Occurrence of tetracycline residues and antimicrobial resistance in gram negative bacteria isolates from cattle farms in Spain — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Occurrence of tetracycline residues and antimicrobial resistance in gram negative bacteria isolates from cattle farms in Spain
Research Centre in Animal Health, CISA-INIA, Madrid, Spain
,
Research Centre in Animal Health, CISA-INIA, Madrid, Spain
,
Research Centre in Animal Health, CISA-INIA, Madrid, Spain
,
Research Centre in Animal Health, CISA-INIA, Madrid, Spain
,
Research Centre in Animal Health, CISA-INIA, Madrid, Spain
,
National Centre for Environmental Health, Group of Water Pollution, Instituto de Salud Carlos III, Madrid, Spain
,
Research Centre in Animal Health, CISA-INIA, Madrid, Spain
1 Research Centre in Animal Health, CISA-INIA, Madrid, Spain
2 Research Centre in Animal Health, CISA-INIA, Madrid, Spain
3 Research Centre in Animal Health, CISA-INIA, Madrid, Spain
4 Research Centre in Animal Health, CISA-INIA, Madrid, Spain
5 Research Centre in Animal Health, CISA-INIA, Madrid, Spain
6 National Centre for Environmental Health, Group of Water Pollution, Instituto de Salud Carlos III, Madrid, Spain
7 Research Centre in Animal Health, CISA-INIA, Madrid, Spain
The usage of antibiotics in animal husbandry has dramatically increased the concentration of antibiotic residues and has promoted the development and abundance of antibiotic resistance in manure. When it is spread onto agricultural land, both residues of antibiotics and bacteria carrying antibiotic resistance genes may be introduced into the environment. In this research, we isolated resistant gram negative bacteria from manure produced in two dairy and two beef cattle farms, located in Madrid (Spain), to determine their resistance to seventeen representative antibiotics commonly used in veterinary therapy. A total of 63 isolates were used to assess the overall bacterial antimicrobial resistance on cattle manure samples. Predominant species were Escherichia coli and Comamonas testosteroni accounting for 25% and 19.6% of the total, respectively. The most found antimicrobial resistances in gram-negative bacteria were to tetracycline (66.7%), sulphamethoxazole (55.6%), ampicillin (52.4%), cephalothin (46.0%), chloramphenicol (44.4%), nalidixic acid (39.7%) and trimethroprim- sulphamethoxazole (33.3%). The mean of resistance and the percentage of multi-resistant bacteria in beef farms were higher and statistically significant when compared to dairy farms which is opposite from the findings of the previous studies. The presence of three tetracyclines in all manure samples was also examined with stable recoveries (76% - 82%) and high sensitivity (limit of quantification 0.015 - 0.03 μg/kg). The concentrations of tetracyclines detected (<0.015 - 10 mg/kg) were consistent to the theoretical tetracycline levels in manure in Spain according to the ex- cretion rate of these antibiotics and the values re-ported in scientific literature in other European coun- tries.
Heuer, H., Schimitt, H. and Small, K. (2011) Antibiotic resistance gene spread due to manure application on agricultural fields. Current Opinion in Microbiology, 14, 236-243. doi:10.1016/j.mib.2011.04.009
Li, Y., Zhang, X., Li, W., et al. (2012) The residues and environmental risks of multiple veterinary antibiotics in animal faeces. Environmental Monitoring and Assessment, 179, 137-153.
Kim, K.R., Owens, G., Kwon, S.I., et al. (2011) Occurrence and environmental fate of veterinary antibiotics in the terrestrial environment. Water, Air, and Soil Pollution, 214, 163-174. doi:10.1007/s11270-010-0412-2
Sarmah, A.K., Meyer, M.T. and Boxall, A.B.A. (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere, 65, 725-759. doi:10.1016/j.chemosphere.2006.03.026
Wei, R., Feng G., Huang, et al. (2011) Occurrence of veterinary antibiotics in animal wastewater around farms in Jiangsu Province, China. Chemosphere, 82, 1408-1414. doi:10.1016/j.chemosphere.2010.11.067
Witte, W. (1998). Medical consequences of antibiotic use in agriculture. Science, 279, 996-997. doi:10.1126/science.279.5353.996
Khachatourians, G.G. (1998) Agricultural use of antibiotics and the evolution and transfer of antibiotic-resistant bacteria. Canadian Medical Association Journal, 159, 1129-1136.
Chee-Sanford, J.C., Mackie, R.I., Koike, S., et al. (2009) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. Journal Environment Quality, 38, 1086-1108. doi:10.2134/jeq2008.0128
Boxall, A.B.A., Fogg, L.A., Kay, P., et al. (2003). Priorisation of veterinary medicines in the UK environment. Toxicology Letters, 142, 207-218. doi:10.1016/S0378-4274(03)00067-5
Capelton, A., Courage, C., Rumsby, P., et al. (2006) Prioritising veterinary medicines according to their potential indirect human exposure and toxicity profiles. Toxicology Letters, 163, 213-223. doi:10.1016/j.toxlet.2005.10.023
Kima Y., Junga, J., Kimb, M., Parkc J., Boxall, A.B.A. and Choi, K. (2008) Prioritizing veterinary pharmaceuticals for aquatic environment in Korea. Environmental Toxicology and Pharmacology, 26, 167-176. doi:10.1016/j.etap.2008.03.006
(1992) DIRECTIVE 92/18/EEC of 20 March 1992 modifying the annex to council directive 81/852/EEC on the approximation of theilaws of Member States relating to analytical, pharmacotoxicological and clinical standards and protocols in respect of the testing of veterinary medicinal products. 1-23.
Binh, C.T.T., Heuer, H., Kaupenjohann, M. and Smalla, K. (2008) Piggery manure used for soil fertilization is a reservoir for transferable antibiotic resistance plasmids. FEMS Microbiology Ecology, 66, 25-37. doi:10.1111/j.1574-6941.2008.00526.x
H?lzel, C.S., Harms, K.S., Küchenhoff, H., et al. (2010) Phenotypic and genotypic bacterial antimicrobial resistance in liquid pig manure is variously associated with contents of tetracyclines and sulfonamides. Journal Applied Microbiology, 108, 1642-1656. doi:10.1111/j.1365-2672.2009.04570.x
Pan, X., Qiang, Z., Ben, W. and Chen, M. (2011) Residual veterinary antibiotics in swine manure from concentrated animal feeding operations in Shandong Province, China. Chemosphere, 84, 695-700. doi:10.1016/j.chemosphere.2011.03.022
Brooks, J.P., McLaughlin, M.R., Scheffler, B. and Miles, D.M. (2010) Microbial and antibiotic resistant constituents associated with biological aerosols and poultry litter within a commercial poultry house. Science of the Total Environment, 408, 4770-4777. doi:10.1016/j.scitotenv.2010.06.038
Edrington, T.S., Fox, W.E., Callaway, T.R., et al. (2009) Pathogen prevalence and influence of composted dairy manure application on antimicrobial resistance profiles of commensally soil bacteria. Foodborne Pathogenic Diseases, 6, 217-224. doi:10.1089/fpd.2008.0184
Peak, N., Knapp, C.W., Yang, R.K., et al. (2007) Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environmental Microbiology, 9, 143-151. doi:10.1111/j.1462-2920.2006.01123.x
Graham, J.P., Price, L.B., Evans, S.L., Graczyk, T.K. and Silbergeld, E.K. (2009) Antibiotic resistant enterococci and staphylococci isolated from flies collected near confined poultry feeding operations. Science of the Total Environmen, 407, 2701-2710. doi:10.1016/j.scitotenv.2008.11.056
Graves, A.K., Liwimbi, L., Israel, D.W., et al. (2011) Distribution of ten antibiotic resistance genes in E. coli isolates from swine manure, lagoon effluent and soil collected from lagoon waste application field. Folia Microbiology, 56, 131-137.
Walczak, J.J. and Xu, S. (2011) Manure as a source of antibiotic-resistant Escherichia coli and enterococci: A case study of a Wisconsin, USA family dairy farm. Water, Air and Soil Pollution, 219, 579-589. doi:10.1007/s11270-010-0729-x
Barkovskii, A.L. and Bridges, C. (2012) Persistence and profiles of tetracycline resistance genes in swine farms and impact of operational practices on their occurrence in farms vicinities. Water, Air and Soil Pollution, 223, 4962.
Agencia Espa?ola de Medicamentos y Productos Sanitarios (AEMPS) (2011) Datos de ventas de antimicrobianos en Espa?a en el a?o 2009. Ministerio de Sanidad, Politica Social e Igualdad. http://www.aemps.gob.es/informa/notasInformativas/medicamentosVeterinarios/2011/docs/ventas-antimicrobianos_ Espana-2009.pdf
Ministerio Agricultura, Pesca y Alimentación (MAPA) (2007) Libro blanco de subproductos de origen animal no destinados a consume humano (SANDACH). Capitulo VI.-Valorización de los SANCHA, Madrid, ISBN 97884-491-0774-0, 155.
Karczmarczyk, M., Abbott, Y., Walsh, C., Leonard, N. and Fanning, S. (2011) Characterization of multidrug-resistant Escherichia coli isolates from animals presenting at a university veterinary hospital. Applied and Environmental Microbiology, 77, 7104-7112. doi:10.1128/AEM.00599-11
Jacobsen, A.M. and Halling-S?rensen, B. (2006) Multicomponent analysis of tetracyclines, sulfonamides and tylosin in swine manure by liquid chromatography-tandem mass spectrometry. Analytical and Bioanalytical Chemistry, 384, 1164-1174. doi:10.1007/s00216-005-0261-9
Babi?, S., Pavlovi?, D.M., A?perger, D., et al. (2010) Determination of multi-class pharmaceuticals in wastewater by liquid chromatography-tandem mass spectrometry (LCMS-MS). Analytical and Bioanalytical Chemisty, 398, 1185-1194. doi:10.1007/s00216-010-4004-1
U.S. Environmental Protection Agency (2007) US.EPA Method 1694: Pharmaceuticals and Personal Care Products in Water, Soil, Sediment, and Biosolids by HPLC/ MS/MS. EPA-821-R-08-002, Washington.
Bonnedahl, J., Drobni, M., Gauthier-Clerc, M., Hernandez, J., Granholm, S., et al. (2009) Dissemination of Escherichia coli with CTX-M type ESBL between humans and yellow-legged gulls in the south of France. PLoS ONE, 4, e5958. doi:10.1371/journal.pone.0005958
Enne, V.I., Cassar, C., Sprigings, K., Woodward, M.J. and Bennett, P.M. (2008) A high prevalence of antimicrobial resistant Escherichia coli isolated from pigs and a low prevalence of antimicrobial resistant E. coli from cattle and sheep in Great Britain at slaughter. FEMS Microbiology Letters, 278, 193-199. doi:10.1111/j.1574-6968.2007.00991.x
Trisuwan, K., Rukachaisirikul, V., Phongpaichit, S., Preedanon, S. and Sakayaroj, J. (2011) Modiolide and pyrone derivatives from the sea fan-derived fungus Curvularia sp. PSU-F22. Archives of Pharmacal Research, 34, 709-714.
Berge, A.C., Hancock, D.D., Sischo, W.M. and Besser, T.E. (2010) Geographic, farm, and animal factors associated with multiple antimicrobial resistance in fecal Escherichia coli isolates from cattle in the western United States. Journal of the American Veterinary Medical Association, 236, 1338-1344. doi:10.2460/javma.236.12.1338
Davis, M.A., Hancock, D.D., Besser, T.E., Daniels, J.B., Baker, K.N. and Call, D.R. (2007) Antimicrobial resistance in Salmonella enterica serovar Dublin isolates from beef and dairy sources. Veterinary Microbiology, 119, 221-230. doi:10.1016/j.vetmic.2006.08.028
Call, D.R., Davis, M.A. and Sawant, A.A. (2008) Antimicrobial resistance in beef and dairy cattle production. Animal Health Research Reviews, 9, 159-167. doi:10.1017/S1466252308001515
Grave, K., Greko, C., Kvaale, M.K., et al. (2012) Sales of veterinary antibacterial agents in nine European countries during 2005-09: Trends and patterns. Journal of Antimicrobial Chemotherapy, 67, 3001-3008. doi:10.1093/jac/dks298
European Medicines Agency (E.M.A.) (2011) Trends in the sales of veterinary antimicrobial agents in nine European countries (2005-2009). EMA/238630/2011.
Sengel?v, G., Halling-S?rensen, B. and Aarestrup, F.M. (2003) Susceptibility of Escherichia coli and Enterococcus faecium isolated from pigs and broiler chickens to tetracycline degradation products and distribution of tetracycline resistance determinants in E. coli from food animals. Veterinary Microbiology, 95, 91-101. doi:10.1016/S0378-1135(03)00123-8
Ghosh, S. and LaPara, T.M. (2007) The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. The Multidiscilinary Journal of Microbial Ecology, 1, 191-203. doi:10.1038/ismej.2007.31
OK, Y.S., Kim S.C., Kim, K.R., et al. (2011) Monitoring of selected veterinary antibiotics in environmental compartments near a composting facility in Gangwon Province, Korea. Environmental Monitoring Assessment, 174, 693-701.
De la Torre, A., Iglesias, I., Carballo, C., Ramírez, P. and Mu?oz, M.J. (2012) An approach for mapping the vulnerability of European Union soils to antibiotic contamination. Science of the Total Environment, 414, 672-679. doi:10.1016/j.scitotenv.2011.10.032
Du, L. and Liu, W. (2012) Occurrence, fate, and ecotoxicity of antibiotics in agro-ecoystems: A review. Agronomy for Sustainable Development, 32, 309-327. doi:10.1007/s13593-011-0062-9
Winckler, C. and Grafe, A. (2001) Use of veterinary drugs in intensive animal production. Journal of Soils and Sediments, 1, 66-70. doi:10.1007/BF02987711
Aust, M.O., Godlinski, F., Travis, G.R., Hao, X., et al. (2008) Distribution of sulfamethazine, chlortetracycline and tylosin in manure and soil of Canadian feedlots after subtherapeutic use in cattle. Environmental Pollution, 156, 1243-1251. doi:10.1016/j.envpol.2008.03.011
Al-Ahmad, A., Daschner F.D. and Kummerer, K. (1999) Biodegradability of cefotiam, ciprofloxacin, meropenem, penicillin G and sulfamethoxazole and inhibition of waster bacteria. Archives of Environmental Contamination and Toxicology, 37, 158-163. doi:10.1007/s002449900501
Boxall, A.B.A., Kay, P., Blackwell, P.A., Fogg and L.A. (2004). Fate of veterinary medicines applied to soils. In: Kummerer, K., Ed., Pharmaceuticals in the Environment, Springer-Verlag, Berlin, 165-180.
Kummerer, K. and Henninger, A. (2003) Promoting resistance by the emission of antibiotics from hospitals and households into effluent. Clinical Microbiology and Infection, 9, 1203-1214. doi:10.1111/j.1469-0691.2003.00739.x
Jjemba, P.K. (2006) Excretion and ecotoxicity of pharmaceutical and personal care products in the environment. Ecotoxicology and Environmental Safety, 63, 113-130. doi:10.1016/j.ecoenv.2004.11.011
Hamscher, G., Sczesny, S., H?per, H. and Nau, H. (2002) Determination of persistent tetracycline residues in soil fertilized with liquid manure by high-performance liquid chromatography with electrospray ionization tandem mass spectrometry. Analytical Chemistry, 74, 1509-1518. doi:10.1021/ac015588m
Arikan, O.A., Mulbry, W., and Rice, C. (2009) Management of antibiotic residues from agricultural sources: Use of composting to reduce chlortetracycline residues in beef manure from treated animals. Journal of Hazardous Materials, 164, 483-489. doi:10.1016/j.jhazmat.2008.08.019
De Liguoro, M. Cibin, V., Capolongo, F., Halling-Sorensen, H. and Montesina, C. (2003) Use of oxytetracycline and tylosin in intensive calf farming: Evaluation of transfer to manure and soil. Chemosphere, 52, 203-212. doi:10.1016/S0045-6535(03)00284-4
Zhao, L., Dong, H.Y. and Wang, H. (2010) Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Science of the Total Environment, 408, 1069-1075. doi:10.1016/j.scitotenv.2009.11.014
Huang, C.H., Renew, J.E., Smeby, K.L., Pinkston, K. and Sedlak, D.L. (2003) Assessment of potential antibiotic contaminants in water and preliminary occurrence analysis. Water Resources Update, 120, 30-40.