An ecological perspective on U.S. industrial poultry production: The role of anthropogenic ecosystems on the emergence of drug-resistant bacteria from agricultural environments

Current Opinion in Microbiology

Volumn 14, Issue 3, 2011, Pages 244-250

  Davis, Meghan F ^a   Price, Lance B ^b   Liu, Cindy Meng Hsin ^b   Silbergeld, Ellen K ^a  

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

^b TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT;

AGRICULTURAL LAND; ANIMAL PRODUCT; ANTIBIOTIC RESISTANCE; CHICKEN; DRUG USE; ECOLOGY; FOOD INDUSTRY; HOST; HUMAN; MICROBIAL COMMUNITY; MICROBIAL POPULATION DYNAMICS; MICROBIOME; NONHUMAN; POULTRY; REVIEW; UNITED STATES;

ANIMAL HUSBANDRY; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; CHICKENS; DRUG RESISTANCE, BACTERIAL; ECOSYSTEM; HUMANS; UNITED STATES;

ANIMALIA;

EID: 79959294115     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2011.04.003     Document Type: Review

References (65)

1. Muir J. My First Summer in the Sierra 1911, Houghton Mifflin.
2. Loreau M. Linking biodiversity and ecosystems: towards a unifying ecological theory. Philos Trans R Soc Lond, B, Biol Sci 2010, 365:49-60.
3. Jackson W., Piper J. The necessary marriage between ecology and agriculture. Ecology 1989, 70:1091-1993.
4. Tilman D., Cassman K.G., Matson P.A., Naylor R., Polasky S. Agricultural sustainability and intensive production practices. Nature 2002, 418:671-677.
5. Martinez S: Vertical coordination of marketing systems: lessons from the poultry, egg, and pork industries. Electronic Report from the Economic Research Service 2002. Available from http://www.ers.usda.gov/publications/AER807/.
6. De Soet F. Agriculture and the environment. Agric Environ 1974, 1:1-15.
7. Love D.C., Davis M.F., Bassett A., Gunther A., Nachman K.E. Dose imprecision and resistance: free-choice medicated feeds in industrial food animal production in the United States. Environ Health Perspect 2011, 119:279-283.
8. Silbergeld E.K., Graham J., Price L.B. Industrial food animal production, antimicrobial resistance, and human health. Annu Rev Public Health 2008, 29:151-169.
9. Leibler J.H., Otte J., Roland-Holst D., Pfeiffer D.U., Magalhaes R.S., Rushton J., Graham J.P., Silbergeld E.K. Industrial food animal production and global health risks: exploring the ecosystems and economics of avian influenza. EcoHealth 2009, 6:58-70.
10. Martinez J.L. Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 2009, 157:2893-2902.
11. Wright G.D. Antibiotic resistance in the environment: a link to the clinic?. Curr Opin Microbiol 2010, 13:589-594.
12. Wright G.D. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 2007, 5:175-186.
13. Sapkota A.R., Lefferts L.Y., McKenzie S., Walker P. What do we feed to food-production animals? A review of animal feed ingredients and their potential impacts on human health. Environ Health Perspect 2007, 115:663-670.
14. GAO: Concentrated animal feeding operations: EPA needs more information and a clearly defined strategy to protect air and water quality from pollutants of concern. Report to Congressional Requesters 2008, Electronic Report from the United States Government Accountability Office, http://www.gao.gov/products/GAO-08-944.
15. Kellogg RL, Lander CH, Moffitt DC, Gollebon N: Manure nutrients relative to the capacity of cropland and pastureland to assimilate nutrients: spatial and temporal trends for the United States. Electronic Report from the United States Department of Agriculture, the Natural Resources Conservation Service and the Economic Research Service 2000, available from (Publication No. nps00-0579). http://www.nrcs.usda.gov/technical/NRI/pubs/manntr.html.
16. Zhang W., Ricketts T., Kremen C., Carney K., Swinton S. Ecosystem services and dis-services to agriculture. Ecol Econ 2007, 64:253-260.
17. Shennan C. Biotic interactions, ecological knowledge and agriculture. Philos Trans R Soc Lond, B, Biol Sci 2008, 363:717-739.
18. Muir W.M., Wong G.K., Zhang Y., Wang J., Groenen M.A.M., Crooijmans R.P.M.A., Megens H., Zhang H., Okimoto R., Vereijken A., et al. Genome-wide assessment of worldwide chicken SNP genetic diversity indicates significant absence of rare alleles in commercial breeds. Proc Natl Acad Sci USA 2008, 105:17312-17317.
19. Jackson R.W., Johnson L.J., Clarke S.R., Arnold D.L. Bacterial pathogen evolution: breaking news. Trends Genet 2010.
20. Lumpkins B.S., Batal A.B., Lee M.D. Evaluation of the bacterial community and intestinal development of different genetic lines of chickens. Poult Sci 2010, 89:1614-1621.
21. Aminov R.I. The role of antibiotics and antibiotic resistance in nature. Environ Microbiol 2009, 11:2970-2988.
22. Kumar K., Gupta S., Chander Y., Singh A. Antibiotic use in agriculture and its impact on the terrestrial environment. Adv Agron 2005, 87.
23. FDA: Summary report on antimicrobials sold or distributed for use in food-producing animals; section 105 of the Animal Drug User Fee Amendments of 2008 (ADUFA). Electronic Report from the United States Food and Drug Administration, 2010, http://www.fda.gov/AnimalVeterinary/NewsEvents/CVMUpdates/ucm236143.htm.
24. Baurhoo B., Ferket P.R., Zhao X. Effects of diets containing different concentrations of mannanoligosaccharide or antibiotics on growth performance, intestinal development, cecal and litter microbial populations, and carcass parameters of broilers. Poult Sci 2009, 88:2262-2272.
25. Lees P., Concordet D., Aliabadi F.S., Toutain P. Drug selection and optimization of dosage schedules to minimize antimicrobial resistance. Antimicrobial Resistance in Bacteria of Animal Origin 2006, 49-72. ASM Press. F. Aarestrup (Ed.).
26. Smith H.W. Effect of antibiotics on bacterial ecology in animals. Am J Clin Nutr 1970, 23:1472-1479.
27. Starr M.P., Reynolds D.M. Streptomycin resistance of coliform bacteria from turkeys fed streptomycin. Am J Public Health Nations Health 1951, 41:1375-1380.
28. Davies J., Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 2010, 74:417-433.
29. Cody A.J., Colles F.M., Sheppard S.K., Maiden M.C.J. Where does Campylobacter come from? A molecular odyssey. Adv Exp Med Biol 2010, 659:47-56.
30. M'ikanatha N.M., Sandt C.H., Localio A.R., Tewari D., Rankin S.C., Whichard J.M., Altekruse S.F., Lautenbach E., Folster J.P., Russo A., et al. Multidrug-resistant Salmonella isolates from retail chicken meat compared with human clinical isolates. Foodborne Pathog Dis 2010, 7:929-934.
31. Henzler D.J., Opitz H.M. The role of mice in the epizootiology of Salmonella enteritidis infection on chicken layer farms. Avian Dis 1992, 36:625-631.
32. Graham J.P., Price L.B., Evans S.L., Graczyk T.K., Silbergeld E.K. Antibiotic resistant enterococci and staphylococci isolated from flies collected near confined poultry feeding operations. Sci Total Environ 2009, 407:2701-2710.
33. Graham J.P., Nachman K.E. Managing waste from confined animal feeding operations in the United States: the need for sanitary reform. J Water Health 2010, 8:646-670.
34. Baquero F., Martinez J., Canton R. Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 2008, 19:260-265.
35. Chee-Sanford J.C., Mackie R.I., Koike S., Krapac I.G., Lin Y., Yannarell A.C., Maxwell S., Aminov R.I. Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual 2009, 38:1086-1108.
36. Stevens M.P., Humphrey T.J., Maskell D.J. Molecular insights into farm animal and zoonotic Salmonella infections. Philos Trans R Soc B: Biol Sci 2009, 364:2709-2723.
37. Rehman H.U., Vahjen W., Awad W.A., Zentek J. Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broiler chickens. Arch Anim Nutr 2007, 61:319-335.
38. Pedroso A.A., Menten J.F.M., Lambais M.R., Racanicci A.M.C., Longo F.A., Sorbara J.O.B. Intestinal bacterial community and growth performance of chickens fed diets containing antibiotics. Poult Sci 2006, 85:747-752.
39. Qu A., Brulc J.M., Wilson M.K., Law B.F., Theoret J.R., Joens L.A., Konkel M.E., Angly F., Dinsdale E.A., Edwards R.A., et al. Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. PLoS ONE 2008, 3:e2945.
40. Diarra M.S., Rempel H., Champagne J., Masson L., Pritchard J., Topp E. Distribution of antimicrobial resistance and virulence genes in Enterococcus spp. and characterization of isolates from broiler chickens. Appl Environ Microbiol 2010, 76:8033-8043.
41. Bonnet C., Diarrassouba F., Brousseau R., Masson L., Topp E., Diarra M.S. Pathotype and antibiotic resistance gene distributions of Escherichia coli isolates from broiler chickens raised on antimicrobial-supplemented diets. Appl Environ Microbiol 2009, 75:6955-6962.
42. Diarra M.S., Silversides F.G., Diarrassouba F., Pritchard J., Masson L., Brousseau R., Bonnet C., Delaquis P., Bach S., Skura B.J., Topp E. Impact of feed supplementation with antimicrobial agents on growth performance of broiler chickens, Clostridium perfringens and enterococcus counts, and antibiotic resistance phenotypes and distribution of antimicrobial resistance determinants in Escherichia coli isolates. Appl Environ Microbiol 2007, 73:6566-6576.
43. Bunemann E.K., Schwenke G.D., Zwieten L.V. Impact of agricultural inputs on soil organisms - a review. Aust J Soil Res 2006, 44:379-406.
44. Kinney C.A., Furlong E.T., Kolpin D.W., Burkhardt M.R., Zaugg S.D., Werner S.L., Bossio J.P., Benotti M.J. Bioaccumulation of pharmaceuticals and other anthropogenic waste indicators in earthworms from agricultural soil amended with biosolid or swine manure. Environ Sci Technol 2008, 42:1863-1870.
45. Simjee S., Mcdermott P.F., White D.G., Hofacre C., Berghaus R.D., Carter P.J., Stewart L., Liu T., Maier M., Maurer J.J. Antimicrobial susceptibility and distribution of antimicrobial-resistance genes among Enterococcus and coagulase-negative Staphylococcus isolates recovered from poultry litter. Avian Dis 2007, 51:884-892.
46. Furtula V., Farrell E.G., Diarrassouba F., Rempel H., Pritchard J., Diarra M.S. Veterinary pharmaceuticals and antibiotic resistance of Escherichia coli isolates in poultry litter from commercial farms and controlled feeding trials. Poult Sci 2010, 89:180-188.
47. Cressman M.D., Yu Z., Nelson M.C., Moeller S.J., Lilburn M.S., Zerby H.N. Interrelations between the microbiotas in the litter and in the intestines of commercial broiler chickens. Appl Environ Microbiol 2010, 76:6572-6582.
48. Nandi S., Maurer J.J., Hofacre C., Summers A.O. Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter. Proc Natl Acad Sci USA 2004, 101:7118-7122.
49. Price L.B., Lackey L.G., Vailes R., Silbergeld E. The persistence of fluoroquinolone-resistant Campylobacter in poultry production. Environ Health Perspect 2007, 115:1035-1039.
50. Graham J.P., Evans S.L., Price L.B., Silbergeld E.K. Fate of antimicrobial-resistant enterococci and staphylococci and resistance determinants in stored poultry litter. Environ Res 2009, 109:682-689.
51. Singer R.S., Ward M.P., Maldonado G. Can landscape ecology untangle the complexity of antibiotic resistance?. Nat Rev Microbiol 2006, 4:943-952.
52. Leibler J.H., Carone M., Silbergeld E.K. Contribution of company affiliation and social contacts to risk estimates of between-farm transmission of avian influenza. PLoS ONE 2010, 5:e9888.
53. Rule A.M., Evans S.L., Silbergeld E.K. Food animal transport: a potential source of community exposures to health hazards from industrial farming (CAFOs). J Infect Public Health 2008, 1:33-39.
54. Hastings R., Colles F.M., McCarthy N.D., Maiden M.C.J., Sheppard S.K. Campylobacter genotypes from poultry transportation crates indicate a source of contamination and transmission. J Appl Microbiol 2011, 110:266-276.
55. Colles F.M., Mccarthy N.D., Sheppard S.K., Layton R., Maiden M.C.J. Comparison of Campylobacter populations isolated from a free-range broiler flock before and after slaughter. Int J Food Microbiol 2010, 137:259-264.
56. Price L.B., Graham J.P., Lackey L.G., Roess A., Vailes R., Silbergeld E. Elevated risk of carrying gentamicin-resistant Escherichia coli among U.S. poultry workers. Environ Health Perspect 2007, 115:1738-1742.
57. Mulders M.N., Haenen A.P.J., Geenen P.L., Vesseur P.C., Poldervaart E.S., Bosch T., Huijsdens X.W., Hengeveld P.D., Dam-Deisz W.D.C., Graat E.A.M., et al. Prevalence of livestock-associated MRSA in broiler flocks and risk factors for slaughterhouse personnel in The Netherlands. Epidemiol Infect 2010, 138:743-755.
58. McEwen S.A., Prescott J.F., Boerlin P. Antibiotics and poultry - a comment. Can Vet J 2010, 51:561-562.
59. Denis M., Chidaine B., Laisney M., Kempf I., Rivoal K., Megraud F., Fravalo P. Comparison of genetic profiles of Campylobacter strains isolated from poultry, pig and Campylobacter human infections in Brittany, France. Pathol Biol 2009, 57:23-29.
60. Gupta A., Nelson J.M., Barrett T.J., Tauxe R.V., Rossiter S.P., Friedman C.R., Joyce K.W., Smith K.E., Jones T.F., Hawkins M.A., et al. Antimicrobial resistance among Campylobacter strains, United States, 1997-2001. Emerging Infect Dis 2004, 10:1102-1109.
61. Aarestrup F.M., Wegener H.C., Collignon P. Resistance in bacteria of the food chain: epidemiology and control strategies. Expert Rev Anti-infective Ther 2008, 6:733-750.
62. Smith T.C., Pearson N. The Emergence of Staphylococcus aureus ST398. Vector Borne and Zoonotic Diseases 2011, 11:327-339.
63. Bystroń J., Podkowik M., Piasecki T., Wieliczko A., Molenda J., Bania J. Genotypes and enterotoxin gene content of S. aureus isolates from poultry. Veterinary Microbiology 2010, 144:498-501.
64. Paul E., Robertson G. Ecology and the agricultural sciences: a false dichotomy?. Ecology 1989, 70:1594-1597.
65. Peterson A.E., Vegosen L., Leibler J., Davis M.F., Feingold B., Silbergeld E. Emerging infectious diseases and the environment. Determinantes Ambientales y Sociales de la Salud [Environmental and Social Determinants of Health] 2010, PAHO, Washington, DC. S. Henao, J. Finkelman (Eds.).