Antibiotic Resistance in Airborne Bacteria Near Conventional and Organic Beef Cattle Farms in California, USA
- 863 Downloads
Levels of antibiotic resistance genes (ARGs) and the fractions of antibiotic resistant bacteria (ARB) among culturable heterotrophic bacteria were compared in outdoor air near conventional (n = 3) and organic (n = 3) cattle rearing facilities. DNA extracts from filters taken from 18 locations were analyzed by quantitative polymerase chain reaction (qPCR) for five ARGs. At the reference (non-agricultural) site, all genes were below detection. ARGs sul1, bla SHV, erm(B), and bla TEM were more frequently detected and at higher levels (up to 870 copies m−3 for bla SHV and 750 copies m−3 for sul1) near conventional farms compared to organic locations while the opposite was observed for erm(F) (up to 210 copies m−3). Isolates of airborne heterotrophic bacteria (n = 1295) collected from the sites were tested for growth in the presence of six antibiotics. By disk diffusion on a subset of isolates, the fractions of ARB were higher for conventional sites compared to organic farms for penicillin (0.9 versus 0.63), cloxacillin (0.74 versus 0.23), cefoperazone (0.58 versus 0.14), and sulfamethazine (0.50 versus 0.33) for isolates on nutrient agar. All isolates’ ΔA600pres/ΔA600abs were measured for each of the six tested antibiotics; isolates from farms downwind of organic sites had a lower average ΔA600pres/ΔA600abs for most antibiotics. In general, all three analyses used to indicate microbial resistance to antibiotics showed increases in air samples nearby conventional versus organic cattle rearing facilities. Regular surveillance of airborne ARB and ARGs near conventional and organic beef cattle farms is suggested.
KeywordsAntibiotic resistance Organic Conventional Air ARGs Cattle
This material is based upon research performed in a renovated collaboratory by the National Science Foundation under Grant No. 0963183, which is an award funded under the American Recovery and Reinvestment Act of 2009 (ARRA). We are grateful to Winston Lee, Karmina Padgett, Elizabeth Roswell, Cindy Xiong, and Alicia Amundson. Funding was provided by the Natural Resources Defense Fund and the Institute of the Environment and Sustainability at UCLA.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they no conflict of interest.
- Antibiotic Resistance Threats in the United States (2013). Centers for Disease Control and Prevention, 2013, www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf.Google Scholar
- Bunner, C. A., Norby, P. C., & Bartlett, T. (2007). Prevalence and pattern of antimicrobial susceptibility in Escherichia coli isolated from pigs reared under antimicrobial-free and conventional production methods. Journal of the American Veterinary Medical Association, 231, 275–283.CrossRefGoogle Scholar
- Chapin, A., Rule, A., Gibson, K., Buckley, T., & Schwab, K. (2005). Airborne multidrug-resistant bacteria isolated from a concentrated swine feeding operation. Environmental Health Perspectives, 113, 137–142.Google Scholar
- Cho, S.-H., Lim, Y. S., & Kang, Y.-H. (2012) Comparison of antimicrobial resistance in escherichia coli strains isolated from healthy poultry and swine farm workers using antibiotics in Korea. Osong Public Health and Research Perspectives, 3, 151–155.Google Scholar
- Ghosh, S., & La Para, T. (2007). The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. International Society for Microbial Ecology Journal, 1, 191–203.Google Scholar
- Gibbs, S. G., Green, C. F., Tarwater, P. M., Mota, L. C., Mena, K. D., & Scarpino, P. V. (2006). Isolation of antibiotic-resistant bacteria from the air plume downwind of a swine confined or concentrated animal feeding operation. Environmental Health Perspectives, 114, 1032–1037.CrossRefGoogle Scholar
- Graham, J. P., Leibler, J. H., Price, L. B., Otte, J. M., Pfeiffer, D. U., Tiensin, T., & Silbergeld, E. K. (2008). The animal-human interface and infectious disease in industrial food animal production: rethinking biosecurity and biocontainment. Public Health Reports, 123, 282–299.Google Scholar
- 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, U.S. Department of Health and Human Services, Food and Drug Administration, (2013). www.fda.gov/downloads/AnimalVeterinary/GuidanceComplianceEnforcement/GuidanceforIndustry/UCM299624.pdf
- Halbert, L. W., Kaneene, J. B., Ruegg, P. M., Warnick, L. D., Wells, S. J., Mansfield, L. S., Foddler, C. P., Campbell, A. M., & Geiger-Zwald, A. M. (2006). Evaluation of antimicrobial susceptibility patterns in Campylobacter spp isolated from dairy cattle and farms managed organically and conventionally in the Midwestern and northeastern United States. JAVMA, 228, 1074–1081.CrossRefGoogle Scholar
- Heuer, H., Solehati, Q., Zimmerling, U., Kleineidam, K., Schloter, M., Muller, T., Focks, A., Thiele-Bruhn, S., & Smalla, K. (2011). Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Applied and Environmental Microbiology, 77, 2527–2530.CrossRefGoogle Scholar
- Huijbers, P.M., Blaak, H., de Jong, M.C.M., Graat, E.A.M., Vandenbroucke-Grauls, C.M.J.E. and Husman, A.M.D.R. (2015). Role of the environment in the transmission of antimicrobial resistance to humans: A review. Envir Sci Technol.Google Scholar
- Luangtongkum, T., Morishita, T., Ison, A., Huang, S., McDermott, P., & Zhang, Q. (2006). Effect of conventional and organic production practices on the prevalence and antimicrobial resistance of Camplobactar spp. in Poultry. Applied and Environmental Microbiology, 72, 3600–3607.CrossRefGoogle Scholar
- Mathew, A. G., Beckmann, M. A., & Saxton, A. M. (2001). A comparison of antibiotic resistance in bacteria isolated from swine herds in which antibiotics were used or excluded. Journal of Swine Health and Production, 9, 125–129.Google Scholar
- McEachran, A. D., Blackwell, B. R., Delton Hanson, J., Wooten, K. J., Mayer, G. D., Cox, S. B., & Smith, P. N. (2015). Antibiotics, bacteria, and antibiotic resistance genes: aerial transport from cattle feed yards via particulate matter. Environmental Health Perspectives, 123(4), 337–343.Google Scholar
- Mellon, M., Benbrook, C., Benbrook, and K.L. (2001). Hogging It: Estimates of Antimicrobial Abuse in Livestock, Union of Concerned Scientists Publications, Cambridge, MA.Google Scholar
- Millman, J. M., Waits, K., Grande, H., Marks, A. R., Marks, J. C., Price, L. B., & Hungate, B. A. (2013). Prevalence of antibiotic-resistant E. coli in retail chicken: comparing conventional, organic, kosher, and raised without antibiotics. F1000 Research, 2, 155–165.Google Scholar
- Miranda, J. M., Mondragón, A., Vázquez, B. I., Fente, C. A., Cepeda, A., & Franco, C. M. (2009) Influence of farming methods on microbiological contamination and prevalence of resistance to antimicrobial drugs in isolates from beef. Meat Science, 82, 284–288.Google Scholar
- Olmstead, J. (2012). How the FDA Fails to Regulate Antibiotics in Ethanol Production, Institute for Agriculture and Trade Policy.Google Scholar
- Pruden, A., Larsson, D. G. J., Amezquita, A., Collignon, P., Brandt, K. K., Graham, D. W., Lazorchak, J. R., Suzuki, S., Silley, P., Snape, J. R., Topp, E., Zhang, T., & Zhu, Y. G. (2013). Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environmental Health Perspectives, 121, 1–9.CrossRefGoogle Scholar
- Ramsden, S. J., Ghosh, S., Bohl, L. J., & LaPara, T. M. (2010). Phenotypic and genotypic analysis of bacteria isolated from three municipal wastewater treatment plants on tetracycline-amended and ciprofloxacin-amended growth media. Journal of Applied Microbiology, 109, 1609–1618.Google Scholar
- Sanderson, H., Fricker, C., Brown, R. S., Majury, A., & Liss, S. N. (2016) Antibiotic resistance genes as an emerging environmental contaminant. Environmental Research, 24, 205–218.Google Scholar
- Shanks, O. C., Sivaganesan, M., Peed, L., Kelty, C. A., Blackwood, A. D., Greene, M. R., Noble, R. T., Bushon, R. N., Stelzer, E. A., Kinzelman, J., Ananeva, T., Singalliano, C., Wanless, D., Griffith, J., Cao, Y., Weisberg, S., Harwood, V. J., Staley, C., Oshima, K. H., Varma, M., & Haugland, R. A. (2012). 560 Interlaboratory comparison of real-time PCR protocols for quantification of general fecal 561 indicator bacteria. Environmental Science & Technology, 46, 945–953.CrossRefGoogle Scholar
- USDA National Organic Program; National Archives and Records Administration (2012a). Title 7: Agriculture.Google Scholar
- WHO. Antimicrobial Resistance: Global Report on Surveillance, WHO Press (2014). http://apps.who.int/iris/bitstream/10665/112642/1/9789241564748_eng.pdf.
- Wittwer, M., Keller, J., Wassenaar, R., Stephan, D. H., Regula, G., & Bissig-Choisat, B. (2005). Genetic diversity and antibiotic resistance patterns in a campylobacter population isolated from poultry farms in Switzerland. Applied and Environmental Microbiology, 71, 2840–2847.CrossRefGoogle Scholar