Application of swine manure on agricultural fields contributes to extended- spectrum ß-lactamase producing Escherichia coli spread in Tai'an, China

Frontiers in Microbiology

Volumn 6, Issue MAR, 2015, Pages

  Gao, Lili ^a,b   Hu, Jiaqing ^a,b   Zhang, Xiaodan ^a,b   Wei, Liangmeng ^a,b   Li, Song ^c   Miao, Zengmin ^c   Chai, Tongjie ^a,b  

^a SHANDONG AGRICULTURAL UNIVERSITY   (China)

^b Sino German Cooperative Research Centre for Zoonosis of Animal Origin Shandong Province Key Laboratory of Animal Biotechnology and Disease Control and Prevention of Shandong Province Research Center for Animal Disease Control Engineering of Shandong Province   (China)

^c TAISHAN MEDICAL UNIVERSITY   (China)

Author keywords

Agricultural fields; Animal manure; Antibiotic resistance gene spread; ERIC PCR; ESBL producing E. coli

Indexed keywords

AMIKACIN; AMOXICILLIN; CEFALOTIN; CEFOTAXIME; CEFTIOFUR; CEFTRIAXONE; CHLORAMPHENICOL; CIPROFLOXACIN; EXTENDED SPECTRUM BETA LACTAMASE; FLORFENICOL; GENTAMICIN; IMIPENEM; KANAMYCIN; NALIDIXIC ACID; TETRACYCLINE;

AGAR GEL ELECTROPHORESIS; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIUM ISOLATION; CHINA; CONTROLLED STUDY; CTX M GENE; DISK DIFFUSION; ENTEROBACTERIAL REPETITIVE INTERGENIC CONSENSUS POLYMERASE CHAIN REACTION; ESBL GENE; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING ENTEROBACTERIACEAE; GENE ISOLATION; MANURE; NONHUMAN; PLASMID; POLYMERASE CHAIN REACTION; QUALITY CONTROL; REPLICON; SOIL ANALYSIS; SWINE MANURE;

ANIMALIA; ENTEROBACTERIACEAE; ESCHERICHIA COLI; SUIDAE;

EID: 84927168618     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00313     Document Type: Article

References (51)

1. Agerso, Y., Aarestrup, F.M., Pedersen, K., Seyfarth, A. M., Struve, T., and Hasman, H. (2012). Prevalence of extended-spectrum cephalosporinase (ESC)-producing Escherichia coli in Danish slaughter pigs and retail meat identified by selective enrichment and association with cephalosporin usage. J. Antimicrob. Chemother. 67, 582-8.
2. Allen. H.K. (2014). Antibiotic resistance gene discovery in food-producing animals. Curr. Opin. Microbiol. Jun;19:25-9.
3. Batchelor, M., Hopkins, K., Threlfall, E. J., Clifton-Hadley, F. A., Stallwood, A. D., Davies, R. H., and Liebana, E. (2005). bla(CTX-M) genes in clinical Salmonella isolates recovered from humans in England and Wales from 1992 to 2003. Antimicrob. Agents Chemother. 49, 1319-22.
4. Blaak, H., de Kruijf, P., Hamidjaja, R. A., van Hoek, A. H., de Roda, H. A., and Schets, F. M. (2014). Prevalence and characteristics of ESBL-producing E. coli in Dutch recreational waters influenced by wastewater treatment plants. Vet. Microbiol. 171, 448-59.
5. Bradford, P. A. (2001). Extended-spectrum beta-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin. Microbiol. Rev. 14, 933-51.
6. Carattoli, A., Bertini, A., Villa, L., Falbo, V., Hopkins, K. L., and Threlfall, E. J. (2005). Identification of plasmids by PCR-based replicon typing. J. Microbiol. Methods 63, 219-28.
7. Chang, S.K., Lo, D.Y., Wei, H.W., and Kuo, H.C. (2015). Antimicrobial resistance of Escherichia coli isolates from canine urinary tract infections. J. Vet. Med .Sci. 77, 59-65.
8. Chen, Z., and Jiang, X. P. (2014). Microbiological safety of chicken litter or chicken litter-based organic fertilizers: a review. Agriculture 4, 1-29.
9. CLSI. (2013). Performance standards for antimicrobial susceptibility testing: 23rd informational supplement (M100-S23). Clinical and Laboratory Standards Institute, Wayne, PA.
10. Curriero, F. C., Patz, J. A., Rose, J. B., and Lele, S. (2001). The association between extreme precipitation and waterborne disease outbreaks in the United States, 1948-1994. Am. J. Public Health 91, 1194-9.
11. D'Costa, V. M., McGrann, K. M., Hughes, D. W., and Wright, G. D. (2006). Sampling the antibiotic resistome. Science 311, 374-7.
12. Edelstein, M., Pimkin, M., Palagin, I., Edelstein, I., and Stratchounski, L. (2003). Prevalence and molecular epidemiology of CTX-M extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Russian hospitals. Antimicrob. Agents Chemother. 47, 3724-32.
13. Ewers, C., Bethe, A., Semmler, T., Guenther, S., and Wieler, L. H. (2012). Extended-spectrum beta lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clin. Microbiol. Infect. 18, 646-55.
14. Forsberg, K.J., Reyes, A., Wang, B., Selleck, E.M., Sommer, M.O., and Dantas, G. (2012). The shared antibiotic resistome of soil bacteria and human pathogens. Science 31, 337, 1107-11.
15. Gao, L., Hu, J., Zhang, X., Ma, R., Gao, J., Li, S., Zhao, M., Miao, Z., and Chai, T. (2014). Dissemination of ESBL-Producing Escherichia coli of Chicken Origin to the Nearby River Water. J. Mol. Microbiol .Biotechnol. 24, 279-85.
16. 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. ISME J. 1, 191-203.
17. Guber, A. K., Pachepsky, Y. A., Shelton, D. R., and Yu, O. (2007). Effect of bovine manure on fecal coliform attachment to soil and soil particles of different sizes. Appl. Environ. Microbiol. 73, 3363-70.
18. Guo, Y. F., Zhang, W. H., Ren, S. Q., Yang, L., Lu, D. H., Zeng, Z. L., Liu, Y. H., and Jiang H. X. (2014). IncA/C plasmid-mediated spread of CMY-2 in multidrug-resistant Escherichia coli from food animals in China. PLoS One 9, e96738.
19. Haque, A., Yoshizumi, A., Saga, T., Ishii, Y., and Tateda, K. (2014). ESBL-producing Enterobacteriaceae in environmental water in Dhaka, Bangladesh. J. Infect. Chemother. 20, 735-7.
20. Heuer, H., Schmitt, H. and Smalla, K. (2011). Antibiotic resistance gene spread due to manure application on agricultural fields. Curr. Opin. Microbiol. 14, 236-43.
21. Heuer, H., Solehati, Q., Zimmerling, U., Kleineidam, K., Schloter, M., Müller, T., Focks, A., Thiele-Bruhn, S., and Smalla, K. (2011). Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Appl. Environ. Microbiol. 77, 2527-30.
22. Heuer, H., and Smalla, K. (2007). Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months. Environ. Microbiol. 9, 657-66.
23. Hu, X., Zhou, Q. and Luo, Y. (2010). Occurrence and source analysis of typical veterinary antibiotics in manure, soil, vegetables and groundwater from organic vegetable bases, northern China. Environ. Pollut. 158, 2992-8.
24. Huang, L., Yao, L., He, Z., Zhou, C., Li, G., Yang, B. and Deng, X. (2014). Roxarsone and its metabolites in chicken manure significantly enhance the uptake of As species by vegetables. Chemosphere 100, 57-62.
25. Jensen, L.B., Baloda, S., Boye, M., Aarestrup, F.M. (2001). Antimicrobial resistance among Pseudomonas spp. and the Bacillus cereus group isolated from Danish agricultural soil. Environ. Int. 26, 581-7.
26. Ju, X.T., Kou, C.L., Christie, P., Dou, Z.X., Zhang, F.S. (2007). Changes in the soil environment from excessive application of fertilizers and manures to two contrasting intensive cropping systems on the North China Plain. Environ. Pollut. 145, 497-506.
27. Khaleel, R., Reddy, K. R. and Overcash, M. R. (1982). Transport of potential pollutants in runoff water from areas receiving animal waste. Water Res. 14, 421-36.
28. Koczura, R., Mokracka, J., Jablonska, L., Gozdecka, E., Kubek, M., and Kaznowski, A. (2012). Antimicrobial resistance of integron-harboring Escherichia coli isolates from clinical samples, wastewater treatment plant and river water. Sci. Total Environ. 414, 680-5.
29. Kumar, K., Gupta, S. C., Baidoo, S. K., Chander, Y., and Rosen. C. J. (2005). Antibiotic uptake by plants from soil fertilized with animal manure. J. Environ. Qual. 34, 2082-5.
30. Laube, H., Friese, A., von Salviati, C., Guerra, B., and Rosler, U. (2014). Transmission of ESBL/AmpC producing Escherichia coli from broiler chicken farms to surrounding areas. Vet. Microbiol. 172, 519-27.
31. Magiorakos, A.P., Srinivasan, A., Carey, R.B., Carmeli, Y., Falagas, M.E., Giske, C.G., Harbarth, S., Hindler, J.F., Kahlmeter, G., Olsson-Liljequist, B., Paterson, D.L., Rice, L.B., Stelling, J., Struelens, M.J., Vatopoulos, A., Weber, J.T., and Monnet, D.L. (2012). Multidrug-resistant, extensively drug resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18, 268-81.
32. Marti, R., Scott, A., Tien, Y.C., Murray, R., Sabourin, L., Zhang, Y., and Topp, E. (2013). Impact of manure fertilization on the abundance of antibiotic-resistant bacteria and frequency of detection of antibiotic resistance genes in soil and on vegetables at harvest. Appl. Environ. Microbiol. 79, 5701-9.
33. Monstein, H.J., Ostholm-Balkhed, A., Nilsson, M. V., Nilsson, M., Dornbusch, K., and Nilsson, L. E. (2007). Multiplex PCR amplification assay for the detection of blaSHV, blaTEM and blaCTX-M genes in Enterobacteriaceae. APMIS 115, 1400-8.
34. Pitout, J.D., and Laupland, K.B. (2008). Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect. Dis. 8, 159-66.
35. Rensing, C., Newby, D.T., and Pepper, I.L. (2002). The role of selective pressure and selfish DNA in horizontal gene transfer and soil microbial community adaptation. Soil Biol. Biochem.34, 285-296.
36. Reuland, E. A., Al, N. N., Raadsen, S. A., Savelkoul, P. H., Kluytmans, J. A., and Vandenbroucke-Grauls, C. M. (2014). Prevalence of ESBL-producing Enterobacteriaceae in raw vegetables. Eur. J. Clin. Microbiol. Infect. Dis. 33, 1843-6.
37. Riber, L., Poulsen, P.H., Al-Soud, W.A., Skov Hansen, L.B., Bergmark, L., Brejnrod, A., Norman, A., Hansen, L.H., Magid, J., and Sørensen, S.J. (2014). Exploring the immediate and long-term impact on bacterial communities in soil amended with animal and urban organic waste fertilizers using pyrosequencing and screening for horizontal transfer of antibiotic resistance. FEMS Microbiol. Ecol. 90, 206-24.
38. Ruimy, R., Brisabois, A., Bernede, C., Skurnik, D., Barnat, S., Arlet, G., Momcilovic, S., Elbaz, S., Moury, F., Vibet, M.A., Courvalin, P., Guillemot, D., and Andremont, A. (2010). Organic and conventional fruits and vegetables contain equivalent counts of Gram-negative bacteria expressing resistance to antibacterial agents. Environ. Microbiol. 12, 608-15.
39. Sengeløv, G., Agersø, Y., Halling-Sørensen, B., Baloda, S.B., Andersen, J.S., Jensen, L.B. (2003). Bacterial antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry. Environ. Int. 28, 587-95.
40. Shaheen, B.W., R. Nayak, S. L. Foley, O. Kweon, J. Deck, M. Park, F. Rafii, and D.M. Boothe. (2011). Molecular characterization of resistance to extended-spectrum cephalosporins in clinical Escherichia coli isolates from companion animals in the United States. Antimicrob. Agents Chemother. 55, 5666-75.
41. Smet, A., Martel, A., Persoons, D., Dewulf, J., Heyndrickx, M., Catry, B., Herman, L., Haesebrouck, F., and Butaye, P. (2008). Diversity of extended-spectrum beta-lactamases and class C beta-lactamases among cloacal Escherichia coli Isolates in Belgian broiler farms. Antimicrob. Agents Chemother. 52, 1238-43.
42. Tate, K.W., Atwill, E.R., George, M.R., McDougald, N.K. and Larsen, R.E. (2000). Cryptosporidium parvum transport from cattle fecal deposits on California rangelands. J. Range Manage. 53, 295-9.
43. Venglovsky, J., Sasakova, N., and Placha, I. (2009). Pathogens and antibiotic residues in animal manures and hygienic and ecological risks related to subsequent land application. Bioresour. Technol. 100, 5386-91.
44. Von Salviati, C., Laube, H., Guerra, B., Roesler, U., and Friese, A. (2015). Emission of ESBL/AmpC producing Escherichia coli from pig fattening farms to surrounding areas. Vet. Microbiol. 30, 77-84.
45. Yuan, W., Chai, T.J., and Miao. Z.M. (2010). ERIC-PCR identification of the spread of airborne Escherichia coli in pig houses. Sci. Total Environ. 408, 1446-50.
46. Zhang H, Zhou Y, Guo S and Chang W (2015). Multidrug resistance found in extended-spectrum beta359 lactamase-producing Enterobacteriaceae from rural water reservoirs in Guantao, China. Front. Microbiol. doi: 10.3389/fmicb.2015.00267.
47. Zhang, J., Zheng, B., Zhao, L., Wei, Z., Ji, J., Li, L., Xiao, Y. (2014). Nationwide high prevalence of CTX-M and an increase of CTX-M-55 in Escherichia coli isolated from patients with community-onset infections in Chinese county hospitals. BMC Infect. Dis. 14, 659.
48. Zhao, S., White, D.G., McDermott, P.F., Friedman, S., English, L., Ayers, S., Meng, J., Maurer, J.J., Holland, R., and Walker, R.D. (2001). Identification and expression of cephamycinase bla(CMY) genes in Escherichia coli and Salmonella isolates from food animals and ground meat. Antimicrob. Agents Chemother. 45, 3647-50.
49. Zheng, H., Zeng, Z., Chen, S., Liu, Y., Yao, Q., Deng, Y., Chen, X., Lv, L., Zhuo, C., Chen, Z., and Liu, J.H. (2012). Prevalence and characterisation of CTX-M beta-lactamases amongst Escherichia coli isolates from healthy food animals in China. Int. J. Antimicrob. Agents 39, 305-10.
50. Zhou, Z., Raskin, L., and Zilles, J.L. (2010). Effects of Swine manure on macrolide, lincosamide, and streptogramin B antimicrobial resistance in soils. Appl. Environ. Microbiol. 76, 2218-24.
51. Zhu, Y.G., Johnson, T.A., Su, J.Q., Qiao, M., Guo, G.X., Stedtfeld, R.D., Hashsham, S.A., and Tiedje, J.M. (2013). Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc. Natl. Acad. Sci. U S A 110, 3435-40.