Antibiotic resistance and genetic diversity of Escherichia coli isolates from traditional and integrated aquaculture in South China

Journal of Environmental Science and Health - Part B Pesticides, Food Contaminants, and Agricultural Wastes

Volumn 48, Issue 11, 2013, Pages 999-1013

  Zhang, Rui Quan ^a   Ying, Guang Guo ^a   Su, Hao Chang ^a   Zhou, Li Jun ^a   Liu, You Sheng ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

antibiotic resistance; antibiotic resistance gene; aquaculture; Escherichia coli

Indexed keywords

ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENES; ANTIBIOTIC SUSCEPTIBILITIES; AQUACULTURE SYSTEMS; BACTERIAL RESISTANCE; DETECTION FREQUENCY; GENETIC DIVERSITY; REAL TIME POLYMERASE CHAIN REACTIONS;

AQUACULTURE; ESCHERICHIA COLI; GENES; POLYMERASE CHAIN REACTION; SULFUR COMPOUNDS;

ANTIBIOTICS;

ANTIBIOTIC RESISTANCE; AQUACULTURE SYSTEM; BIOTECHNOLOGY; FECAL COLIFORM; GENETIC VARIATION; INTEGRATED APPROACH;

CHINA;

ANTIINFECTIVE AGENT; ESCHERICHIA COLI PROTEIN;

ANIMAL; ANIMAL DISEASE; ANTIBIOTIC RESISTANCE; AQUACULTURE; ARTICLE; CHINA; DRUG EFFECT; DUCK; ESCHERICHIA COLI; GENETIC VARIABILITY; GENETICS; ISOLATION AND PURIFICATION; MANURE; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; ANTI-BACTERIAL AGENTS; AQUACULTURE; CHINA; DRUG RESISTANCE, BACTERIAL; DUCKS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENETIC VARIATION; MANURE; MICROBIAL SENSITIVITY TESTS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84883628098     PISSN: 03601234     EISSN: 15324109     Source Type: Journal    
DOI: 10.1080/03601234.2013.816611     Document Type: Article

References (57)

1. Defoirdt, T., Sorgeloos, P. and Bossier, P. 2011. Alternatives to antibiotics for the control of bacterial disease in aquaculture. Curr. Opin. Microbiol, 14: 251 - 258.
2. Cabello, F. C. 2006. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ. Microbiol, 8: 1137 - 1144.
3. Pruden, A., Pei, R. T., Storteboom, H. and Carlson, K. H. 2006. Antibiotic resistance genes as emerging contaminants: Studies in northern Colorado. Environ. Sci. Technol., 40: 7445 - 7450. 2006
4. Baquero, F., Alvarez-Ortega, C. and Martinez, J. L. 2009. Ecology and evolution of antibiotic resistance. Environ. Microbiol. Rep, 1: 469 - 476.
5. Agerso, Y. and Petersen, A. 2007. The tetracycline resistance determinant Tet 39 and the sulphonamide resistance gene sulII are common among resistant Acinetobacter spp. isolated from integrated fish farms in Thailand. J. Antimicrob. Chemother, 59: 23 - 27.
6. Dang, S. T., Petersen, A., Van Truong, D., Chu, H. T. and Dalsgaard, A. 2011. Impact of medicated feed on the development of antimicrobial resistance in bacteria at integrated pig-fish farms in Vietnam. Appl. Environ. Microbiol, 77: 4494 - 4498.
7. Hoa, P. T.P., Managaki, S., Nakada, N., Takada, H., Shimizu, A., Anh, D. H., Viet, P. H. and Suzuki, S. 2011. Antibiotic contamination and occurrence of antibiotic-resistant bacteria in aquatic environments of northern Vietnam. Sci. Total Environ, 409: 2894 - 2901.
8. Su, H. C., Ying, G. G., Tao, R., Zhang, R. Q., Fogarty, L. R. and Kolpin, D. W. 2011. Occurrence of antibiotic resistance and characterization of resistance genes and integrons in Enterobacteriaceae isolated from integrated fish farms in south China. J. Environ. Monit, 13: 3229 - 3236.
9. Gao, P., Mao, D., Luo, Y., Wang, L., Xu, B. and Xu, L. 2012. Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Res, 46: 2355 - 2364.
10. Roberts, M. C. 2005. Update on acquired tetracycline resistance genes. FEMS Microbiol. Lett, 245: 195 - 203.
11. Zhang, X. X., Zhang, T. and Fang, H. 2009. Antibiotic resistance genes in water environment. Appl. Microbiol. Biot, 82: 397 - 414.
12. Akinbowale, O. L., Peng, H. and Barton, M. D. 2007. Diversity of tetracycline resistance genes in bacteria from aquaculture sources in Australia. J. Appl. Microbiol, 103: 2016 - 2025.
13. Miranda, C. D., Kehrenberg, C., Ulep, C., Schwarz, S. and Roberts, M. C. 2003. Diversity of tetracycline resistance genes in bacteria from Chilean salmon farms. Antimicrob. Agents Chemother., 47: 883 - 888.
14. Perreten, V. and Boerlin, P. 2003. A new sulfonamide resistance gene (sul3) in Escherichia coli is widespread in the pig population of Switzerland. Antimicrob. Agents Chemother, 47: 1169 - 1172.
15. Seyfried, E. E., Newton, R. J., Rubert, K. F., Pedersen, J. A. and McMahon, K. D. 2010. Occurrence of tetracycline resistance genes in aquaculture facilities with varying use of oxytetracycline. Microb. Ecol, 59: 799 - 807.
16. Tao, R., Ying, G. G., Su, H. C., Zhou, H. W. and Sidhu, J. P. 2010. Detection of antibiotic resistance and tetracycline resistance genes in Enterobacteriaceae isolated from the Pearl rivers in South China. Environ. Pollut, 158: 2101 - 2109.
17. Hu, J. Y., Shi, J C., Chang, H., Li, D., Yang, M. and Kamagata, Y. C. 2008. Phenotyping and genotyping of antibiotic-resistant Escherichia coli isolated from a natural river basin. Environ. Sci. Technol, 42: 3415 - 3420.
18. Dang, H., Zhang, X., Song, L., Chang, Y. and Yang, G. 2006. Molecular characterizations of oxytetracycline resistant bacteria and their resistance genes from mariculture waters of China. Mar. Pollut. Bull, 52: 1494 - 1503.
19. Schmidt, A. S., Bruun, M. S., Dalsgaard, I. and Larsen, J. L. 2001. Incidence, distribution, and spread of tetracycline resistance determinants and integron-associated antibiotic resistance genes among motile aeromonads from a fish farming environment. Appl. Environ. Microbiol, 67: 5675 - 5682.
20. Kim, S. R., Nonaka, L. and Suzuki, S. 2004. Occurrence of tetracycline resistance genes tet(M) and tet(S) in bacteria from marine aquaculture sites. FEMS Microbiol. Lett, 237: 147 - 156.
21. Hoa, P. T.P., Nonaka, L., Viet, P. H. and Suzuki, S. 2008. Detection of the sul1, sul2, and sul3 genes in sulfonamide-resistant bacteria from wastewater and shrimp ponds of north Vietnam. Sci. Total Environ, 405: 377 - 384.
22. 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 - 951.
23. Reinthaler, F. F., Feierl, G., Galler, H., Haas, D., Leitner, E., Mascher, F., Melkes, A. and Posch, J. 2010. ESBL-producing E. coli in Austrian sewage sludge. Water Res, 44: 1981 - 1985.
24. Bibbal, D., Dupouy, V., Ferré, J. P., Toutain, P. L., Fayet, O., Prère, M. F. and Bousquet-Mélou, A. 2007. Impact of three ampicillin dosage regimens on selection of ampicillin resistance in Enterobacteriaceae and excretion of bla(TEM) genes in swine feces. Appl. Environ. Microbiol, 73: 4785 - 4790.
25. Cortés, P., Blanc, V. and Mora, A. 2010. Isolation and characterization of potentially pathogenic antimicrobial-resistant Escherichia coli strains from chicken and pig farms in Spain. Appl. Environ. Microbiol, 76: 2799 - 2805.
26. Jacobs, L. and Chenia, H. Y. 2007. Characterization of integrons and tetracycline resistance determinants in Aeromonas spp. isolated from South African aquaculture systems. Int. J. Food Microbiol, 114: 295 - 306.
27. Radimersky, T., Frolkova, P., Janoszowska, D., Dolejska, M., Svec, P., Roubalova, E., Cikova, P. and Cizek, A. 2010. Antibiotic resistance in faecal bacteria (Escherichia coli, Enterococcus spp.) in feral pigeons. J. Appl. Microbiol., 109: 1687 - 1695.
28. Chen, H., Shu, W., Chang, X., Chen, J. A. and Guo, Y. 2010. The profile of antibiotics resistance and integrons of extended-spectrum beta-lactamase producing thermotolerant coliforms isolated from the Yangtze River basin in Chongqing. Environ. Pollut., 158: 2459 - 2464.
29. Henriques, I., Moura, A., Alves, A., Saavedra, M. J. and Correia, A. 2006. Analysing diversity among beta-lactamase encoding genes in aquatic environments. FEMS Microbiol. Ecol, 56: 418 - 429.
30. Food and Agriculture Organization of the United Nations. 2001. Integrated agriculture-aquaculture, 407 Rome: FAO FISHERIES TECHNICAL Paper, FAO/IIRR/World Fish Center.
31. Petersen, A. and Dalsgaard, A. 2003. Species composition and antimicrobial resistance genes of Enterococcus spp., isolated from integrated and traditional fish farms in Thailand. Environ. Microbiol, 5: 395 - 402.
32. US EPA. 2006. Escherichia coli (E. coli) in Water by Membrane Filtration Using Modified Membrane-Thermo Tolerant Escherichia coli Agar (Modified mTEC), Office of Water, US EPA: Washington, DC. EPA 1603
33. Jacobs, M. B. and Gerstein, M. J. Handbook of Microbiology, Princeton, NJ: D. Van Nostrand Company Inc. 1960
34. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing: Fifteenth Informational Supplement M100-S15. CLSI: Wayne, PA, USA, 2010
35. Krumperman, P. H. 1983. Multiple antibiotic resistance indexing of Escherichia to indentify high-risk source of fecal contamination of foods. Appl. Environ. Microbiol, 46: 165 - 170.
36. Nonga, H. E. and Muhairwa, A. P. 2010. Prevalence and antibiotic susceptibility of thermophilic Campylobacter isolates from free range domestic duck (Cairina moschata) in Morogoro municipality, Tanzania. Trop. Anim. Health Pro, 42: 165 - 172.
37. Silva, N., Igrejas, G., Figueiredo, N., Gonçalves, A., Radhouani, H., Rodrigues, J. and Poeta, P. 2010. Molecular characterization of antimicrobial resistance in Enterococci and Escherichia coli isolates from European wild rabbit (Oryctolagus cuniculus). Sci. Total Environ, 408: 4871 - 4876.
38. Allen, S. E., Boerlin, P., Janecko, N., Lumsden, J. S., Barker, I. K., Pearl, D. L., Reid-Smith, R. J. and Jardine, C. 2011. Antimicrobial resistance in generic Escherichia coli Isolates from wild small mammals living in swine farm, residential, landfill, and natural environments in Southern Ontario, Canada. Appl. Environ. Microbiol, 77: 882 - 888.
39. Pallecchi, L., Lucchetti, C., Bartoloni, A., Bartalesi, F., Mantella, A., Gamboa, H., Carattoli, A. and Paradisi, F. 2007. Population structure and resistance genes in antibiotic-resistant bacteria from a remote community with minimal antibiotic exposure. Antimicrob. Agents Chemother, 51: 1179 - 1184.
40. Gordon, L., Giraud, E., Ganière, J. P., Armand, F., Bouju-Albert, A., Cotte, N., Mangion, C. and Le Bris, H. 2007. Antimicrobial resistance survey in a river receiving effluents from freshwater fish farms. J. Appl. Microbiol, 102: 1167 - 1176.
41. Le, T. X., Munekage, Y. and Kato, S. 2005. Antibiotic resistance in bacteria from shrimp farming in mangrove areas. Sci. Total Environ, 349: 95 - 105.
42. Zhang, Y., Li, Y. and Sun, X. L. 2011. Antibiotic resistance of bacteria isolated from shrimp hatcheries and cultural ponds on Donghai Island, China. Mar. Pollut. Bull, 62: 2299 - 2307.
43. Ishida, Y., Ahmed, A. M., Mahfouz, N. B., Kimura, T., El-Khodery, S. A., Moawad, A. A. and Shimamoto, T. 2010. Molecular analysis of antimicrobial resistance in gram-negative bacteria Isolated from fish farms in Egypt. J. Vet. Med. Sci, 72: 727 - 734.
44. Tendencia, E. A. and de la Pena, L. D. 2001. Antibiotic resistance of bacteria from shrimp ponds. Aquaculture, 195: 193 - 204.
45. Vaseeharan, B., Ramasamy, P., Murugan, T. and Chen, J. C. 2005. In vitro susceptibility of antibiotics against Vibrio spp. and Aeromonas spp. isolated from Penaeus monodon hatcheries and ponds. Int. J. Antimicrob. Ag., 26: 285 - 291.
46. Verner-Jeffreys, D. W., Welch, T. J., Schwarz, T., Pond, M. J., Woodward, M. J., Haig, S. J., Rimmer, G. S., Roberts, E., Morrison, V. and Baker-Austin, C. 2009. High prevalence of multidrug-tolerant bacteria and associated antimicrobial resistance genes isolated from ornamental fish and their carriage water. Plos One, 4: e8388
47. Agerso, Y. and Sandvang, D. 2005. Class 1 integrons and tetracycline resistance genes in Alcaligenes, Arthrobacter and Pseudomonas spp. isolated from pigsties and manured soil. Appl. Environ. Microbiol, 71: 7941 - 7947.
48. Frank, T., Gautier, V., Talarmin, A., Bercion, R. and Arlet, G. 2007. Characterization of sulphonamide resistance genes and class 1 integron gene cassettes in Enterobacteriaceae, Central African Republic (CAR). J. Antimicrob. Chemother, 59: 742 - 745.
49. Ng, K., Martin, I. and Alfa, M. 2001. Multiplex PCR for the detection of tetracycline resistant genes. Mol. Cell Probes, 15: 209 - 215.
50. Roberts, M. C., Pang, Y., Riley, D. E., Hillier, S. L. and Berger, R. C. 1993. Detection of Tet M and Tet O tetracycline resistance genes by polymerase chain reaction. Mol. Cell. Probes, 7: 387 - 393.
51. Agersø, Y. and Sandvang, D. 2005. Class 1 integrons and tetracycline resistance genes in Alcaligenes, Arthrobacter, and Pseudomonas spp. isolated from pigsties and manured soil. Appl. Environ. Microbiol, 71: 7941 - 7947.
52. Aminov, R. I., Garrigues-Jeanjean, N. and Mackie, R. I. 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 - 32.
53. Wu, N., Qiao, M., Zhang, B., Cheng, W. D. and Zhu, Y. G. 2010. Abundance and Diversity of Tetracycline Resistance Genes in Soils Adjacent to Representative Swine Feedlots in China. Environ. Sci. Technol, 44: 6933 - 6939.
54. Kerrn, M. B., Klemmensen, T., Frimodt-Møller, N. and Espersen, F. 2002. Susceptibility of Danish Escherichia coli strains isolated from urinary tract infections and bacteraemia, and distribution of sul genes conferring sulphonamide resistance. J. Antimicrob. Chemother, 50: 513 - 516.
55. Pei, R., Kim, S. C., Carlson, K. H. and Pruden, A. 2006. Effect of River Landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Res., 40: 2427 - 2435.
56. Henriques, I., Moura, A., Alves, A., Saavedra, M. J. and Correia, A. 2006. Analysing diversity among beta-lactamase encoding genes in aquatic environments. FEMS Microbiol. Ecol, 56: 418 - 429.
57. Chen, H., Shu, W., Chang, X., Chen, J. A., Guo, Y. and Tan, Y. 2010. The profile of antibiotics resistance and integrons of extended-spectrum beta-lactamase producing thermotolerant coliforms isolated from the Yangtze River basin in Chongqing. Environ. Pollut, 158: 2459 - 2464.