Tran Hoa Ly * , Hong Mong Huyen and Tran Thi Tuyet Hoa

* Corresponding author (

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Recently, extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli was isolated from cultured striped catfish, red tilapia and wild fish in Mekong Delta, Vietnam. ESBL genes are located on plasmids, facilitating their spreads among Gram-negative bacilli bacteria species. To better understand the dissemination of resistance genes in aquatic system, the antimicrobial susceptibility patterns and the molecular characteristics of ESBL-producing E. coli isolates were investigated by disk diffusion method and polymerase chain reaction. The results indicated that: (i) the proportion of antibiotic resistance of ESBL-producing E. coli was relatively high in most type of antibiotics except meropenem and cefoxitin; Considerably, multiple drugs resistance was recorded at high percentage, including 100% for ESBL-producing E. coli isolates of snakehead fish, 90% depended on the figure for striped catfish, 85% for ESBL-producing E. coli isolates of red tilapia and 50% for that of wild fish (ii) the number of ESBL-producing E. coli isolates carrying multiple ESBL genes were 90%, with significantly higher than those of carrying single ESBL gene at just 10%. In addition, the B2 virulence group was mainly isolated from wild fish, which was higher compared to groups of cultured fish (iii) the majority of isolates harbored multiple sulfonamides resistance genes (72.2%), which was significantly higher compared to the percentages of isolates carrying single genes (27.8%). The study illustrated that there were the significant widespread of antibiotic-resistant genes of ESBL-producing E. coli as well as a considerable ratio of multidrug resistance.
Keywords: ESBL-producing Escherichia coli, extended spectrum beta-lactamase genes, fish, Mekong Delta, sul genes

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Alexopoulou, K., Foka, A., Petinaki, E., Jelastopulu, E., Dimitracopoulos, G., Spiliopoulou, I., 2006. Comparison of two commercial methods with PCR restriction fragment length polymorphism of the tuf gene in the identification of coagulase-negative staphylococci. Lett Appl Microbiol. 43(4): 450-4.

Antunes, P., Machado, J., Sousa, J. C. and Peixe, L., 2005. Dissemination of sulfonamide resistance genes (sul1, sul2, and sul3) in Portuguese Salmonella enterica strains and relation with integrons. Antimicrobial Agents and Chemotherapy. 49(2): 836-839.

Arabi, H., Pakzad, I., Nasrollahi, A., et al., 2015. Sulfonamide resistance genes (sul) in extended spectrum beta lactamase (ESBL) and non-ESBL producing Escherichia coli Isolated from Iranian Hospitals. Jundishapur Journal of Microbiology. 8(7): 19-61.

Asma, M.A.J., 2006. Extended-spectrum beta-lactamases (ESBLS): A global problem. Kuwait Medical Journal. 38(3): 171-185.

Bean, D.C., Livermore, D. M. and Hall, L. M., 2009. Plasmids imparting sulfonamide resistance in Escherichia coli: implications for persistence. Antimicrobial Agents and Chemotherapy. 53(3): 1088-1093.

Blahna, M.T., Zalewski C. A., Reuer, J., Kahlmeter, G., Foxman, B. and Marrs, C. F., 2006. The role of horizontal gene transfers of trimethoprim-sulfamethoxazole resistance among uropathogenic Escherichia coli in Europe and Canada. Journal of Antimicrobial Chemotherapy. 57(4): 666-672.

Byrne-Bailey, K.G., Gaze, W.H., Kay, P., Boxall, A.B.A., Hawkey, P.M. and Wellington, E.M.H., 2009. Prevalence of sulfonamide resistance genes in bacterial isolates from manured agricultural soils and pig slurry in the United Kingdom. Antimicrobial Agents and Chemotherapy. 53(2): 696-702.

Cao, V., Lambert, T., Nhu, D.Q., et al., 2002. Distribution of Extended spectrum β-lactamases in clinical isolates of Enterobacteriaceae in Vietnam. Antimicrobial agents and chemotherapy. 46(12): 3739–3743.

Carneiro, D.O., Figuerido,H. C. P., Pereira Júnior,D. J., Leal, A. G. and Logato, P. V. R., 2007. Perfil de susceptibilidade a antimicrobianos de bactérias isoladas em diferentes sisemas de cultivo de tilapia-do-Nilo (Oriochromis niloticus). Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 59(4): 869-876.

Clermont, O., Bonacorsi, S. and Bingen, E., 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Applied and Environmental Microbiology. 66(10):4555–4558.

CLSI, Clinical and Laboratory Standards Institute, 2011. Performance Standards for Antimicrobial Susceptibility Testing. Fifteenth Informational Supplement, M100-S15. CLSI; Wayne, PA, USA.

Enne, V.I., Livermore, D. M., Stephens, P. and Hall, L. M., 2001. Persistence of sulfonamide resistance in Escherichia coli in the UK despite national prescribing restriction. The Lancet. 357(9265): 1325–1328.

Enne, V.I., King, A., Livermore, D.M. and Hall, L.M., 2002. Sulfonamide resistance in Haemophilus influenzae mediated by acquisition of sul2 or a short insertion in chromosomal folP. Antimicrobial Agents and Chemotherapy. 46(6): 1934–1939.

Frank, T., Gautier, V., Talarmin, A., Bercion, R. and Arlet, G., 2007. Characterization of sulfonamide resistance genes and class 1 integron gene cassettes in Enterobacteriaceae, Central African Republic. Journal of Antimicrobial Chemotherapy. 59(4): 742–745.

Guerra, B., Junker, E. and Helmuth, R., 2004. Incidence of the recently described sulfonamide resistance gene sul3 among German Salmonella enterica strains isolated from livestock and food. Antimicrobial Agents and Chemotherapy. 48(7): 2712–2715.

Hammerum, A.M., Sandvang, D., Andersen, S. R., et al., 2006. Detection of sul1, sul2 and sul3 in sulfonamide resistant Escherichia coli isolates obtained from healthy humans, pork and pigs in Denmark. International Journal of Food Microbiology. 106(2): 235-237.

Heuer, H. and Smalla, K., 2007. Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months. Environmental Microbiology. 9: 657-66.

Heuer, O. E., Kruse, H., Grave, K., Collignon, P., Karunasagar, I. and Angulo, F. J., 2009. Human health consequences of use of antimicrobial agents in aquaculture. Clinical Infectious Diseases. 49(8): 1248-1253.

Huovinen, P., 2001. Resistance to trimethoprim-sulfamethoxazole. Clinical Infectious Diseases. 32(11): 1608-1614.

Jakobsen, L., Kurbasic, A., Skjot-Rasmussen, L., Ejrnaes, K., Porsbo, L. J., and Pedersen, K., 2010. Escherichia coli isolates from broiler chicken meat, broiler chickens, pork, and pigs share phylogroups and antimicrobial resistance with community dwelling humans and patients with urinary tract infection. Foodborne Pathogens and Disease. 7(5): 537-547.

John, T., 2010. Trimethoprim, Co-Trimoxazole (Co-T) and related agents. Kucers' The Use of Antibiotics. 1076-1087.

Kerrn, M.B., Klemmensen, T., Frimodt-Moller, N. and Espersen, F., 2002. Susceptibility of Danish Escherichia coli strains isolated from urinary tract infections and bacteremia, and distribution of sul genes conferring sulfonamide resistance. Journal of Antimicrobial Chemotherapy. 50(4): 513-516.

Le, V. H., Ryuji, K., Khong, D. T., et al., 2015. Widespread dissemination of extended-spectrum β-lactamase-producing, multidrug-resistant Escherichia coli in livestock and fishery products in Vietnam. International Journal of Food Contamination. 2(1): 17.

Lillo, J., Pai, K., Balode, A., et al., 2014. Differences in Extended-spectrum beta-lactamase producing Escherichia coli virulence factor genes in the Baltic Sea region. Biomedicine Research International. 2014(2): 427254.

Mitsuhashi, S. 1971. Transferable drug resistance factor R. University of Tokyo Press. Tokyo. 203 pages.

Monstein, H. J., Maria, T. and Lennart, E. N., 2009. Molecular identification of CTX-M and blaOXY/K1 β-lactamase genes in Enterobacteriaceae by sequencing of universal M13-sequence tagged PCR-amplicons. Biomedicine Central Infectious Disease. 9: 7.

Nasreldin, E. and Khaldoon, A., 2015. Incidence and antimicrobial susceptibility pattern of extended-spectrum-β-lactamase-producing Escherichia coli isolated from retail imported mackerel fish. African Journal of Biotechnology.14(23): 1954-1960.

Pitout, J.D., Laupland, K.B., 2008. Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis. 8: 159–66.

Rådström, P., Swedberg, G. and Sköld, O., 1991. Genetic analyses of sulfonamide resistance and its dissemination in gram-negative bacteria illustrate new aspects of R plasmid evolution. Antimicrobial Agents and Chemotherapy. 35(9): 1840–1848.

Shoemaker, C.A., Evans, J.J. and Klesius, P.H., 2000. Density and Dose: factors affecting mortality of Streptococcus innate infected tilapia (Oreochromis niloticus). Aquaculture. 188(3-4): 229-235.

Su, H. Ch., Ying, G. G., Tao, R., Zhang, R. Q., Zhao, J. L. and Liu, Y. Sh., 2012. Class 1 and 2 integrons, sul resistance genes and antibiotic resistance in Escherichia coli isolated from Dongjiang River, South China. Journal of Environmental pollution. 169:42-49.

Trobos, M., Jakobsen, L., Olsen, K. E., et al., 2008. Prevalence of sulfonamide resistance and class 1 integron genes in Escherichia coli isolates obtained from broilers, broiler meat, healthy humans and urinary infections in Denmark. International Journal of Food Microbiology. 32(4): 367-369.

Trobos, M., Christensen, H., Sunde, M., Nordentoft, S., Agerso,Y. and Simonsen, G. S., 2009. Characterization of sulfonamide-resistant Escherichia coli using comparison of sul2 gene sequences and multi-locus sequence typing. Microbiology.155(3): 831–836.

Van, T. T. H., Moutafis, G., Istivan, T., Tran, L. T., and Coloe, P. J., 2007a. Detection of Salmonella spp. In retail raw food samples from Vietnam and characterization of their antibiotic resistance. Applied Environmental Microbiology. 73(21): 6885–6890.

Van, T. T. H., Moutafis, G., Tran, L. T. and Coloe, P. J., 2007b. Antibiotic resistance in food-borne bacterial contaminants in Vietnam. Applied Environmental Microbiology. 73(24): 7906-7911.

Wu, S., Dalsgaard, A., Hammerum, A. M., Porsbo, L. J. and Jensen, L. B., 2010. Prevalence and characterization of plasmids carrying sulfonamide resistance genes among Escherichia coli from pigs, pig carcasses and human. Acta Veterinaria Scandinavica. 52(1): 47.