Evidence for natural transfer of a tetracycline resistance gene between bacteria from the human colon and bacteria from the bovine rumen. Appl Environ Microbiol 1992; 58(4): 1313–20

    PubMed  CAS  Google Scholar 

  154. Hummel R, Tschäpe H, Witte W. Spread of plasmid-mediated nourseothricin resistance due to antibiotic use in animal husbandry. J Basic Microbiol 1986; 8: 461–6

    Article  Google Scholar 

  155. Chalus-Dancla E, Glupczynski Y, Gerbaud G, et al. Detection of apramycin-resistant Enterobacteriaceae in hospital isolates. FEMS Microbiol Lett 1989; 61: 261–6

    Article  Google Scholar 

  156. Hunter JE, Hart CA, Shelley JC, et al. Human isolates of apramycin-resistant Escherichia coli which contain the genes for the AAC(3)IV enzyme. Epidemiol Infect 1993; 110(2): 253–9

    Article  PubMed  CAS  Google Scholar 

  157. Threlfall EJ, Rowe B, Ferguson JL, et al. Characterization of plasmids conferring resistance to gentamicin and apramycin in strains of Salmonella typhimurium. phage type 204c isolated in Britain. J Hyg Camb 1986; 97(3): 419–26

    Article  PubMed  CAS  Google Scholar 

  158. Chaslus Dancla E, Martel JL, Carlier C, et al. Emergence of aminoglycoside 3-N-acetyltransferase IV in Escherichia coli and Salmonella typhimurium. isolated from animals in France. Antimicrob Agents Chemother 1986; 29(2): 239–43

    Article  PubMed  CAS  Google Scholar 

  159. Salauze D, Otal I, Gomez-Lus R, et al. Aminoglycoside acetyl-transferase 3-IV (aacC4) and hygromycin B 4-1 phosphotransferase (hphB) in bacteria isolated from human and animal sources. Antimicrob Agents Chemother 1990; 34(10): 1915–20

    Article  PubMed  CAS  Google Scholar 

  160. Chaslus Dancla E, Pohl P, Meurisse M, et al. High genetic homology between plasmids of human and animal origins conferring resistance to the aminoglycosides gentamicin and apramycin. Antimicrob Agents Chemother 1991; 35(3): 590–3

    Article  PubMed  CAS  Google Scholar 

  161. Simonsen GS, Haaheim H, Dahl KH, et al. Transmission of VanA-type vancomycin-resistant enteroccci and VanA resistance elements between chicken and humans at avoparcin-exposed farms. Microb Drug Resist Mech Epidemiol Dis 1998; 4: 313–8

    Article  CAS  Google Scholar 

  162. Kirk M, Chen HY, Hill RLR, et al. Novel insertion sequences from vancomycin-resistant Enterococcus faecium isolated from poultry [abstract]. Proceedings of 37th International Conference on Antimicrobial Agents and Chemotherapy; 1997 Sep 28–Oct 1; Toronto, C-134

  163. van den Bogaard AE. A veterinary antibiotic policy: a personal view on the perspectives in The Netherlands. Vet Microbiol 1993; 35(3–4): 303–12

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anthony E. van den Bogaard.

Rights and permissions

Reprints and permissions

About this article

Cite this article

van den Bogaard, A.E., Stobberingh, E.E. Antibiotic Usage in Animals. Drugs 58, 589–607 (1999). https://doi.org/10.2165/00003495-199958040-00002

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2165/00003495-199958040-00002

Keywords

Navigation