Industrial food animal production, antimicrobial resistance, and human health

Annual Review of Public Health

Volumn 29, Issue , 2008, Pages 151-169

  Silbergeld, Ellen K ^a   Graham, Jay ^a   Price, Lance B ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Agriculture; Bacteria; Drug resistant pathogens; Environment; Horizontal gene transfer; Infectious disease; Poultry

Indexed keywords

ANTIINFECTIVE AGENT; ARSANILIC ACID; AVILAMYCIN; AVOPARCIN; BACITRACIN; BAMBERMYCIN; CARBADOX; CHLORTETRACYCLINE; EFROTOMYCIN; ERYTHROMYCIN; IONOPHORE; LINCOMYCIN; MACROLIDE; MONENSIN; NARASIN; NEOMYCIN; OLAQUINDOX; OXYTETRACYCLINE; PENICILLIN G; POLYESTER; POTASSIUM; PROCAINE PENICILLIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; ROXARSONE; SALINOMYCIN; SULFAMERAZINE; TETRACYCLINE; TYLOSIN; UNINDEXED DRUG; VIRGINIAMYCIN;

AGRICULTURAL PROCEDURES; AGRICULTURAL WORKER; AIR ANALYSIS; ANTIBIOTIC RESISTANCE; BACTERIAL TRANSMISSION; CONFERENCE PAPER; CROP PRODUCTION; ENVIRONMENTAL FACTOR; EVOLUTIONARY ADAPTATION; FOOD CONTAMINATION; FOOD INDUSTRY; FOOD INTAKE; HEALTH CARE UTILIZATION; HEALTH STATUS; HORIZONTAL GENE TRANSFER; HUMAN; INFECTION; NONHUMAN; POLLUTION; PREVALENCE; PRIORITY JOURNAL; PUBLIC HEALTH SERVICE; RISK ASSESSMENT; SOIL ANALYSIS; WATER ANALYSIS;

ANIMAL FEED; ANIMAL HUSBANDRY; ANIMALS; ANTI-INFECTIVE AGENTS; DRUG RESISTANCE, MICROBIAL; ENVIRONMENTAL POLLUTION; FOOD ADDITIVES; FOOD SUPPLY; HUMANS; MEAT; PUBLIC HEALTH; WORLD HEALTH;

EID: 42649115403     PISSN: 01637525     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.publhealth.29.020907.090904     Document Type: Conference Paper

References (87)

1. Aarestrup FM, Agerso Y, Gerner-Smidt P, Madsen M, Jensen LB. 2000. Comparison of antimicrobial resistance phenotypes and resistance genes in Enterococcus faecalis and Enterococcus faecium from humans in the community, broilers, and pigs in Denmark. Diagn. Microbiol. Infect. Dis. 37:127-37
2. Aarestrup FM, Seyfarth AM, Emborg HD, 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. 45:2054-59
3. Anderson ME, Sobsey MD. 2006. Detection and occurrence of antimicrobially resistant E. coli in groundwater on or near swine farms in eastern North Carolina. Water Sci. Technol. 54:211-18
4. Blazquez J, Oliver A, Gomez-Gomez JM. 2002. Mutation and evolution of antibiotic resistance: antibiotics as promoters of antibiotic resistance? Curr. Drug Targets 3:345-49
5. Bull S, Allen V, Domingue G, Jorgensen F, Frost JA, et al. 2006. Sources of Campylobacter spp. colonizing housed broiler flocks during rearing. Appl. Env. Microbiol. 72:645-52
6. Burgos J, Ellington B, Varela M. 2005. Presence of multi-drug resistant enteric bacteria in dairy farm topsoil. J. Dairy Sci. 88:1391-98
7. Cabello FC. 2006. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ. Microbiol. 8:1137-44
8. Chander Y, Kumar K, Goyal SM, Gupta SC. 2005. Antibacterial activity of soil-bound antibiotics. J. Environ. Qual. 34:1952-57
9. 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. 113:137-42
10. Cole D, Drum DJV, Stallknecht DE, White DG, Lee MD, et al. 2005. Free-living Canada geese and antimicrobial resistance. Emerg. Infect. Dis. 11:935-38
11. Collignon P. 2005. Fluoroquinolone use in food animals. Emerg. Infect. Dis. 11:1789-90; author reply 1790-92
12. D'Costa VM, McGrann KM, Hughes DW, Wright GD. 2006. Sampling the antibiotic resistome. Science 311:374-77
13. Donabedian SM, Perri MB, Vager D, Hershberger E, Malani P, et al. 2006. Quinupristin-dalfopristin resistance in Enterococcus faecium isolates from humans, farm animals, and grocery store meat in the United States. J. Clin. Microbiol. 44:3361-65
14. Emborg HD, Andersen JS, Seyfarth AM, Andersen SR, Boel J, Wegener HC. 2003. Relations between the occurrence of resistance to antimicrobial growth promoters among Enterococcus faecium isolated from broilers and broiler meat. Int. J. Food Microbiol. 84:273-84
15. 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. 27:199-208
16. 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. 431-36
17. Erb A, Sturmer T, Marre R, Brenner H. 2007. Prevalence of antibiotic resistance in Escherichia coli: overview of geographical, temporal, and methodological variations. Eur. J. Clin. Microbiol. Infect. Dis. 26:83-90
18. Fevre EM, Bronsvoort BM, Hamilton KA, Cleaveland S. 2006. Animal movements and the spread of infectious diseases. Trends Microbiol. 14:125-31
19. Fey PD, Safranek TJ, Rupp ME, Ribot E, Iwen PC, et al. 2000. Ceftriaxone-resistant salmonella infection acquired by a child from cattle. N. Engl. J. Med. 342:1242-49
20. Gerber P, Chilonda P, Franceschini G, Menzi H. 2005. Geographical determinants and environmental implications of livestock production intensification in Asia. Bioresour. Technol. 96:263-76
21. 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. 114:1032-37
22. Graham JP, Boland JJ, Silbergeld E. 2007. Growth promoting antibiotics in food animal production: an economic analysis. Public Health Rep. 122:79-87
23. Gupta A, Nelson JM, Barrett TJ, Tauze R, Rossiter SP, et al. 2004. Antimicrobial resistance among Campylobacter strains, United States, 1997-2001. Emerg. Infect. Dis. 10:1102-9
24. Hamscher G, Pawelzick HT, Sczesny S, Nau H, Hartung J. 2003. Antibiotics in dust originating from a pig-fattening farm: a new source of health hazard for farmers? Environ. Health Perspect. 111:1590-94
25. Hayes JR, English LL, Carter PJ, Proescholdt T, Lee KY, et al. 2003. Prevalence and antimicrobial resistance of enterococcus species isolated from retail meats. Appl. Environ. Microbiol. 69:7153-60
26. Hayes JR, English LL, Carr LE, Wagner DD, Joseph SW. 2004. Multiple-antibiotic resistance of Enterococcus spp. isolated from commercial poultry production environments. Appl. Environ. Microbiol. 70:6005-11
27. Henzler DJ, Opitz HM. 1992. The role of mice in the epizootiology of Salmonella enteritidis infection on chicken layer farms. Avian. Dis. 36:625-31
28. 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. 5:26
29. Islam M, Doyle MP, Phatak SC, Millner P, Jiang X. 2004. Persistence of enterohemorrhagic Escherichia coli O157:H7 in soil and on leaf lettuce and parsley grown in fields treated with contaminated manure composts or irrigation water. J. Food Prot. 67:1365-70
30. Jensen LB, Agerso Y, Sengelov G. 2002. Presence of erm genes among macrolide-resistant Gram-positive bacteria isolated from Danish farm soil. Environ. Int. 28:487-91
31. Jensen VF, Jakobsen L, Emborg HD, Seyfarth AM, Hammerum AM. 2006. Correlation between apramycin and gentamicin use in pigs and an increasing reservoir of gentamicin-resistant Escherichia coli. J. Antimicrob. Chemother. 58:101-7
32. Johnson JR, Kuskowski MA, Smith K, O'Bryan TT, Tatini S. 2005. Antimicrobial-resistant and extraintestinal pathogenic Escherichia coli in retail foods. J. Infect. Dis. 191:1040-49
33. Kieke AL, Borchardt MA, Kieke BA, Spencer SK, Vendermause MF, et al. 2006. Use of streptogramin growth promoters in poultry and isolation of streptogramin-resistant Enterococcus faecium from humans. J. Infect. Dis. 194:1200-8
34. Klare I, Badstubner D, Konstabel C, Bohme 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. 5:45-52
35. Last JM. 1995. A Dictionary of Epidemiology. New York: Oxford Univ. Press
36. Laxminarayan R. 2007. Extending the Cure: Policy Responses to the Growing Threat of Antibiotic Resistance. Washington, DC: Resour. Future
37. Lay DC, Haussmann MF, Daniels MJ. 2000. Hoop housing for feeder pigs offers a welfare-friendly environment compared to a nonbedded confinement system. J. Appl. Anim. Welf. Sci. 3:33-48
38. Levin BR, Perrot V, Walker N. 2000. Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154:985-97
39. Levy S, Miller R. 1989. Gene Transfer in the Environment. McGraw Hill: Environ. Biotechnol.
40. Levy SB, Marshall B. 2004. Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med. 10:S122-29
41. Luangtongkum T, Morishita TY, Ison AJ, Huang S, McDermott PF, Zhang Q. 2006. Effect of conventional and organic production practices on the prevalence and antimicrobial resistance of Campylobacter spp. in poultry. Appl. Environ. Microbiol. 72:3600-7
42. Mackie RI, Koike S, Krapac I, Chee-Sanford J, Maxwell S, Aminov RI. 2006. Tetracycline residues and tetracycline resistance genes in groundwater impacted by swine production facilities. Anim. Biotechnol. 17:157-76
43. Martinez S. 2002. Vertical coordination of marketing systems: lessons from the poultry, egg, and pork industries. http://www.ers.usda.gov/ publications/aer807fm.pdf
44. McManus PR, Stockwell VO, Sundin GW, Jones AL. 2002. Antibiotic use in plant agriculture. Annu. Rev. Phytopathol. 40:443-65
45. Mellon M, Benbrook C, Benbrook KL. 2001. Hogging It!: Estimates of Antimicrobial Abuse in Livestock. Cambridge, MA: Union Concerned Sci. Publ.
46. Miller GY, Algozin KA, McNamara PE, Bush EJ. 2003. Productivity and economic effects of antibiotics use for growth promotion in U.S. pork production. J. Agric. Appl. Econ. 35:469-82
47. Nachamkin I. 2000. Campylobacter. Washington, DC: ASM Press
48. Nandi S, Maurer JJ, Hofacre C, Summers AO. 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
49. Nichols GL. 2005. Fly transmission of Campylobacter. Emerg. Infect. Dis. 11:361-64
50. Norstrom M, Hofshagen M, Stavnes T, Schau J, Lassen J, Kruse H. 2006. Antimicrobial resistance in Campylobacter jejuni from humans and broilers in Norway. Epidemiol. Infect. 134:127-30
51. Natl. Res. Counc. 1999. The use of Drugs in Food Animals: Benefits and Risks. Washington: Natl. Acad.
52. Nwosu VC. 2001. Antibiotic resistance with particular reference to soil microorganisms. Res. Microbiol. 152:421-30
53. Ojeniyi AA. 1989. Direct transmission of Escherichia coli from poultry to humans. Epidemiol. Infect. 103:513-22
54. Okeke IN, Laxminarayan R, Bhutta ZA, Duse AG, Jenkins P, et al. 2005. Antimicrobial resistance in developing countries. Part I: recent trends and current status. Lancet. Infect. Dis. 5:481-93
55. Pang Y, Brown B, Steingrube B, Wallace R, Roberts M. 1994. Tetracycline resistance determinants in Mycobacterium and Streptomyces species. Antimicrob. Agents Chemother. 38:1408-12
56. Pop-Vicas AE, D'Agata EM. 2005. The rising influx of multidrug-resistant gram-negative bacilli into a tertiary care hospital. Clin. Infect. Dis. 40:1792-98
57. Power C. 2004. The source and means of spread of avian influenza virus in the Lower Fraser Valley of British Columbia during an outbreak in the winter of 2004; Canadian Food Inspection Agency: Animal Disease Surveillance Unit. http://www.inspection.gc.ca
58. Price LB, Johnson E, Vailes R, Silbergeld E. 2005. Fluoroquinolone- resistant Campylobacter isolates from conventional and antibiotic-free chicken products. Environ. Health Perspect. 113:557-60
59. Price LB, Graham JP, Lackey L, Roess A, Vailes R, Silbergeld EK. 2007. Elevated risk of carrying gentamicin resistant Escherichia coli among US poultry workers. Environ. Health Perspect. 115: doi: 10.1289/ehp. 1991, 2007
60. Rowe-Magnus DA, Guerout AM, Mazel D. 2002. Bacterial resistance evolution by recruitment of superintegron gene cassettes. Mol. Microbiol. 43:1657-69
61. Saenz RA, Hethcote HW, Gray GC. 2006. Confined animal feeding operations as amplifiers of influenza. Vector Borne Zoonotic Dis. 6:338-46
62. Salyers A, Shoemaker NB. 2006. Reservoirs of antibiotic resistance genes. Anim. Biotechnol. 17:137-46
63. Sapkota AR, Ojo KK, Roberts MC, Schwab KJ. 2006. Antibiotic resistance genes in multidrug-resistant Enterococcus spp. and Streptococcus spp. recovered from the indoor air of a large-scale swine-feeding operation. Lett. Appl. Microbiol. 43:534-40
64. Sapkota AR, Lefferts LY, McKenzie S, Walker P. 2007. What do we feed to food production animals? A review of animal feed ingredients and their potential impacts on human health. Environ. Health Perspect. 115:663-70
65. Sarmah AK, Meyer MT, Boxall AB. 2006. A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65:725-59
66. Sato K, Bartlett PC, Saeed MA. 2005. Antimicrobial susceptibility of Escherichia coli isolates from dairy farms using organic vs conventional production methods. J. Am. Vet. Med. Assoc. 226:589-94
67. Simjee S, White DG, Meng J, Wagner DD, Qaiyumi S, et al. 2002. Prevalence of streptogramin resistance genes among Enterococcus isolates recovered from retail meats in the Greater Washington DC area. J. Antimicrob. Chemother. 50:877-82
68. Sivapalasingam S, Friedman CR, Cohen L, Tauxe RV. 2004. Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J. Food Prot. 67:2342-53
69. 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. 340:1525-32
70. Smith DL, Harris AD, Johnson JA, Silbergeld EK, Morris JG Jr. 2002. Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. Proc. Natl. Acad. Sci. USA 99:6434-39
71. Smith DL, Dushoff J, Morris JG. 2005. Agricultural antibiotics and human health. PLoS Med. 2:e232
72. Sorum M, Johnsen PJ, Aasnes B, Rosvoll T, Kruse H, et al. 2006. Prevalence, persistence, and molecular characterization of glycopeptide- resistant enterococci in Norwegian poultry and poultry farmers 3 to 8 years after the ban on avoparcin. Appl. Environ. Microbiol. 72:516-21
73. Stevens DL, Ma Y, Salmi DB, McIndoo E, Wallace RJ, Bryant AE. 2007. Impact of antibiotics on expression of virulence-associated exotoxin genes in methicillin-sensitive and methicillin-resistant Staphylococcus aureus. J. Infect. Dis. 195:202-11
74. Stine OC, Johnson JA, Keefer-Norris A, Perry KL, Tigno J, et al. 2007. Widespread distribution of tetracycline resistance genes in a confined animal feeding facility. Int. J. Antimicrob. Agents 29:348-52
75. Summers AO. 2002. Generally overlooked fundamentals of bacterial genetics and ecology. Clin. Infect. Dis. 34(Suppl. 3):S85-92
76. Summers AO. 2006. Genetic linkage and horizontal gene transfer, the roots of the antibiotic multi-resistance problem. Anim. Biotechnol. 17:125-35
77. Sunde M, Norstrom M. 2006. The prevalence of associations between and conjugal transfer of antibiotic resistance genes in Escherichia coli isolated from Norwegian meat and meat products. J. Antimictrob. Chemother. 58:741-47
78. Tauxe RV. 2002. Emerging foodborne pathogens. Int. J. Food Microbiol. 78:31-41
79. Tenover FC. 2006. Mechanisms of antimicrobial resistance in bacteria. Am. J. Med. 119:S3-10; discussion S62-70
80. Teuber M. 2001. Veterinary use and antibiotic resistance. Curr. Opin. Microbiol. 4:493-99
81. 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. 42:1368-74
82. U.S. Dept. Agric. FY-2005 annual report manure and byproduct utilization national program 206. www.ars.usda.gov/research/programs/ programs.htm?np_code=206&docid=13337
83. Van den Bogaard AE, Stobberingh EE. 1999. Antibiotic usage in animals: impact on bacterial resistance and public health. Drugs 58:589-607
84. Van den Bogaard AE, Stobberingh EE. 2000. Epidemiology of resistance to antibiotics. Links between animals and humans. Int. J. Antimicrob. Agents 14:327-35
85. World Health Org. 2001. WHO global strategy for containment of antimicrobial resistance. http://www.who.int/csr/resources/publications/ drugresist/WHO_CDS_CSR_DRS_2001_2_EN/en/
86. Wright GD. 2007. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat. Rev. Microbiol. 5:175-86
87. Zhang Q, Sahin O, McDermott PF, Payot S. 2006. Fitness of antimicrobial-resistant Campylobacter and Salmonella. Microbes Infect. 8:1972-78