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Aerobiologia

pp 1–12 | Cite as

A preliminary evaluation of veterinary antibiotics, estrogens, in vitro estrogenic activity and microbial communities in airborne particulate matter collected near dairy production facilities

  • Philip N. SmithEmail author
  • Andrew D. McEachran
  • Kimberly J. Wooten
  • Brett R. Blackwell
Original paper
  • 9 Downloads

Abstract

Particulate matter (PM) emitted from beef cattle feedyards transports manure-affiliated compounds including antibiotics and steroids from feedyards into the surrounding environment. Similarly, commercial dairy operations have the potential to release PM, comprised largely of aerosolized manure, into the surrounding environment along with associated veterinary antibiotics and steroids. The goal of this study was to quantify and compare total suspended particulates, antibiotics and estrogens collected upwind and downwind of dairies in the Southern High Plains, and to characterize microbial community structure and in vitro estrogenic activity of collected PM. PM collected downwind of dairies had greater microbial diversity (as measured by number of operational taxonomic units) and had greater frequencies of detection for antibiotics and estrogens than associated upwind PM. Dominant bacterial phyla and overall microbial community composition were similar among upwind and downwind PM, and extracts of upwind and downwind PM produced no in vitro estrogenic activity. Although this study surveyed a limited number of dairies in the region, these results suggest that dairy operations in the Southern High Plains, in contrast to feedyards, appear to be minor contributors of total aerial PM and associated antibiotics and steroids to the terrestrial environment.

Keywords

PM production Aerial transport Veterinary antibiotics In vitro assay 

Notes

Acknowledgements

This research was supported by a grant from the Texas Tech University College of Arts and Sciences entitled “Next-Gen Sequencing Enhancement” to Philip N. Smith, Greg Mayer, and Stephen B. Cox, and the AT&T Chancellor’s Fellowship (Texas Tech University) to Andrew McEachran. We appreciate the collaborative spirit of Research and Testing Laboratory (Lubbock, TX) and their assistance with pyrosequencing analysis.

References

  1. Alvarez, D. A., Shappell, N. W., Billey, L. O., Bermudez, D. S., Wilson, V. S., Kolpin, D. W., et al. (2013). Bioassay of estrogenicity and chemical analyses of estrogens in streams across the United States associated with livestock operations. Water Research, 47(10), 3347–3363.CrossRefGoogle Scholar
  2. Anderson, J. O., Thundiyil, J. G., & Stolbach, A. (2012). Clearing the air: A review of the effects of particulate matter air pollution on human health. Journal of Medical Toxicology, 8(2), 166–175.CrossRefGoogle Scholar
  3. Anderson, M. J., & Willis, T. J. (2003). Canonical analysis of principal coordinates: A useful method of constrained ordination for ecology. Ecology, 84(2), 511–525.CrossRefGoogle Scholar
  4. Aust, M.-O., Godlinski, F., Travis, G. R., Hao, X., McAllister, T. A., Leinweber, P., et al. (2008). Distribution of sulfamethazine, chlortetracycline and tylosin in manure and soil of Canadian feedlots after subtherapeutic use in cattle. Environmental Pollution, 156(3), 1243–1251.CrossRefGoogle Scholar
  5. Blackwell, B. R., Buser, M. D., Johnson, B. J., Baker, M., Cobb, G. P., & Smith, P. N. (2013). Analysis of veterinary growth promoters in airborne particulate matter by liquid chromatography-tandem mass spectrometry. In G. P. Cobb & P. N. Smith (Eds.), Evaluating veterinary pharmaceutical behavior in the environment (pp. 137–148). Washington, DC: American Chemical Society Division of Environmental Chemistry.CrossRefGoogle Scholar
  6. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5), 335–336.CrossRefGoogle Scholar
  7. Cavallin, J. E., Durhan, E. J., Evans, N., Jensen, K. M., Kahl, M. D., Kolpin, D. W., et al. (2014). Integrated assessment of runoff from livestock farming operations: Analytical chemistry, in vitro bioassays, and in vivo fish exposures. Environmental Toxicology and Chemistry, 33(8), 1849–1857.CrossRefGoogle Scholar
  8. Chee-Sanford, J. C., Mackie, R. I., Koike, S., Krapac, I. G., Lin, Y.-F., Yannarell, A. C., et al. (2009). Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. Journal of Environmental Quality, 38, 1086–1108.CrossRefGoogle Scholar
  9. Demirpence, E., Duchesne, M.-J., Badia, E., Gagne, D., & Pons, M. (1993). MVLN cells: A bioluminescent MCF-7-derived cell line to study the modulation of estrogenic activity. The Journal of Steroid Biochemistry and Molecular Biology, 46(3), 355–364.CrossRefGoogle Scholar
  10. Dowd, S. E., Callaway, T. R., Wolcott, R. D., Sun, Y., McKeehan, T., Hagevoort, R. G., et al. (2008). Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiology, 8, 125.CrossRefGoogle Scholar
  11. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., & Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16), 2194–2200.CrossRefGoogle Scholar
  12. Gadd, J. B., Tremblay, L. A., & Northcott, G. L. (2010). Steroid estrogens, conjugated estrogens and estrogenic activity in farm dairy shed effluents. Environmental Pollution, 158(3), 730–736.CrossRefGoogle Scholar
  13. Garcia, J., Bennett, D. H., Tancredi, D., Schenker, M. B., Mitchell, D., & Mitloehner, F. M. (2013). A survey of particulate matter on California dairy farms. Journal of Environmental Quality, 42(1), 40–47.CrossRefGoogle Scholar
  14. Ghosh, S., & LaPara, T. M. (2007). The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME Journal, 1(3), 191–203.CrossRefGoogle Scholar
  15. Gutendorf, B., & Westendorf, J. (2001). Comparison of an array of in vitro assays for the assessment of the estrogenic potential of natural and synthetic estrogens, phytoestrogens and xenoestrogens. Toxicology, 166(1), 79–89.CrossRefGoogle Scholar
  16. Hanselman, T. A., Graetz, D. A., & Wilkie, A. C. (2003). Manure-borne estrogens as potential environmental contaminants: A review. Environmental Science and Technology, 37(24), 5471–5478.CrossRefGoogle Scholar
  17. Hutchins, S. R., White, M. V., Hudson, F. M., & Fine, D. D. (2007). Analysis of lagoon samples from different concentrated animal feeding operations for estrogens and estrogen conjugates. Environmental Science and Technology, 41(3), 738–744.CrossRefGoogle Scholar
  18. Ivie, G. W., Christopher, R. J., Munger, C. E., & Coppock, C. E. (1986). Fate and residues of [4-C] estradiol-17 after Intramuscular Injection into Holstein Steer calves. Journal of Animal Science, 62(3), 681–690.CrossRefGoogle Scholar
  19. Kim, S. C., & Carlson, K. (2007). Quantification of human and veterinary antibiotics in water and sediment using SPE/LC/MS/MS. Analytical and Bioanalytical Chemistry, 387(4), 1301–1315.CrossRefGoogle Scholar
  20. Levy, S. B., & Marshall, B. (2004). Antibacterial resistance worldwide: Causes, challenges and responses. Nature Medicine, 10(12 SUPPL.), S122–S129.CrossRefGoogle Scholar
  21. Ling, A. L., 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 and Technology, 47(9), 4046–4052.CrossRefGoogle Scholar
  22. Lozupone, C., Hamady, M., & Knight, R. (2006). UniFrac—An online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics, 7, 371.CrossRefGoogle Scholar
  23. McDonald, D., Price, M. N., Goodrich, J., Nawrocki, E. P., DeSantis, T. Z., Probst, A., et al. (2012). An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. The ISME Journal, 6(3), 610–618.CrossRefGoogle Scholar
  24. McEachran, A. D., Blackwell, B. R., Hanson, J. D., Wooten, K. J., Mayer, G. D., Cox, S. B., et al. (2015). Antibiotics, bacteria, and antibiotic resistance genes: Aerial transport from cattle feed yards via particulate matter. Environmental Health Perspectives, 123, 337–343.CrossRefGoogle Scholar
  25. Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., & Wagner, H. (2010). vegan: Community Ecology Package. R package version 1.17-1, 2010. R package version (pp. 1–17).Google Scholar
  26. Purdy, C. W., Clark, R. N., & Straus, D. C. (2007). Analysis of aerosolized particulates of feedyards located in the Southern High Plains of Texas. Aerosol Science and Technology, 41(5), 497–509.CrossRefGoogle Scholar
  27. Purdy, C. W., Clark, R. N., & Straus, D. C. (2009). Ambient and indoor particulate aerosols generated by dairies in the southern High Plains. Journal of Dairy Science, 92(12), 6033–6045.CrossRefGoogle Scholar
  28. Raman, D. R., Williams, E. L., Layton, A. C., Burns, R. T., Easter, J. P., Daugherty, A. S., et al. (2004). Estrogen content of dairy and swine wastes. Environmental Science and Technology, 38(13), 3567–3573.CrossRefGoogle Scholar
  29. Rice, W. C., Galyean, M. L., Cox, S. B., Dowd, S. E., & Cole, N. A. (2012). Influence of wet distillers grains diets on beef cattle fecal bacterial community structure. BMC Microbiology, 12, 25.CrossRefGoogle Scholar
  30. Shappell, N. W., Elder, K. H., & West, M. (2010a). Estrogenicity and nutrient concentration of surface waters surrounding a large confinement dairy operation using best management practices for land application of animal wastes. Environmental Science and Technology, 44(7), 2365–2371.CrossRefGoogle Scholar
  31. Shappell, N. W., Hyndman, K. M., Bartell, S. E., & Schoenfuss, H. L. (2010b). Comparative biological effects and potency of 17α-and 17β-estradiol in fathead minnows. Aquatic Toxicology, 100(1), 1–8.CrossRefGoogle Scholar
  32. Watanabe, N., Harter, T. H., & Bergamaschi, B. A. (2008). Environmental occurrence and shallow ground water detection of the antibiotic monensin from dairy farms. Journal of Environmental Quality, 37(5_Supplement), S-78.CrossRefGoogle Scholar
  33. Wegener, H. C. (2003). Antibiotics in animal feed and their role in resistance development. Current Opinion in Microbiology, 6(5), 439–445.CrossRefGoogle Scholar
  34. Wei, H., Yan-xia, L., Ming, Y., & Wei, L. (2011). Presence and determination of manure-borne estrogens from dairy and beef cattle feeding operations in Northeast China. Bulletin of Environmental Contamination and Toxicology, 86(5), 465–469.CrossRefGoogle Scholar
  35. Wooten, K. J., Blackwell, B. R., McEachran, A. D., Mayer, G. D., & Smith, P. N. (2015). Airborne particulate matter collected near beef cattle feedyards induces androgenic and estrogenic activity in vitro. Agriculture, Ecosystems and Environment, 203, 29–35.CrossRefGoogle Scholar
  36. Zhao, L., Dong, Y. H., & Wang, H. (2010). Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Science of the Total Environment, 408(5), 1069–1075.CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Environmental ToxicologyTexas Tech UniversityLubbockUSA

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