Environmental Science and Pollution Research

, Volume 22, Issue 9, pp 6932–6940 | Cite as

Occurrence of sulfonamide-, tetracycline-, plasmid-mediated quinolone- and macrolide-resistance genes in livestock feedlots in Northern China

  • Quanhua Mu
  • Jin Li
  • Yingxue Sun
  • Daqing Mao
  • Qing Wang
  • Yi Luo
Research Article


Antibiotic resistance genes (ARGs) in livestock feedlots deserve attention because they are prone to transfer to human pathogens and thus pose threats to human health. In this study, the occurrence of 21 ARGs, including tetracycline (tet)-, sulfonamide (sul)-, plasmid-mediated quinolone (PMQR)- and macrolide-resistance (erm) genes were investigated in feces and adjacent soils from chicken, swine, and cattle feedlots in Northern China. PMQR and sul ARGs were the most prevalent and account for over 90.0 % of the total ARGs in fecal samples. Specifically, PMQR genes were the most prevalent, accounting for 59.6 % of the total ARGs, followed by sul ARGs (34.2 %). The percentage of tet ARGs was 3.4 %, and erm ARGs accounted for only 1.9 %. Prevalence of PMQR and sul ARGs was also found in swine and cattle feces. The overall trend of ARG concentrations in feces of different feeding animals was chicken > swine > beef cattle in the studied area. In soils, sul ARGs had the highest concentration and account for 71.1 to 80.2 % of the total ARGs, which is possibly due to the widely distributed molecular carriers (i.e., class one integrons), facilitating sul ARG propagation. Overall, this study provides integrated profiles of various types of ARGs in livestock feedlots and thus provides a reference for the management of antibiotic use in livestock farming.


Antibiotic resistance genes Livestock farming Antibiotics 



This work was supported by the National Natural Science Foundation of China (Grant Nos. 31270542, 21037002, and 21277075), the State Environmental Protection Commonweal Project (201309031), and the Ministry of Education Program for New Century Excellent Talents (NCET-11-0254). The authors owe sincere appreciation to Dr. Fengxia Yang, Dr. Shuai Yu, and Dr. Kangxin He for their kind instructions during the experiments. Special thanks to Dr. Su Chen for providing some of the manure and soil samples.

Conflict of interest

The authors declare no competing financial interests.

Supplementary material

11356_2014_3905_MOESM1_ESM.doc (230 kb)
ESM 1 (DOC 230 kb)


  1. Aarestrup F (2012) Sustainable farming: get pigs off antibiotics. Nature 486(7404):465–466CrossRefGoogle Scholar
  2. Agersø Y, Wulff G, Vaclavik E, Halling-Sørensen B, Jensen LB (2006) Effect of tetracycline residues in pig manure slurry on tetracycline-resistant bacteria and resistance gene tet (M) in soil microcosms. Environ Int 32(7):876–882CrossRefGoogle Scholar
  3. Aminov R, Garrigues-Jeanjean N, Mackie R (2001) Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl Environ Microbiol 67:22–32CrossRefGoogle Scholar
  4. Aminov R, Chee-Sanford J, Garrigues N, Teferedegne B, Krapac I, White B, Mackie R (2002) Development, validation, and application of PCR primers for detection of tetracycline efflux genes of gram-negative bacteria. Appl Environ Microbiol 68(4):1786–1793CrossRefGoogle Scholar
  5. Campagnolo ERJK, Karpati A, Rubin CS, Kolpin DW, Meyer MT (2002) Antimicrobial residues in animal waste and water resources proximal to large-scale swine and poultry feeding operations. Sci Total Environ 299(1–3):89–95CrossRefGoogle Scholar
  6. Cattoir V, Poirel L, Rotimi V, Soussy C-J, Nordmann P (2007) Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 60:394–397CrossRefGoogle Scholar
  7. Cavaco L, Hasman H, Xia S, Aarestrup FM (2009) qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother 53:603–608CrossRefGoogle Scholar
  8. Chen J, Yu Z, Michel FC, 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. Appl Environ Microbiol 73(14):4407–4416CrossRefGoogle Scholar
  9. Chen J, Michel FC, Sreevatsan S, Morrison M, Yu Z (2010) Occurrence and persistence of erythromycin resistance genes (erm) and tetracycline resistance genes (tet) in waste treatment systems on swine farms. Microb Ecol 60(3):479–486CrossRefGoogle Scholar
  10. Cheng W, Chen H, Su C, Yan S (2013) Abundance and persistence of antibiotic resistance genes in livestock farms: a comprehensive investigation in eastern China. Environ Int 61:1–7CrossRefGoogle Scholar
  11. Hansen LH, Jensen LB, Sørensen HI, Sørensen SJ (2007) Substrate specificity of the OqxAB multidrug resistance pump in Escherichia coli and selected enteric bacteria. J Antimicrob Chemother 60:145–147. doi: 10.1093/jac/dkm167 CrossRefGoogle Scholar
  12. Heuer H, Focks A, Lamshöft M, Smalla K, Matthies M, Spiteller M (2008) Fate of sulfadiazine administered to pigs and its quantitative effect on the dynamics of bacterial resistance genes in manure and manured soil. Soil Biol Biochem 40(7):1892–1900CrossRefGoogle Scholar
  13. Heuer H, Schmitt H, Smalla K (2011) Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol 14(3):236–243CrossRefGoogle Scholar
  14. Ji X, Shen Q, Liu F, Ma J, Xu G, Wang Y, Wu M (2012) Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China. J Hazard Mater 235–236:178–185Google Scholar
  15. Khan SJ, Roser DJ, Davies CM, Peters GM, Stuetz RM, Tucker R, Ashbolt NJ (2008) Chemical contaminants in feedlot wastes: concentrations, effects and attenuation. Environ Int 34(6):839–859CrossRefGoogle Scholar
  16. Kim HB, Wang M, Park CH, Kim E-C, Jacoby GA, Hooper DC (2009) oqxAB encoding a multidrug efflux pump in human clinical isolates of Enterobacteriaceae. Antimicrob Agents Chemother 53:3582–3584CrossRefGoogle Scholar
  17. Knapp CW, Engemann CA, Hanson ML, Keen PL, Hall KJ, Graham DW (2008) Indirect evidence of transposon-mediated selection of antibiotic resistance genes in aquatic systems at low-level oxytetracycline exposures. Environ Sci Technol 42(14):5348–5353CrossRefGoogle Scholar
  18. Koike S, Krapac I, Oliver H, Yannarell A, Chee-Sanford J, Aminov R, Mackie R (2007) Monitoring and source tracking of tetracycline resistance genes in lagoons and groundwater adjacent to swine production facilities over a 3-year period. Appl Environ Microbiol 73(15):4813–4823CrossRefGoogle Scholar
  19. Levy SB, FitzGerald GB, Macone AB (1976) Changes in intestinal flora of farm personnel after introduction of a tetracycline-supplemented feed on a farm. N Engl J Med 295:583–588. doi: 10.1056/NEJM197609092951103 CrossRefGoogle Scholar
  20. Li J, Wang T, Shao B, Shen J, Wang S, Wu Y (2012) Plasmid-mediated quinolone resistance genes and antibiotic residues in wastewater and soil adjacent to swine feedlots: potential transfer to agricultural lands. Environ Health Perspect 120(8):1144–1149CrossRefGoogle Scholar
  21. Li L et al (2013) Spread of oqxAB in Salmonella enterica serotype Typhimurium predominantly by IncHI2 plasmids. J Antimicrob Chemother 68:2263–2268Google Scholar
  22. Liu BT et al. (2013) Dissemination and characterization of plasmids carrying oqxAB-blaCTX-M genes in Escherichia coli isolates from food-producing animals. PloS one 8:e73947Google Scholar
  23. Luo Y, Mao D, Rysz M, Zhou Q, Zhang H, Xu L, Alvarez JJP (2010) Trends in antibiotic resistance genes occurrence in the Haihe River, China. Environ Sci Technol 44(19):7220–7225CrossRefGoogle Scholar
  24. Luo Y, Xu L, Rysz M, Wang Y, Zhang H, Alvarez PJJ (2011) Occurrence and transport of tetracycline, sulfonamide, quinolone, and macrolide antibiotics in the Haihe River Basin, China. Environ Sci Technol 45(5):1827–1833CrossRefGoogle Scholar
  25. Luo Y, Wang Q, Lu Q, Mu Q, Mao D (2014) Ionic liquid facilitates the proliferation of antibiotic resistance genes mediated by class i integrons. Environ Sci Technol Lett 1(5):266–270CrossRefGoogle Scholar
  26. McKinney CW, Loftin KA, Meyer MT, Davis JG, Pruden A (2010) Tet and sul antibiotic resistance genes in livestock lagoons of various operation type, configuration, and antibiotic occurrence. Environ Sci Technol 44(16):6102–6109CrossRefGoogle Scholar
  27. Ministry of Agriculture (2003) Pollution-free food: application guideline of veterinary drug in broiler chicken breeding; NY-5035-2001. Ministry of Agriculture, BeijingGoogle Scholar
  28. Peak N, Knapp CW, Yang RK, Hanfelt MM, Smith MS, Aga DS, Graham DW (2007) Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environ Microbiol 9(1):143–151CrossRefGoogle Scholar
  29. Price LB, Lackey LG, Vailes R, Silbergeld E (2007) The persistence of fluoroquinolone-resistant Campylobacter in poultry production. Environ Health Perspect 115(7):1035CrossRefGoogle Scholar
  30. Pruden A, Pei R, Storteboom H, Carlson KH (2006) Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ Sci Technol 40(23):7445–7450CrossRefGoogle Scholar
  31. Qu A et al (2008) Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. Plos One 3:e2945. doi: 10.1371/journal.pone.0002945 CrossRefGoogle Scholar
  32. Sengeløv G, Agersø Y, Halling-Sørensen B, Baloda SB, Andersen JS, Jensen LB (2003) Bacterial antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry. Environ Int 28(7):587–595CrossRefGoogle Scholar
  33. Sørensen AH, Hansen LH, Johannesen E, Sørensen SJ (2003) Conjugative plasmid conferring resistance to olaquindox. Antimicrob Agents and Chemother 47:798-799 doi: 10.1128/aac.47.2.798-799.2003
  34. Wu N, Qiao M, Zhang B, Cheng WD, Zhu YG (2010) Abundance and diversity of tetracycline resistance genes in soils adjacent to representative swine feedlots in China. Environ Sci Technol 44(18):6933–6939CrossRefGoogle Scholar
  35. Xia L-N et al (2010) A survey of plasmid-mediated fluoroquinolone resistance genes from Escherichia coli isolates and their dissemination in Shandong, China. Foodborne Pathog Dis 7:207–215CrossRefGoogle Scholar
  36. Yu Z, Morrison M (2004) Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotech 36(5):808–813Google Scholar
  37. Zhang XX, Zhang T (2011) Occurrence, abundance, and diversity of tetracycline resistance genes in 15 sewage treatment plants across China and other global locations. Environ Sci Technol 45(7):2598–2604CrossRefGoogle Scholar
  38. Zhao J et al (2010a) Prevalence and dissemination of oqxAB in Escherichia coli isolates from animals, farmworkers, and the environment. Antimicrob Agents Chemother 54:4219–4224CrossRefGoogle Scholar
  39. Zhao L, Dong YH, Wang H (2010b) Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Sci Total Environ 408(5):1069–1075CrossRefGoogle Scholar
  40. Zhou LJ, Ying GG, Zhao JL, Yang JF, Wang L, Yang B, Liu S (2011) Trends in the occurrence of human and veterinary antibiotics in the sediments of the Yellow River, Hai River and Liao River in northern China. Environ Pollut 159(7):1877–1885CrossRefGoogle Scholar
  41. Zhu YG et al (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci U S A 110(9):3435–344CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Key Laboratory of Pollution Processes and Environmental Criteria (Ministry of Education), College of Environmental Science and EngineeringNankai UniversityTianjinChina
  2. 2.Collage of Environmental Science and EngineeringTianjin UniversityTianjinChina

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