Skip to main content
SpringerLink
Log in

Antibiotic Resistance in Airborne Bacteria Near Conventional and Organic Beef Cattle Farms in California, USA

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

An Erratum to this article was published on 05 September 2016

Abstract

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alali, W. Q., Thakur, S., Berghaus, R. D., Martin, M. P., & Gebreyes, W. A. (2010). Prevalence and distribution of salmonella in organic and conventional broiler poultry farms. Foodborne Pathogens and Disease, 7, 1363–1371.

    Article  CAS  Google Scholar 

  • 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.

  • van den Bogaard, A. E., London, N., Driessen, C., & Stobberingh, E. E. (2001). Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. The Journal of Antimicrobial Chemotherapy, 47, 763–771.

    Article  Google Scholar 

  • van den Bogaard, A. E., Williams, R., London, N., Top, J., & Stobberingh, E. (2002). Antibiotic resistance of faecal enterococci in poultry, poultry farmers and poultry slaughterers. The Journal of Antimicrobial Chemotherapy, 49, 497–505.

    Article  Google Scholar 

  • Brown, M. G., & Balkwill, D. L. (2009). Antibiotic resistance in Bacteria Isolated from the deep terrestrial SUBSURFACE. Microbial Ecology, 57(3), 484–493.

    Article  CAS  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.

    Article  CAS  Google Scholar 

  • Burrows, G. E., Griffin, D. D., Pippin, A., & Harris, K. (1989). A comparison of the routes of administration of erythromycin in cattle. Journal of Veterinary Pharmacology and Therapeutics, 12, 289–295.

    Article  CAS  Google 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.

  • Czekalski, N., Berthold, T., Caucci, S., Egli, A., & Burgmann, H. (2012). Increased levels of multiresistant bacteria and resistance genes after wastewater treatment and their dissemination into Lake Geneva, Switzerland. Frontiers in Microbiology., 3, 1–18.

    Article  Google Scholar 

  • Fahrenfeld, N., Ma, Y., O’Brien, M., & Pruden, A. (2013). Reclaimed water as a reservoir of antibiotic resistance genes: distribution system and irrigation implications. Frontiers in Microbiology, 4, 1–10.

    Article  Google Scholar 

  • Garder, J. L., Moorman, T. B., & Soupir, M. (2014). Transport and persistance of tylosin-resistant enterococci, erm genes, and tylosin in soil and drainage water from fields receiving swine manure. Journal of Environmental Quality, 43, 1484–1493.

    Article  Google Scholar 

  • Gebreyes, W. A., Thakur, S., & Morrow, W. E. (2005). Campylobacter coli: prevalence and antimicrobial resistance in antimicrobial-free (ABF) swine production systems. Journal of Antimicrobial Chemotherapy, 56, 765–768.

    Article  CAS  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.

    CAS  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.

    Article  CAS  Google 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 

  • Graham, D. W., Olicares-Rieumont, S., Knapp, C. W., Lima, L., Werner, D., & Bowen, E. (2011). Antibiotic resistance gene abundances associated with waste discharges to the Almendates River near Havana, Cuba. Environmental Science and Technology, 45(2), 418–424.

    Article  CAS  Google Scholar 

  • Green, C. F., Gibbs, S. G., Tarwater, P. M., Mota, L. C., & Scarpino, P. V. (2006). Bacterial plume emanating from the air surrounding swine confinement operations. Journal of Occupational and Environmental Hygiene, 3, 9–15.

    Article  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.

    Article  CAS  Google Scholar 

  • Heuer, O. E., Pedersen, K., Andersen, J. S., & Madsen, M. (2001). Prevalence and antimicrobial susceptibility of thermophilic Campylobacter in organic and conventional broiler flocks. Letters in Applied Microbiology, 33, 269–274.

    Article  CAS  Google 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.

    Article  CAS  Google Scholar 

  • Huang, J., Hu, H., Tang, F., Li, Y., Lu, S., & Lu, Y. (2011). Inactivation and reactivation of antibiotic-resistant bacteria by chlorination in secondary effluents of a municipal wastewater treatment plant. Water Research, 45, 2775–2781.

    Article  CAS  Google 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.

  • Knapp, C. (2010). Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environmental Science & Technology, 44, 580–587.

    Article  CAS  Google Scholar 

  • Knapp, C., Zhang, W., Sturm, B., & Graham, D. (2010). Differential fate of erythromycin and beta-lactam resistance genes from swine lagoon waste under different aquatic conditions. Environmental Pollution, 158, 1506–1512.

    Article  CAS  Google Scholar 

  • Levy, S. B. (1978). Emergence of antibiotic resistant bacteria in the intestinal flora of farm inhabitants. Journal of Infectious Diseases, 137, 688–690.

    Article  CAS  Google Scholar 

  • Levy, S. B., & Marshall, B. (2004). Antibacterial resistance worldwide: causes, challenges and responses. Nature Medicine, 10(12 Suppl), S122–9.

    Article  CAS  Google Scholar 

  • Ling, A., Pace, N. R., Hernandez, M. T., & LaPara, T. M. (2013). Tetracycline resistance and class 1 Integron genes associated with indoor and outdoor aerosols. Environmental Science & Technology, 47(9), 4046–4052.

    Article  CAS  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.

    Article  CAS  Google 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.

    CAS  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.

  • 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.

  • Negreanu, Y., Pasternak, Z., Jurkevitch, E., & Cytryn, E. (2012). Impact of treated wastewater irrigation on antibiotic resistance in agricultural soils. Environmental Science & Technology, 46, 4800–4808.

    Article  CAS  Google Scholar 

  • Olmstead, J. (2012). How the FDA Fails to Regulate Antibiotics in Ethanol Production, Institute for Agriculture and Trade Policy.

  • Price, L. B., Johnson, E., Vailes, R., & Silbergeld, E. (2005). Fluoroquinolone-resistant Campylobacter isolates from conventional and antibiotic-free chicken products. Environmental Health Perspectives, 113, 557–560.

    Article  CAS  Google Scholar 

  • Price, L. B., Lackey, L. G., Vailes, R., & Silbergeld, E. (2007). The persistence of fluoroquinolone-resistant Campylobacter in poultry production. Environmental Health Perspectives, 115, 1035–1039.

    Article  CAS  Google Scholar 

  • Pruden, A., Pei, R., Storteboom, H., & Carlson, K. H. (2006). Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environmental Science & Technology, 40, 7445–7450.

    Article  CAS  Google Scholar 

  • Pruden, A., Arabi, M., & Storteboom, H. N. (2012). Correlation between upstream human activities and riverine antibiotic resistance genes. Environmental Science & Technology, 46, 11541–11549.

    Article  CAS  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.

    Article  Google Scholar 

  • Pruden, A. (2014). Balancing water sustainability and public health goals in the face of growing concerns about antibiotic. Environmental Science & Technology, 48, 5–14.

    Article  CAS  Google 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.

    CAS  Google Scholar 

  • Ray, K. A., Warnick, L. D., Mitchell, R. M., Kaneene, J. B., Ruegg, P. L., Wells, S. J., Fossler, C. P., Halbert, W., & May, K. (2006). Antimicrobial susceptibility of Salmonella from organic and conventional dairy farms. Journal of Dairy Science, 89, 2038–2050.

    Article  CAS  Google Scholar 

  • Reinstein, S., Fox, J. T., Shi, X., Alam, M. J., Renter, G., & Nagaraja, T. G. (2009). Prevalence of Escherichia coli O157:H7 in organically and naturally raised beef cattle. Applied and Environmental Microbiology, 75, 5421–5423.

    Article  CAS  Google Scholar 

  • Rule, A. M., Evans, S. L., & Silbergeld, E. K. (2008). Food animal transport: a potential source of community exposures to health hazards from industrial farming (CAFOs). Journal of Infection and Public Health, 1, 33–39.

    Article  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.

  • Sato, K., Bartlett, P. C., & Saeed, M. A. (2006). Antimicrobial susceptibility of Escherichia coli isolates from dairy farms using organic versus conventional production methods. Journal of the American Veterinary Medical Association, 226, 589–594.

    Article  Google Scholar 

  • Schnoor, J. L. (2014). Re-emergence of emerging contaminants. Environmental Science & Technology, 48(19), 11019–11020.

    Article  CAS  Google Scholar 

  • Schwartz, T., Kohnen, W., Jansen, B., & Obst, U. (2003). Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiology Ecology, 43, 325–335.

    Article  CAS  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.

    Article  CAS  Google Scholar 

  • Silbergeld, E. E., Graham, J., & Price, L. B. (2008). Industrial food animal production, antimicrobial resistance, and human health. Annual Review of Public Health, 29, 151–169.

    Article  Google Scholar 

  • Stoll, C., Sidhu, J. P. S., Tiehm, A., & Toze, S. (2012). Prevalence of clinically relevant antibiotic resistance genes in surface water samples collected from Germany and Australia. Environmental Science & Technology, 46, 9716–9726.

    Article  CAS  Google Scholar 

  • Storteboom, H., Arabi, M., Davis, J. D., Crimi, B., & Pruden, A. (2010). Tracking antibiotic resistance genes in the south platte river basin using molecular signatures of urban, agricultural, and pristine sources. Environmental Science & Technology, 44, 7397–7404.

    Article  CAS  Google Scholar 

  • Su, H. C., Pan, C. G., Ying, G. G., Zhao, J. L., Zhou, L. J., Liu, Y. S., Tao, R., Zhang, R. Q., & He, L. Y. (2014). Contamination profiles of antibiotic resistance genes in the sediments at a catchment scale. The Science of the Total Environment, 490, 708–714.

    Article  CAS  Google Scholar 

  • USDA National Organic Program; National Archives and Records Administration (2012a). Title 7: Agriculture.

  • 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.

    Article  CAS  Google Scholar 

  • Woolhouse, M., & Farrar, J. (2014). An intergovernmental panel on antimicrobial resistance. Nature, 509, 555–557.

    Article  Google Scholar 

  • Xu, Y., Yu, W., Ma, Q., & Zhou, H. (2015). Occurrence of (fluoro)quinolones and (fluoro)quinolone resistance in soil receiving swine manure for 11 years. Science of the Total Environment, 530–531, 191–197.

    Article  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Department of Civil and Environmental Engineering, University of California Los Angeles, Los Angeles, CA, 90095, USA

    Cristina Echeverria, Vanessa Thulsiraj, Amy Zimmer-Faust, Ariel Flores, Madeleine Laitz, Gregory Healy, Shaily Mahendra, Suzanne E. Paulson, Yifang Zhu & Jennifer A. Jay

Authors
  1. Helen M. Sancheza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cristina Echeverria
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vanessa Thulsiraj
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Amy Zimmer-Faust
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ariel Flores
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Madeleine Laitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gregory Healy
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shaily Mahendra
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Suzanne E. Paulson
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yifang Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jennifer A. Jay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jennifer A. Jay.

Ethics declarations

Conflict of Interest

The authors declare that they no conflict of interest.

Additional information

An erratum to this article can be found at http://dx.doi.org/10.1007/s11270-016-3072-z.

Electronic supplementary material

Supporting Information will include the following: Meteorological data for conventional sites and organic sites, the primer sequences and qPCR reaction conditions used in the study, and a schematic illustration of the high-throughput method.

ESM 1

(PDF 253 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sancheza, H.M., Echeverria, C., Thulsiraj, V. et al. Antibiotic Resistance in Airborne Bacteria Near Conventional and Organic Beef Cattle Farms in California, USA. Water Air Soil Pollut 227, 280 (2016). https://doi.org/10.1007/s11270-016-2979-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-016-2979-8

Keywords

Search

Navigation