Abstract
The sub-therapeutic use of tylosin in commercial swine operations can produce selective pressure for the development of antibiotic resistant bacteria. When swine manure from such operations is applied on drained agricultural fields, it can lead to transport and dissemination of resistant microorganisms through soils, into tile drainage lines, and ultimately into surface waters. The objective of this study was to investigate the occurrence and transport of tylosin-resistant enterococci from two different tile-drained agricultural fields receiving biennial swine-waste applications during different seasons. Resistance to tylosin in manure, soil, and tile water was investigated by a phenotype-based method and polymerase chain reaction. All enterococci in manure samples obtained from the spring application were resistant to tylosin, whereas 68 % of the total enterococci from the fall application were resistant to tylosin. Average concentrations of total and tylosin-resistant enterococci in soil samples over the two sampling periods were 9.8 × 103 and 7.5 × 103 cfu/g of soil, respectively. Total and tylosin-resistant enterococci concentrations in tile water collected from the two plots were significantly different (P < 0.05) during the spring and fall experiments. In drainage water, the total enterococci peaked at 2.6 × 103 and 5.0 × 103 cfu/100 mL for the fall and spring experiments, respectively, while tylosin-resistant enterococci peaked at 1.4 × 103 and 1.2 × 103 cfu/100 mL for the fall and spring experiments, respectively. Total suspended solid concentrations in tile water were correlated with enterococci concentrations when base flow was present. Seven out of eight macrolide-resistance genes tested were detected (ermA, ermB, ermC, ermF, ermT, ermX, and msrA, but not mefA). Five of these genes (ermB, ermC, ermF, ermT, and msrA) were detected in at least 9 % of the samples. On average, most of the phenotypically resistant isolates (97 %) harbored msrA, while only 10 % contained ermT and 9 % contained ermC. Genes containing ermF and ermB were detected in 78 % and 69 % of resistant isolates, respectively. Only 2 % of the total isolates (n = 4) harbored all five genes. Of the isolates collected from manure, soil, and water samples, 12 % were confirmed as Enterococcus faecalis with 96 % of the confirmed E. faecalis isolates containing multiple resistance genes. The findings from this study are useful to provide baseline information on the export of total and tylosin-resistant enterococci during rainfall events from manured, tile-drained agricultural fields of the Upper Midwestern USA.
Similar content being viewed by others
References
Aarestrup, F. M., & Carstensen, B. (1998). Effect of tylosin used as a growth promoter on the occurrence of macrolide-resistant enterococci and staphylococci in pigs. Microbial Drug Resistance, 4(4), 307–312.
Abu-Ashour, J., Joy, D. M., Lee, H., Whiteley, H. R., & Zelin, S. (1998). Movement of bacteria in unsaturated soil columns with macropores. Transactions of ASAE, 41(4), 1043–1050.
American Public Health Association. (1998). Standard methods for the examination of water and wastewater, 18 ed., Washington, DC, USA.
Auckenthaler, A., Raso, G., & Huggenberger, P. (2002). Particle transport in a karst aquifer: Natural and artificial tracer experiments with bacteria, bacteriophages and microspheres. Water Science and Technology, 46(3), 131–138.
Bakhsh, A., Kanwar, R. S., & Karlen, D. L. (2005). Effects of liquid swine manure applications on NO3-N leaching losses to subsurface drainage water from loamy soils in Iowa. Agriculture Ecosystem and Environment, 109(1–2), 118–128.
Barton, M. D. (2000). Antibiotic use in animal feed and its impact on human health. Nutrition Research Reviews, 13(2), 279–299.
Beven, K., & Germann, P. (1982). Macropores and water flow in soils. Water Resources Research, 18(5), 1311–1325.
Boxall, A. B. A., Blackwell, P., Cavallo, R., Kay, P., & Tolls, J. (2002). The sorption and transport of a sulphonamide antibiotic in soil systems. Toxicology Letters, 131(1–2), 19–28.
Butaye, P., Devriese, L. A., & Haesebrouck, F. (2001). Differences in antibiotic resistance patterns of Enterococcus faecalis and Enterococcus faecium strains isolated from farm and pet animals. Antimicrobial Agents and Chemotheraphy, 45(5), 1374–1378.
Campagnolo, E. R., Johnson, K. R., Karpati, A., Rubin, C. S., Kolpin, D. W., Meyer, M. T., Esteban, J. E., Currier, R. W., Smith, K., Thu, K. M., & McGeehin, M. (2002). Antimicrobial residues in animal waste and water resources proximal to large-scale swine and poultry feeding operations. Science of the Total Environment, 299(1–3), 89–95.
Chee-Sanford, J. C., Aminov, R. I., Krapac, I. J., Garrigues-Jeanjean, N., & Mackie, R. I. (2001). Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities. Applied and Environmental Microbiology, 67(4), 1494–1502.
Chee-Sanford, J. C., Mackie, R. I., Koike, S., Krapac, I. G., Lin, Y. F., Yannarell, A. C., Maxwell, S., & Aminov, R. I. (2009). Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. Journal of Environmental Quality, 38(3), 1086–1108.
Chen, J., Yu, Z. T., Michel, F. C., Wittum, T., & Morrison, M. (2007). Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides-lincosamides-streptogramin B in livestock manure and manure management systems. Applied and Environmental Microbiology, 73(14), 4407–4416.
Cook, M. J., & Baker, J. L. (2001). Bacteria and nutrient transport to the lines shortly after application of large volumes of liquid swine manure. Transactions of ASAE, 44(3), 495–503.
Cromwell, G. L. (2002). Why and how antibiotics are used in swine production. Animal Biotechnology, 13(1), 7–27.
Davies, C. M., Long, J. A., Donald, M., & Ashbolt, N. J. (1995). Survival of fecal microorganisms in marine and freshwater sediments. Applied and Environmental Microbiology, 61(5), 1888–1896.
De Graef, E. M., Decostere, A., De Leener, D., Goossens, H., Baele, M., & Haesebrouck, F. (2007). Prevalence and mechanism of resistance against macrolids, licosamides, and streptogramins among Enterococcus faecium isolates from food-producing animals and hospital patients in Belgium. Microbial Drug Resistance, 13(2), 135–141.
Dolliver, H., & Gupta, S. (2008). Antibiotic losses in leaching and surface runoff from manure-amended agricultural land. Journal of Environmental Quality, 37(3), 1227–1237.
FDA. (2006). Freedom of information summary. Supplemental New Animal Drug Application NADA 013–076. Available at: www.fda.gov/downloads/AnimalVeterinary/Products.
Friend, J. J., & Chan, K. Y. (1995). Influence of cropping on the population of a native earthworm and consequent effects on hydraulic-properties of vertisols. Australian Journal of Soil Research, 33(6), 995–1006.
Gagliardi, J. V., & Karns, J. S. (2000). Leaching of Escherichia coli O157:H7 in diverse soils under various agricultural management practices. Applied and Environmental Microbiology, 66(3), 877–883.
Graham, J. P., Price, L. B., Evans, S. L., Graczyk, T. K., & Silbergeld, E. K. (2009). Antibiotic resistant enterococci and staphylococci isolated from flies collected near confined poultry feeding operations. Science of the Total Environment, 407(8), 2701–2710.
Guber, A. K., Shelton, D. R., & Pachepsky, Y. A. (2005). Transport and retention of manure-borne coliforms in soil. Vadose Zone Journal, 4(3), 828–837.
Harris, G. L., Nicholls, P. H., Bailey, S. W., Howse, K. R., & Mason, D. J. (1994). Factors influencing the loss of pesticides in drainage from a cracking clay soil. Journal of Hydrology, 159(1–4), 235–253.
Jackson, C. R., Fedorka-Cray, P. J., Barrett, J. B., & Ladely, S. R. (2004a). Effects of tylosin use on erythromycin resistance in enterococci isolated from swine. Applied and Environmental Microbiology, 70(7), 4205–4210.
Jackson, C. R., Fedorka-Cray, P. J., & Barrett. (2004b). Use of a genus- and species-specific multiplex PCR for identification of enterococci. Journal of Clinical Microbiology, 42(8), 3558–3565.
Jensen, L. B., Frimont-Moller, N., & Aarestrup, F. M. (1999). Presence of erm gene classes in gram-positive bacteria of animal and human origin in Denmark. FEMS Microbiology Letters, 170, 151–158.
Jett, B. D., Huycke, M. M., & Gilmore, M. S. (1994). Virulence of enterococci. Clinical Microbiology Reviews, 7(4), 462–478.
Jindal, A., Kocherginskaya, S., Mehboob, A., Robert, M., Mackie, R. I., Raskin, L., & Zilles, J. L. (2006). Antimicrobial use and resistance in swine waste treatment systems. Applied and Environmental Microbiology, 72(12), 7813–7820.
Kanwar, R. S. (2006). Effects of cropping systems on NO3-N losses to tile drain. Journal of the American Water Resources Association, 42(6), 1493–1501.
Kanwar, R. S., Bjorneberg, D., & Baker, D. (1999). An automated system for monitoring the quality and quantity of subsurface drain flow. Journal of Agricultural Engineering Research, 73(2), 123–129.
Kaukas, A., Hinton, M., & Linton, A. H. (1988). The effect of growth-promoting antibiotics on the faecal enterococci of healthy young chickens. Journal of Applied Bacteriology, 64(1), 57–64.
Kay, P., Blackwell, P. A., & Boxall, A. B. (2004). Fate of veterinary antibiotics in a macroporous tile drained clay soil. Environmental Toxicology and Chemistry, 23(5), 1136–1144.
Koike, S., Krapac, I. G., Oliver, H. D., Yannarell, A. C., Chee-Sanford, J. C., Aminov, R. I., & Mackie, R. I. (2007). Monitoring and source tracking of tetracycline resistance genes in lagoons and groundwater adjacent to swine production facilities over a 3-year period. Applied and Environmental Microbiology, 73(15), 4813–4823.
Kumar, K., Thompson, A., Singh, A. K., Chander, Y., & Gupta, S. C. (2004). Enzyme–linked immunosorbent assay for ultratrace determination of antibiotics in aqueous samples. Journal of Environmental Quality, 33, 250–256.
Leclercq, R. (2002). Mechanisms of resistance to macrolides and lincosamides: Nature of the resistance elements and their clinical implications. Clinical Infectious Diseases, 34(4), 482–492.
Luna, V. A., Coates, P., Eady, E. A., Cove, J. H., Nguyen, T. T., & Roberts, M. C. (1999). A variety of gram-positive bacteria carry mobile mef genes. Journal of Antimicrobial Chemotherapy, 44(1), 19–25.
Mackie, R. I., Koike, S., Krapac, I., Chee-Sanford, J., Maxwell, S., & Aminov, R. I. (2006). Tetracycline residues and tetracycline resistance genes in groundwater impacted by swine production facilities. Animal Biotechnology, 17(2), 157–176.
Ma, L., Malong, R. W., Heilman, P., Karlen, D. L., Kanwar, R. S., Cambardella, C. A., Saseendran, S. A., & Ahuja, L. R. (2007). RZWQM simulation of long-term crop production, water and nitrogen balances in Northeast Iowa. Geoderma, 140(3), 247–259.
McIntosh, G., & Sharratt, B. S. (2003). Over winter stability and hydrology of various size macropores in the northern US corn belt. Soil Science, 168(5), 338–346.
NARMS. (2005). 2002 NARMS Retail Meat Annual Report - Enterococcus. Available at www.fda.gov.
Oliveira, A. J., & Pinhata, J. M. (2008). Antimicrobial resistance and species composition of Enterococcus spp. isolated from waters and sands of marine recreational beaches in Southeastern Brazil. Water Research, 42(8–9), 2242–2250.
Onan, L. J., & LaPara, T. M. (2003). Tylosin-resistant bacteria cultivated from agricultural soil. FEMS Microbiology Letters, 220(1), 15–20.
Portillo, A., Ruiz-Larrea, F., Zarazaga, M., Alonso, A., Martinez, J. L., & Torres, C. (2000). Macrolide resistance genes in Enterococcus spp. Antimicrobial Agents and Chemotherapy, 44(4), 967–971.
Roberts, M. C., Sutcliffe, J., Courvalin, P., Jensen, L. B., Rood, J., & Seppala, H. (1999). Nomenclature for macrolide and macrolide-lincosamide-streptogramin B resistance determinants. Antimicrobial Agents and Chemotherapy, 43(12), 2823–2830.
Rysz, M., & Alvarez, P. J. (2006). Transport of antibiotic-resistant bacteria and resistance-carrying plasmids through porous media. Water Science and Technology, 54(11–12), 363–370.
Sapkota, A. R., Curriero, F. C., Gibson, K. E., & Schwab, K. J. (2007). Antibiotic-resistant enterococci and fecal indicators in surface water and groundwater impacted by a concentrated swine feeding operation. Environmental Health Perspectives, 115(7), 1040–1045.
Salyers, A. A., & Amabile-Cuevas, C. F. (1997). Why are antibiotic resistance genes so resistant to elimination? Antimicrobial Agents and Chemotherapy, 41(11), 2321–2325.
Shea, K. M. (2003). Antibiotic resistance: What is the impact of agricultural uses of antibiotics on children’s health? Pediatrics, 112(1), 253–258.
Sherer, B. M., Miner, J. R., Moore, J. A., & Buckhouse, J. C. (1992). Indicator bacterial survival in stream sediments. Journal of Environmental Quality, 21(4), 591–595.
Shipitalo, M. J., & Gibbs, F. (2000). Potential of earthworm burrows to transmit injected animal wastes to tile drains. Soil Science Society of America Journal, 64(6), 2103–2109.
Snow, D.D., Cassada, D.A., Monson, S.J., Zhu, J., Spalding, R.F., (2003). Tetracycline and macrolide antibiotics. Liquid cChromatography/mass spectrometry, MS/MS and time of flight MS. American Chemical Society. pp. 161–174.
Soupir, M. L., Mostaghimi, S., Yagow, E. R., Hagedorn, C., & Vaughan, D. H. (2006). Transport of fecal bacteria from poultry litter and cattle manures applied to pastureland. Water, Air, and Soil Pollution, 169(1–4), 125–136.
Soupir, M. L., Mostaghimi, S., & Dillaha, T. (2010). Attachment of Escherichia coli and enterococci to particles in runoff. Journal of Environmental Quality, 39(3), 1019–1027.
Sutcliffe, J., Grebe, T., Tait-Kamradt, A., & Wondrack, L. (1996a). Detection of erythromycin-resistant determinants by PCR. Antimicrobial Agents and Chemotherapy, 40(11), 2562–2566.
Sutcliffe, J., Tait-Kamradt, A., & Wondrack, L. (1996b). Streptococcus pneumoniae and Streptococcus pyogenes resistant to macrolides but sensitive to clindamycin: A common resistance pattern mediated by an efflux system. Antimicrobial Agents and Chemotherapy, 40(8), 1817–1824.
Thal, L. A., Chow, J. W., Mahayni, R., Bonilla, H., Perri, M. B., Donabedian, S. A., Silverman, J., Taber, S., & Zervos, M. J. (1995). Characterization of antimicrobial resistance in enterococci of animal origin. Antimicrobial Agents and Chemotherapy, 39(9), 2112–2115.
Unc, A., & Goss, M. J. (2004). Transport of bacteria from manure and protection of water resources. Applied Soil Ecology, 25(1), 1–18.
USDA. (2009). 2007 Census of agriculture. United States Department of Agriculture, Washington, DC
USDA, NRCS. (1995). Soil survey of Floyd County. Iowa: United States Department of Agriculture and National Resources Conservation Service.
USEPA. (1986). Ambient water quality criteria for bacteria—1986. U.S. Environmental Protection Agency, Washington, DC
USEPA. (1999). Standard operating procedure for the analysis of residue, non-filterable. (suspended solids), water, method 160.2 NS (gravimetric, 103–105 °C). U.S. Environmental Protection Agency, Washington, DC
USEPA. (2002). Method 1600: Membrane filter test method for enterococci in water. U.S. Environmental Protection Agency, Washington, DC
Warnemuende, E. A., & Kanwar, R. S. (2002). Effects of swine manure application on bacterial quality of leachate from intact soil columns. Transactions of ASAE, 45(6), 1849–1857.
Watkinson, A. J., Micalizzi, G. B., Graham, G. M., Bates, J. B., & Costanzo, S. D. (2007). Antibiotic-resistant Escherichia coli in wastewaters, surface waters, and oysters from an urban riverine system. Applied and Environmental Microbiology, 73(17), 5667–5670.
Weisblum, B. (1995). Erythromycin resistance by ribosome modification. Antimicrobial Agents and Chemotherapy, 39(3), 577–585.
Zucker, L. A., & Brown, C. (1998). Agricultural drainage: Water quality and subsurface drainage studies in the Midwest. Ohio State University Extension Bulletin, 871, 1–40.
Acknowledgments
This research was partially supported by Iowa State University and through a multi-university USDA-NRI grant on the Role of Directly Connected Macropores in Pathogen Transport to Subsurface Drainage and Iowa State University. We thank Dr. Kanwar and his research group for allowing us to collect samples during their experiments and Dr. Thomas Moorman and Dr. Laura Jarboe for their support and contribution to our study. Special thanks to Christina Goeddel, Pramod Pandey, and Martha Zwonitzer for assistance with field experiments, sample collection, and sample analysis.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hoang, T.T.T., Soupir, M.L., Liu, P. et al. Occurrence of Tylosin-Resistant Enterococci in Swine Manure and Tile Drainage Systems under No-Till Management. Water Air Soil Pollut 224, 1754 (2013). https://doi.org/10.1007/s11270-013-1754-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-013-1754-3