1932

Abstract

Rapidly rising incomes are driving demand for animal protein and livestock globally. The move toward more intensive production systems to support this increased demand is projected to increase the dependence on antibiotic growth promoters. The volume of antibiotics used for growth promotion in livestock outstrips that used for disease treatment in humans and creates significant selection pressure for the evolution of antibiotic resistance—a challenge for global health and resource conservation. This review describes the benefits and costs of antibiotic growth promoters in livestock and considers the prospects for more fully accounting for the externality costs.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-resource-100814-125015
2015-10-05
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/resource/7/1/annurev-resource-100814-125015.html?itemId=/content/journals/10.1146/annurev-resource-100814-125015&mimeType=html&fmt=ahah

Literature Cited

  1. Aarestrup FM, Jensen VF, Emborg HD, Jacobsen E, Wegener HC. 2010. Changes in the use of antimicrobials and the effects on productivity of swine farms in Denmark. Am. J. Vet. Res. 71:726–33 [Google Scholar]
  2. Aarestrup FM, Seyfarth AM, Emborg H-D, Pedersen K, Hendriksen RS, Bager F. 2001. Effect of abolishment of the use of antimicrobial agents for growth promotion on occurrence of antimicrobial resistance in fecal enterococci from food animals in Denmark. Antimicrob. Agents Chemother. 45:72054–59 [Google Scholar]
  3. Andersson DI, Hughes D. 2014. Microbiological effects of sublethal levels of antibiotics. Nat. Rev. Microbiol. 12:7465–78 [Google Scholar]
  4. Armstrong GL, Conn LA, Pinner RW. 1999. Trends in infectious disease mortality in the United States during the 20th century. JAMA 281:161–66 [Google Scholar]
  5. Bager F, Aarestrup FM, Madsen M, Wegener HC. 1999. Glycopeptide resistance in Enterococcus faecium from broilers and pigs following discontinued use of avoparcin. Microb. Drug Resist. 5:153–56 [Google Scholar]
  6. Bager F, Madsen M, Christensen J, Aarestrup FM. 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. 31:1-295–112 [Google Scholar]
  7. Barug D, de Jong J, Kies AK, Verstegen MWA. 2006. Antimicrobial Growth Promoters: Where Do We Go From Here? Wageningen, Neth.: Wageningen Acad.
  8. Bengtsson B, Greko C. 2014. Antibiotic resistance—consequences for animal health, welfare, and food production. Ups. J. Med. Sci. 119:296–102 [Google Scholar]
  9. Bertrand S, Weill F-X, Cloeckaert A, Vrints M, Mairiaux E et al. 2006. Clonal emergence of extended-spectrum beta-lactamase (CTX-M-2)-producing Salmonella enterica serovar Virchow isolates with reduced susceptibilities to ciprofloxacin among poultry and humans in Belgium and France (2000 to 2003). J. Clin. Microbiol. 44:82897–903 [Google Scholar]
  10. Braude R, Wallace HD, Cunha TJ. 1953. The value of antibiotics in the nutrition of swine; a review. Antibiot. Chemother. 3:3271–91 [Google Scholar]
  11. Brorsen BW, Lehenbauer T, Ji D, Connor J. 2002. Economic impacts of banning subtherapeutic use of antibiotics in swine production. J. Agric. Appl. Econ. 34(3):489–500
  12. Burroughs W. 1959. Five-year summary of more than 400 experimental comparisons of feed additives in beef cattle rations at college experimental stations. Presented at ASAP Ext. Sect. Meet., Nov.
  13. Campagnolo ER, Johnson KR, Karpati A, Rubin CS, Kolpin DW et al. 2002. Antimicrobial residues in animal waste and water resources proximal to large-scale swine and poultry feeding operations. Sci. Total Environ. 299:1–389–95 [Google Scholar]
  14. Chantziaras I, Boyen F, Callens B, Dewulf J. 2013. Correlation between veterinary antimicrobial use and antimicrobial resistance in food-producing animals: a report on seven countries. J. Antimicrob. Chemother. 69:827–34 [Google Scholar]
  15. Chapin A, Rule A, Gibson K, Buckley T, Schwab K. 2005. Airborne multidrug-resistant bacteria isolated from a concentrated swine feeding operation. Environ. Health Perspect 113:2137–42 [Google Scholar]
  16. Chapman HD, Johnson ZB. 2002. Use of antibiotics and roxarsone in broiler chickens in the USA: analysis for the years 1995 to 2000. Poult. Sci. 81:3356–64 [Google Scholar]
  17. Chee-Sanford JC, Aminov RI, Krapac IJ, Garrigues-Jeanjean N, Mackie RI. 2001. Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities. Appl. Environ. Microbiol. 67:41494–502 [Google Scholar]
  18. Coates ME, Dickinson CD, Harrison GF, Kon SK, Cummins SH, Cuthbertson WFJ. 1951. Mode of action of antibiotics in stimulating growth of chicks. Nature 168:4269332 [Google Scholar]
  19. Cogliani C, Goossens H, Greko C. 2011. Restricting antimicrobial use in food animals: lessons from Europe. Microbe 6:274–79 [Google Scholar]
  20. Cromwell GL. 2002. Why and how antibiotics are used in swine production. Anim. Biotechnol. 13:17–27 [Google Scholar]
  21. Delgado CL. 2003. Rising consumption of meat and milk in developing countries has created a new food revolution. J. Nutr. 133:11S3907–10 [Google Scholar]
  22. Dibner JJ, Richards JD. 2005. Antibiotic growth promoters in agriculture: history and mode of action. Poult. Sci. 84:4634–43 [Google Scholar]
  23. Dritz SS, Tokach MD, Goodband RD, Nelssen JL. 2002. Effects of administration of antimicrobials in feed on growth rate and feed efficiency of pigs in multisite production systems. J. Am. Vet. Med. Assoc. 220:111690–95 [Google Scholar]
  24. Dutil L, Irwin R, Finley R, Ng LK, Avery B et al. 2010. Ceftiofur resistance in Salmonella enterica serovar Heidelberg from chicken meat and humans, Canada. Emerg. Infect. Dis. 16:148–54 [Google Scholar]
  25. Elwinger K. 1976. Synthesis of Danish and Swedish experiments with growth-stimulating substances (mainly bacitracin zinc and Payzone) in poultry feed. Rep., Dep. Anim. Nutr. Manag., Swed. Univ. Agric. Sci. (In Swedish)
  26. Emborg H, Ersboll AK, Heuer OE, Wegener HC. 2001. The effect of discontinuing the use of antimicrobial growth promoters on the productivity in the Danish broiler production. Prev. Vet. Med. 50:53–70 [Google Scholar]
  27. Endtz HP, Ruijs GJ, van Klingeren B, Jansen WH, van der Reyden T, Mouton RP. 1991. Quinolone resistance in Campylobacter isolated from man and poultry following the introduction of fluoroquinolones in veterinary medicine. J. Antimicrob. Chemother. 27:2199–208 [Google Scholar]
  28. Engberg J, Aarestrup FM, Taylor DE, Gerner-Smidt P, Nachamkin I. 2001. Quinolone and macrolide resistance in Campylobacter jejuni and C. coli: resistance mechanisms and trends in human isolates. Emerg. Infect. Dis. 7:124–34 [Google Scholar]
  29. Engster HM, Marvil D, Stewart-Brown B. 2002. The effect of withdrawing growth promoting antibiotics from broiler chickens: a long-term commercial industry study. J. Appl. Poult. Res. 11:4431–36 [Google Scholar]
  30. ESVAC (European Surveillance of Veterinary Antibiotic Consumption) 2014. Sales of veterinary antimicrobial agents in 26 EU/EEA countries in 2012. Rep., ESVAC, Eur. Med. Agency
  31. Gaskins HR, Collier CT, Anderson DB. 2002. Antibiotics as growth promotants: mode of action. Anim. Biotechnol. 13:129–42 [Google Scholar]
  32. Gerber PJ, Hristov AN, Henderson B, Makkar H, Oh J et al. 2013. Technical options for the mitigation of direct methane and nitrous oxide emissions from livestock: a review. Anim. Int. J. Anim. Biosci. 7:Suppl. 2220–34 [Google Scholar]
  33. Gibbs SG, Green CF, Tarwater PM, Mota LC, Mena KD, Scarpino PV. 2006. Isolation of antibiotic-resistant bacteria from the air plume downwind of a swine confined or concentrated animal feeding operation. Environ. Health Perspect. 114:71032–37 [Google Scholar]
  34. Graham JP, Boland JJ, Silbergeld E. 2007. Growth promoting antibiotics in food animal production: an economic analysis. Public Health Rep. 122:179–87 [Google Scholar]
  35. Graveland H, Wagenaar JA, Heesterbeek H, Mevius D, van Duijkeren E, Heederik D. 2010. Methicillin resistant Staphylococcus aureus ST398 in veal calf farming: human MRSA carriage related with animal antimicrobial usage and farm hygiene. PLOS ONE 5:6e10990 [Google Scholar]
  36. Gropp JM, Birzer D, Schuhmacher A. 1992. Vom Gesamtnutzen der Futterzusatz-stoffe. In Beitrag zur Auflösung des Widerstreits von Ökonomie und Ökologie, pp. 168–204. Bonn: Verlag Ferberschen Univ. Gießen
  37. Gropp JM, Schuhmacher A. 1997. Antimicrobial growth promoters in animal husbandry. The Medical Impact of the Use of Antimicrobials in Food Animals39–49 Geneva: WHO [Google Scholar]
  38. Guo X, Mroz TA, Popkin B M, Zhai F. 2000. Structural change in the impact of income on food consumption in China, 1989–1993. Econ. Dev. Cult. Change 48:4737–60 [Google Scholar]
  39. Gupta A, Nelson JM, Barrett TJ, Tauxe RV, Rossiter SP et al. 2004. Antimicrobial resistance among Campylobacter strains, United States, 1997–2001. Emerg. Infect. Dis. 10:61102–9 [Google Scholar]
  40. Hayes DJ, Jensen HH. 2003. Lessons from the Danish ban on feed-grade antibiotics. Work. Pap., Cent. Agric. Rural Dev., Iowa State Univ.
  41. Hays VW. 1977. Effectiveness of feed additive usage of antibacterial agents in swine and poultry production Rep., Off. Technol. Assess., US Congr. https://archive.org/stream/effectivenessoff00hays#page/n3/mode/2up
  42. Heikkilä A-M, Nousiainen JI, Pyörälä S. 2012. Costs of clinical mastitis with special reference to premature culling. J. Dairy Sci. 95:1139–50 [Google Scholar]
  43. Herrmann M, Laxminarayan R. 2010. Antibiotic effectiveness: new challenges in natural resource management. Annu. Rev. Resour. Econ. 2:1125–38 [Google Scholar]
  44. Hill DC, Branion HD, Slinger SJ, Anderson GW. 1953. Influence of environment on the growth response of chicks to penicillin. Poult. Sci. 32:3462–66 [Google Scholar]
  45. Hogeveen H, Huijps K, Lam TJGM. 2011. Economic aspects of mastitis: new developments. N. Z. Vet. J. 59:116–23 [Google Scholar]
  46. Hollis A, Ahmed Z. 2013. Preserving antibiotics, rationally. N. Engl. J. Med. 369:262474–76 [Google Scholar]
  47. Hook SE, Wright A-DG, McBride BW. 2010. Methanogens: methane producers of the rumen and mitigation strategies. Archaea 2010:1–11 [Google Scholar]
  48. Huber H, Giezendanner N, Stephan R, Zweifel C. 2011. Genotypes, antibiotic resistance profiles and microarray-based characterization of methicillin-resistant Staphylococcus aureus strains isolated from livestock and veterinarians in Switzerland. Zoonoses Public Health 58:5343–49 [Google Scholar]
  49. Huijsdens XW, van Dijke BJ, Spalburg E, van Santen–Verheuvel MG, Heck ME et al. 2006. Community-acquired MRSA and pig-farming. Ann. Clin. Microbiol. Antimicrob. 5:126 [Google Scholar]
  50. Hummel R, Tschäpe H, Witte W. 1986. Spread of plasmid-mediated nourseothricin resistance due to antibiotic use in animal husbandry. J. Basic Microbiol. 26:8461–66 [Google Scholar]
  51. Jakobsen L, Kurbasic A, Skjøt-Rasmussen L, Ejrnaes K, Porsbo LJ et al. 2010a. Escherichia coli isolates from broiler chicken meat, broiler chickens, pork, and pigs share phylogroups and antimicrobial resistance with community-dwelling humans and patients with urinary tract infection. Foodborne Pathog. Dis. 7:5537–47 [Google Scholar]
  52. Jakobsen L, Spangholm DJ, Pedersen K, Jensen LB, Emborg H-D et al. 2010b. Broiler chickens, broiler chicken meat, pigs and pork as sources of ExPEC related virulence genes and resistance in Escherichia coli isolates from community-dwelling humans and UTI patients. Int. J. Food Microbiol. 142:1–2264–72 [Google Scholar]
  53. Jukes TH, Stokstad ELR, Tayloe RR, Cunha TJ, Edwards HM, Meadows GB. 1950. Growth-promoting effect of aureomycin on pigs. Arch. Biochem 26:2324–25 [Google Scholar]
  54. Key N, McBride WD. 2014. Sub-therapeutic antibiotics and the efficiency of U.S. hog farms. Am. J. Agric. Econ. 96:3831–50 [Google Scholar]
  55. Khanna T, Friendship R, Dewey C, Weese JS. 2008. Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Vet. Microbiol. 128:3–4298–303 [Google Scholar]
  56. Kjeldsen N, Callesen J. 2006. Terminated use of antimicrobial growth promoters in pig production in Denmark: effects on pig welfare and productivity. See Barug et al. 2006, pp. 127–35
  57. Klare I, Badstübner D, Konstabel C, Böhme G, Claus H, Witte W. 1999. Decreased incidence of VanA-type vancomycin-resistant enterococci isolated from poultry meat and from fecal samples of humans in the community after discontinuation of avoparcin usage in animal husbandry. Microb. Drug Resist. 5:145–52 [Google Scholar]
  58. Laanen M, Persoons D, Ribbens S, de Jong E, Callens B et al. 2013. Relationship between biosecurity and production/antimicrobial treatment characteristics in pig herds. Vet. J. 198:2508–12 [Google Scholar]
  59. Ladely SR, Harrison MA, Fedorka-Cray PJ, Berrang ME, Englen MD, Meinersmann RJ. 2007. Development of macrolide-resistant Campylobacter in broilers administered subtherapeutic or therapeutic concentrations of tylosin. J. Food Prot. 70:81945–51 [Google Scholar]
  60. Laxminarayan R, Brown GM. 2001. Economics of antibiotic resistance: a theory of optimal use. J. Environ. Econ. Manag. 42:2183–206 [Google Scholar]
  61. Levy SB, FitzGerald GB, Macone AB. 1976. Changes in intestinal flora of farm personnel after introduction of a tetracycline-supplemented feed on a farm. N. Engl. J. Med. 295:11583–88 [Google Scholar]
  62. Liu X, Miller GY, McNamara PE. 2003. Do antibiotics reduce production risk for U.S. pork producers? Presented at Meet. Am. Agric. Econ. Assoc., Montreal, July 27–30
  63. MacDonald JM, Wang S-L. 2011. Foregoing sub-therapeutic antibiotics: the impact on broiler grow-out operations. Appl. Econ. Perspect. Policy 33:179–98 [Google Scholar]
  64. Mann T, Paulsen A. 1976. Economic impact of restricting feed additives in livestock and poultry production. Am. J. Agric. Econ. 58:147–53 [Google Scholar]
  65. Marshall BM, Levy SB. 2011. Food animals and antimicrobials: impacts on human health. Clin. Microbiol. Rev. 24:4718–33 [Google Scholar]
  66. Mazurek J, Pusz P, Bok E, Stosik M, Baldy-Chudzik K. 2013. The phenotypic and genotypic characteristics of antibiotic resistance in Escherichia coli populations isolated from farm animals with different exposure to antimicrobial agents. Pol. J. Microbiol. 62:2173–79 [Google Scholar]
  67. McBride WD, Key N, Mathews KH. 2008. Subtherapeutic antibiotics and productivity in U.S. hog production. Appl. Econ. Perspect. Policy 30:2270–88 [Google Scholar]
  68. Melliere AL, Brown H, Rathmacher RP. 1973. Finishing swine performance and response to tylosin. J. Anim. Sci. 37:286 [Google Scholar]
  69. Millen DD, Pacheco RDL, Meyer PM, Rodrigues PHM, Arrigoni MDB. 2011. Current outlook and future perspectives of beef production in Brazil. Anim. Front. 1:246–52 [Google Scholar]
  70. Miller GY, Algozin KA, McNamara PE, Bush EJ. 2003. Productivity and economic effects of antibiotics used for growth promotion in U.S. pork production. J. Agric. Appl. Econ. 35(3):469–82
  71. Miller GY, Liu X, McNamara PE, Bush EJ. 2005. Farm-level impacts of banning growth- promoting antibiotic use in U.S. pig grower/finisher operations. J. Agribus. 23:2147–62 [Google Scholar]
  72. Millman JM, Waits K, Grande H, Marks AR, Marks JC et al. 2013. Prevalence of antibiotic-resistant E. coli in retail chicken: comparing conventional, organic, kosher, and raised without antibiotics. F1000 Res. 2:155 [Google Scholar]
  73. Mitchell SM, Ullman JL, Teel AL, Watts RJ, Frear C. 2013. The effects of the antibiotics ampicillin, florfenicol, sulfamethazine, and tylosin on biogas production and their degradation efficiency during anaerobic digestion. Bioresour. Technol. 149:244–52 [Google Scholar]
  74. Moore PR, Evenson A, Luckey TD, McCoy E, Elvehjem CA, Hart EB. 1946. Use of sulfasuxidine, streptothricin, and streptomycin in nutritional studies with the chick. J. Biol. Chem. 165:2437–41 [Google Scholar]
  75. Natl. Res. Counc 1999. The Use of Drugs in Food Animals: Benefits and Risks. Washington, DC: Natl. Acad. Press
  76. Nelson JM, Chiller TM, Powers JH, Angulo FJ. 2007. Fluoroquinolone-resistant Campylobacter species and the withdrawal of fluoroquinolones from use in poultry: a public health success story. Clin. Infect. Dis. 44:7977–80 [Google Scholar]
  77. Nordstrom L, Liu CM, Price LB. 2013. Foodborne urinary tract infections: a new paradigm for antimicrobial-resistant foodborne illness. Front. Microbiol 4:29 [Google Scholar]
  78. Pantosti A, Del Grosso M, Tagliabue S, Macrì A, Caprioli A. 1999. Decrease of vancomycin-resistant enterococci in poultry meat after avoparcin ban. Lancet 354:9180741–42 [Google Scholar]
  79. Perdue Foods 2014. Perdue Foods reaches milestone in reducing antibiotic use, sets standard for responsible use. Press Release. http://goo.gl/knYwnv
  80. Popkin BM. 2001. Nutrition in transition: the changing global nutrition challenge. Asia Pac. J. Clin. Nutr. 10:S13–18 [Google Scholar]
  81. Popkin BM. 2011. Contemporary nutritional transition: determinants of diet and its impact on body composition. Proc. Nutr. Soc. 70:182–91 [Google Scholar]
  82. Price LB, Johnson E, Vailes R, Silbergeld E. 2005. Fluoroquinolone-resistant Campylobacter isolates from conventional and antibiotic-free chicken products. Environ. Health Perspect. 113:5557–60 [Google Scholar]
  83. Price LB, Stegger M, Hasman H, Aziz M, Larsen J et al. 2012. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 3:1e00305–11 [Google Scholar]
  84. Reti KL, Thomas MC, Yanke LJ, Selinger LB, Inglis GD. 2013. Effect of antimicrobial growth promoter administration on the intestinal microbiota of beef cattle. Gut Pathog. 5:18 [Google Scholar]
  85. Rogers JA, Branine ME, Miller CR, Wray MI, Bartle SJ et al. 1995. Effects of dietary virginiamycin on performance and liver abscess incidence in feedlot cattle. J. Anim. Sci. 73:19–20 [Google Scholar]
  86. Rosen GD. 1995. Antibacterials in poultry and pig nutrition. Biotechnology in Animal Feeds and Animal Feeding Wallace RJ, Chesson A. 143–72 Weinheim, Ger.: Wiley [Google Scholar]
  87. Salinas-Chavira J, Lenin J, Ponce E, Sanchez U, Torrentera N, Zinn RA. 2009. Comparative effects of virginiamycin supplementation on characteristics of growth-performance, dietary energetics, and digestion of calf-fed Holstein steers. J. Anim. Sci 87:124101–8 [Google Scholar]
  88. Sapkota AR, Hulet RM, Zhang G, McDermott P, Kinney EL et al. 2011. Lower prevalence of antibiotic-resistant enterococci on U.S. conventional poultry farms that transitioned to organic practices. Environ. Health Perspect. 119:111622–28 [Google Scholar]
  89. Silbergeld EK, Graham J, Price LB. 2008. Industrial food animal production, antimicrobial resistance, and human health. Annu. Rev. Public Health 29:151–69 [Google Scholar]
  90. Smith DL, Harris AD, Johnson JA, Silbergeld EK, Morris JG. 2002. Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. PNAS 99:96434–39 [Google Scholar]
  91. Smith KE, Besser JM, Hedberg CW, Leano FT, Bender JB et al. 1999. Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992–1998. Investigation team. N. Engl. J. Med. 340:201525–32 [Google Scholar]
  92. Smith TC, Male MJ, Harper AL, Kroeger JS, Tinkler GP et al. 2009. Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in midwestern U.S. swine and swine workers. PLOS ONE 4:1e4258 [Google Scholar]
  93. Sneeringer S. 2014. The economics of sub-therapeutic antibiotic use in U.S. livestock agriculture. Presented at Antibiot. Resist. Anim. Hum. Interface Worksh., Princeton, NJ, May 13
  94. Sørensen TL, Blom M, Monnet DL, Frimodt-Møller N, Poulsen RL, Espersen F. 2001. Transient intestinal carriage after ingestion of antibiotic-resistant Enterococcus faecium from chicken and pork. N. Engl. J. Med. 345:161161–66 [Google Scholar]
  95. Speer VC, Vohs RL, Catron DV, Maddock HM, Culbertson CC. 1950. Effect of aureomycin and animal protein factor on healthy pigs. Arch. Biochem. 29:452–53 [Google Scholar]
  96. Starr MP, Reynolds DM. 1951. Streptomycin resistance of coliform bacteria from turkeys fed streptomycin. Am. J. Public Health Nations Health 41:11, Part 11375–80 [Google Scholar]
  97. Swann MM. 1969. Joint Committee on the Use of Antibiotics in Animal Husbandry and Veterinary Medicine. Rep., HMSO, London
  98. Thomke E. 1998. Growth promotants in feeding pigs and poultry. I. Growth and feed efficiency responses to antibiotic growth promotants. Ann. Zootech. 47:285–97 [Google Scholar]
  99. Tilman D, Balzer C, Hill J, Befort BL. 2011. Global food demand and the sustainable intensification of agriculture. PNAS 108:5020260–64 [Google Scholar]
  100. Unicomb LE, Ferguson J, Stafford RJ, Ashbolt R, Kirk MD et al. 2006. Low-level fluoroquinolone resistance among Campylobacter jejuni isolates in Australia. Clin. Infect. Dis. 42:101368–74 [Google Scholar]
  101. USDA 2013. Feedlot 2011—Part III: Trends in Health and Management Practices on U.S. Feedlots, 1994–2011. Fort Collins, CO: USDA/APHIS/VS/CEAH/NAHMS
  102. US FDA (Food Drug Admin.) 2012. Drug use review. http://www.fda.gov/downloads/Drugs/DrugSafety/InformationbyDrugClass/UCM319435.pdf
  103. US FDA 2013. Guidance for industry #213: new animal drugs and new animal drug combination products administered in or on medicated feed or drinking water of food-producing animals: recommendations for drug sponsors for voluntarily aligning product use conditions with GFI #209. Guid. Doc., US FDA. http://www.fda.gov/downloads/AnimalVeterinary/GuidanceComplianceEnforcement/GuidanceforIndustry/UCM299624.pdf
  104. US FDA 2014. FDA annual summary report on antimicrobials sold or distributed in 2012 for use in food-producing animals. Rep., US FDA
  105. US FDA. 2015. FDA annual summary report on antimicrobials sold or distributed in 2013 for use in food-producing animals. Rep., US FDA
  106. van Cleef BAGL, Graveland H, Haenen APJ, van de Giessen AW, Heederik D et al. 2011a. Persistence of livestock-associated methicillin-resistant Staphylococcus aureus in field workers after short-term occupational exposure to pigs and veal calves. J. Clin. Microbiol. 49:31030–33 [Google Scholar]
  107. van Cleef BAGL, Monnet DL, Voss A, Krziwanek K, Allerberger F et al. 2011b. Livestock-associated methicillin-resistant Staphylococcus aureus in humans, Europe. Emerg. Infect. Dis. 17:3502–5 [Google Scholar]
  108. van den Bogaard AE, Bruinsma N, Stobberingh EE. 2000. The effect of banning avoparcin on VRE carriage in The Netherlands. J. Antimicrob. Chemother. 46:1146–48 [Google Scholar]
  109. Van Lunen TA. 2003. Growth performance of pigs fed diets with and without tylosin phosphate supplementation and reared in a biosecure all-in all-out housing system. Can. Vet. J. 44:7571–76 [Google Scholar]
  110. Voss A, Loeffen F, Bakker J, Klaassen C, Wulf M. 2005. Methicillin-resistant Staphylococcus aureus in pig farming. Emerg. Infect. Dis. 11:121965–66 [Google Scholar]
  111. Wegener HC, Aarestrup FM, Jensen LB, Hammerum AM, Bager F. 1999. Use of antimicrobial growth promoters in food animals and Enterococcus faecium resistance to therapeutic antimicrobial drugs in Europe. Emerg. Infect. Dis. 5:332935 [Google Scholar]
  112. WHO 2002. Impacts of antimicrobial growth promoter termination in Denmark. http://apps.who.int/iris/handle/10665/68357
  113. Wierup M. 2001. The Swedish experience of the 1986 year ban of antimicrobial growth promoters, with special reference to animal health, disease prevention, productivity, and usage of antimicrobials. Microb. Drug Resist. 7:183–90 [Google Scholar]
  114. Woods A. 2011. A historical synopsis of farm animal disease and public policy in twentieth century Britain. Philos. Trans. R. Soc. B 366:15731943–54 [Google Scholar]
  115. Wulf MWH, Verduin CM, van Nes A, Huijsdens X, Voss A. 2012. Infection and colonization with methicillin resistant Staphylococcus aureus ST398 versus other MRSA in an area with a high density of pig farms. Eur. J. Clin. Microbiol. Infect. Dis. 31:161–65 [Google Scholar]
  116. Zimmerman DR. 1986. Role of subtherapeutic levels of antimicrobials in pig production. J. Anim. Sci. 62:Suppl. 36–16 [Google Scholar]
/content/journals/10.1146/annurev-resource-100814-125015
Loading
/content/journals/10.1146/annurev-resource-100814-125015
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error