Prevalence of antibiotic resistance genes and genetic relationship of Escherichia coli serotype O45, O113, O121, and O157 isolated from cattle in the Mekong Delta, Vietnam

Main Article Content

Nguyen Khanh Thuan
Nguyen Thanh Lam
Nguyen Tran Phuoc Chien
Nguyen Phuc Khanh
Ly Thi Lien Khai
Tran Ngoc Bich


A total of 39 Escherichia coli strains serotype O45, O113, O121, and O157 isolated from cattle in the Mekong Delta were examined the antimicrobial susceptibility to 13 antibiotics by the disc-diffusion method. Those strains were also analyzed for the presence of antibiotic resistance genes by PCR assay, and their genetic relationship by ERIC-PCR assay. The results of antimicrobial susceptibility testing showed that those strains were sensitive to most of the examined antibiotics, but were relatively high resistance to ampicillin (64.10%), and colistin (53.85%). Those E. coli strains could be resistant against one to eight antibiotics with 22 resistance patterns obtained. Moreover, those E. coli strains harbored one to seven antibiotic resistance genes. Gene tetA (51.28%) and blaampC (48.72%) were detected frequently while gene tetB, blaCMY, and cat1 were not found in those E. coli strains. A total of 21 combined patterns of antibiotic resistance genes were recorded, and the most frequent combined pattern was blaampC+tetA (12.82%). ERIC-PCR analysis revealed that each E. coli serotype exhibited various genetic patterns with 40%-100% of similarity. The most elevated number of patterns were in E. coli O157 (nine patterns), followed by E. coli O121 (six patterns). The prevalence of antibiotic resistance genes and diverse genetic characteristics in those E. coli strains originated from cattle constitute potential risks to local health in the Mekong Delta.

Article Details

How to Cite
Khanh Thuan, N. ., Thanh Lam, N. ., Tran Phuoc Chien, N. ., Phuc Khanh, N. ., Thi Lien Khai, L. ., & Ngoc Bich, T. . (2022). Prevalence of antibiotic resistance genes and genetic relationship of Escherichia coli serotype O45, O113, O121, and O157 isolated from cattle in the Mekong Delta, Vietnam: Veterinary Integrative Sciences, 20(3), 695–707. Retrieved from
Research Articles


Algammal, A.M., El-Sayed, M.E., Youssef, F.M., Saad, S.A., Elhaig, M.M., Batiha, G.E.,Hozzein, W.N., Ghobashy, M.O.I., 2020. Prevalence, the antibiogram and the frequency of virulence genes of the most predominant bacterial pathogens incriminated in calf pneumonia. AMB Express. 10(1), 1-8.

Ali, T., ur Rahman, S., Zhang, L., Shahid, M., Zhang, S., Liu, G., Gao, J., Han, B., 2016.ESBL-producing Escherichia coli from cows suffering mastitis in China contain clinical Class 1 integrons with CTX-M linked to IS CR1. Front. Microbiol. 7, 1931.

Anuradha, A.A., Rahul, P.K., Chandrakant, D.B., Padmakar, D.D., Shivaji, D.L., Bandu, N.G., 2014. Prevalence of antimicrobial resistant pathotypes of Escherichia coli in beef cattle and slaughterhouse premise. Afr. J. Microbiol. Res. 8(3), 277-286.

Armstrong, G.L., Hollingsworth, J., Morris, J.G., Jr., 1996. Emerging foodborne pathogens: Escherichia coli O157:H7 as a model of entry of a new pathogen into the food supply of the developed world. Epidemiol. Rev. 18(1), 29-51.

Awawdeh, L., 2018. Studies on avian pathogenic Escherichia coli in commercial broiler chicken in South East Queensland [PhD Thesis, School of Veterinary Science]. University of Queensland.

Badouei, M.A., Jajarmi, M., Mirsalehian, A., 2015. Virulence profiling and genetic relatedness of Shiga toxin-producing Escherichia coli isolated from humans and ruminants. Comp. Immunol. Microbiol. Infect. Dis. 38, 15-20.

Bai, L., Zhao, J., Gan, X., Wang, J., Zhang, X., Cui, S., Xia, S., Hu, Y., Yan, S., Wang, J.,2016. Emergence and diversity of Salmonella enterica serovar Indiana isolates with concurrent resistance to ciprofloxacin and cefotaxime from patients and food-producing animals in China. Antimicrob. Agents Chemother. 60(6), 3365-3371.

Bengtsson-Palme, J., 2018. The diversity of uncharacterized antibiotic resistance genes can be predicted from known gene variants—but not always. Microbiome. 6(1), 1-12.

Boerlin, P., Travis, R., Gyles, C.L., Reid-Smith, R., Heather, Lim N.J., Nicholson, V.,McEwen, S.A., Friendship, R., Archambault, M., 2005. Antimicrobial resistance and virulence genes of Escherichia coli isolates from swine in Ontario. Appl. Environ.Microbiol. 71(11), 6753-6761.

Bradford, P.A., 2001. Extended-spectrum β-lactamases in the 21st century: characterization,epidemiology, and detection of this important resistance threat. Clin. Microbiol. Rev.14(4), 933-951.

Bui, T.L.M., Luu, H.M., Nguyen, N.X.D., 2018. Prevalence of extendedspectrum beta-lactamaseproducing Escherichia coli on chicken rearer in the Mekong Delta.Can Tho Univ. J. Sci. 4, 1-5.

Buvens, G., Bogaerts, P., Glupczynski, Y., Lauwers, S., Piérard, D., 2010. Antimicrobial resistance testing of verocytotoxin-producing Escherichia coli and first description of TEM-52 extended-spectrum β-lactamase in serogroup O26. Antimicrob. Agents Chemother. 54(11), 4907-4909.

Cabal, A., Porrero, M.C., ML, D.L.C., Saez, J.L., Barcena, C., Lopez, G., Gortazar, C.,Dominguez, L., Alvarez, J., 2016. Molecular characterization and antimicrobial resistance of STEC strains isolated from healthy cattle in 2011 and 2013 in Spain.Epidemiol. Infect. 144(14), 2956-2966.

Carattoli, A., Filetici, E., Villa, L., Dionisi, A.M., Ricci, A., Luzzi, I., 2002. Antibiotic resistance genes and Salmonella genomic island 1 in Salmonella enterica serovar Typhimurium isolated in Italy. Antimicrob. Agents. Chemother. 46(9), 2821-2828.

Carattoli, A., 2009. Resistance plasmid families in Enterobacteriaceae. Antimicrob. Agents.Chemother. 53(6), 2227-2238.

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(2), 394-397.

CLSI, 2020. Performance standard for antimicrobial susceptibility testing, 29th edition.Clinical and Laboratory Standard Institute M100S, Wayne, PA, USA.

Cobbold, R., Desmarchelier, P., 2001. Characterisation and clonal relationships of Shiga-toxigenic Escherichia coli (STEC) isolated from Australian dairy cattle. Vet.Microbiol. 79(4), 323-335.

da Costa, P.M., Oliveira, M., Bica, A., Vaz-Pires P., Bernardo F., 2007. Antimicrobial resistance in Enterococcus spp. and Escherichia coli isolated from poultry feed and feed ingredients. Vet. Microbiol. 120(1-2), 122-131.

DebRoy, C., Roberts, E., Fratamico, P.M., 2011. Detection of O antigens in Escherichia coli.Anim. Health Res. Rev. 12(2), 169-185.

Erickson, M.C., Doyle, M.P., 2007. Food as a vehicle for transmission of Shiga toxin–producing Escherichia coli. J. Food Prot. 70(10), 2426-2449.

Escobar-Páramo, P., Le Menac'h, A., Le Gall, T., Amorin, C., Gouriou, S., Picard, B., Skurnik,D., Denamur, E., 2006. Identification of forces shaping the commensal Escherichia coli genetic structure by comparing animal and human isolates. Environ. Microbiol. 8(11), 1975-1984.

Forward, K., Willey, B., Low, D., McGeer, A., Kapala, M., Kapala, M., Burrows, L., 2001.Molecular mechanisms of cefoxitin resistance in Escherichia coli from the Toronto area hospitals. Diagn. Microbiol. Infect. Dis. 41(1-2), 57-63.

Frye, J.G., Jackson, C.R., 2013. Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from US food animals. Front. Microbiol. 4, 135.

Geue, L., Klare, S., Schnick, C., Mintel, B., Meyer, K., Conraths, F.J., 2009. Analysis of the clonal relationship of serotype O26: H11 enterohemorrhagic Escherichia coli isolates from cattle. Appli. Environ. Microbiol. 75(21), 6947-6953.

Habets, A., Crombé, F., Nakamura, K., Guérin, V., De Rauw, K., Piérard, D., Saulmont, M.,Hayashi, T., Mainil, J., Thiry, D., 2021. Genetic characterization of Shigatoxigenic and enteropathogenic Escherichia coli O80: H2 from diarrhoeic and septicaemic calves and relatedness to human Shigatoxigenic E. coli O80: H2. J. Appl. Microbiol.130(1), 258-264.

Iweriebor, B.C., Iwu, C.J., Obi, L.C., Nwodo, U.U., Okoh, A.I., 2015. Multiple antibiotic resistances among Shiga toxin producing Escherichia coli O157 in feces of dairy cattle farms in Eastern Cape of South Africa. BMC Microbiol. 15(1), 1-9.

Jaja, I.F., Oguttu, J., Jaja, C.J.I., Green, E., 2020. Prevalence and distribution of antimicrobial resistance determinants of Escherichia coli isolates obtained from meat in South Africa. Plos One. 15(5), e0216914.

Johnson, J.R., Sannes, M.R., Croy, C., Johnston, B., Clabots, C., Kuskowski, M.A., Bender,J., Smith, K.E., Winokur, P.L., Belongia, E.A., 2007. Antimicrobial drug–resistantEscherichia coli from humans and poultry products, Minnesota and Wisconsin,2002–2004. Emerg. Infect. Dis. 13(6), 838.

Jouini, A., Vinué, L., Slama, K.B., Saenz, Y., Klibi, N., Hammami, S., Boudabous, A., Torres,C., 2007. Characterization of CTX-M and SHV extended-spectrum β-lactamases and associated resistance genes in Escherichia coli strains of food samples in Tunisia. J.Antimicrob. Chemother. 60(5), 1137-1141.

Kadlec, K., Schwarz, S., 2008. Analysis and distribution of class 1 and class 2 integrons and associated gene cassettes among Escherichia coli isolates from swine, horses, cats and dogs collected in the BfT-GermVet monitoring study. J. Antimicrob. Chemother.62(3), 469-473.

Kennedy, J., Simmonds, L., Orme, R., Doherty, W., 2017. An unusual case of Escherichia coli O157: H7 infection with pseudomembranous colitis-like lesions associated with haemolytic-uraemic syndrome and neurological sequelae. BMJ Case Rep. 2017,bcr-2016-218586.

Kluytmans, J.A., Overdevest, I.T., Willemsen, I., Kluytmans-van den Bergh, M.F., van der Zwaluw, K., Heck, M., Rijnsburger, M., Vandenbroucke-Grauls, C.M., Savelkoul,P.H., Johnston, B.D., Gordon, D., Johnson, J.R., 2013. Extended-spectrum β-lactamase–producing Escherichia coli from retail chicken meat and humans: comparison of strains, plasmids, resistance genes, and virulence factors. Clin. Infect.Dis. 56(4), 478-487.

Lin, A., Nguyen, L., Lee, T., Clotilde, L.M., Kase, J.A., Son, I., Carter, J.M., Lauzon, C.R.,2011. Rapid O serogroup identification of the ten most clinically relevant STECs by Luminex microbead-based suspension array. J. Microbiol. Methods. 87(1), 105-110.

Ly, T.L.K., Tran, T.P., Nguyen, T.T., HA, T.T., 2009. Prevalence of Escherichia coli O157 from cattle and foods in the Mekong Delta, Vietnam. J. Vet. Epidemiol. 13(2),107-113.

Maynard, C., Fairbrother, J.M., Bekal, S., Sanschagrin, F., Levesque, R.C., Brousseau, R.,Masson, L., Lariviere, S., Harel, J., 2003. Antimicrobial resistance genes in enterotoxigenic Escherichia coli O149: K91 isolates obtained over a 23-year period from pigs. Antimicrob. Agents Chemother. 47(10), 3214-3221.

Momtaz, H., Karimian, A., Madani, M., Safarpoor Dehkordi, F., Ranjbar, R., Sarshar, M.,Souod, N., 2013. Uropathogenic Escherichia coli in Iran: serogroup distributions,virulence factors and antimicrobial resistance properties. Ann. Clin. Microbiol.Antimicrob. 12(1), 1-12.

Montso, K.P., Dlamini, S.B., Kumar, A., Ateba, C.N., 2019. Antimicrobial resistance factors of extended-spectrum beta-lactamases producing Escherichia coli and Klebsiella pneumoniae isolated from cattle farms and raw beef in North-West Province, South Africa. BioMed Res. Int. 2019, 4318306.

Navajas‐Benito, E.V., Alonso, C.A., Sanz, S., Olarte, C., Martínez‐Olarte, R., Hidalgo‐Sanz,S., Somalo, S., Torres, C., 2017. Molecular characterization of antibiotic resistance in Escherichia coli strains from a dairy cattle farm and its surroundings. J. Sci. Food

Agric. 97(1), 362-365.

Olatoye, I.O., 2010. The incidence and antibiotics susceptibility of Escherichia coli O157: H7 from beef in Ibadan Municipal, Nigeria. Afr. J. Biotechnol. 9(8).

Randall, L., Cooles, S., Osborn, M., Piddock, L., Woodward, M.J., 2004. Antibiotic resistance genes, integrons and multiple antibiotic resistance in thirty-five serotypes of Salmonella enterica isolated from humans and animals in the UK. J. Antimicrob.Chemother. 53(2), 208-216.

Ranjbar, R., Tabatabaee, A., Behzadi, P., Kheiri, R., 2017. Enterobacterial repetitive intergenic consensus polymerase chain reaction (ERIC-PCR) genotyping of Escherichia coli strains isolated from different animal stool specimens. Iranian J. Pathol. 12(1), 25-34.

Sobur, M.A., Sabuj, A.A.M., Sarker, R., Rahman, A.T., Kabir, S.L., Rahman, M.T., 2019. Antibiotic-resistant Escherichia coli and Salmonella spp. associated with dairy cattle and farm environment having public health significance. Vet. World. 12(7), 984.

Soumet, C., Ermel, G., Fach, P., Colin, P., 1994. Evaluation of different DNA extraction procedures for the detection of Salmonella from chicken products by polymerase chain reaction. Lett. Appl. Microbiol. 19(5), 294-298.

Sunde, M., Norström, M., 2006. The prevalence of, associations between and conjugal transfer of antibiotic resistance genes in Escherichia coli isolated from Norwegian meat and meat products. J. Antimicrob. Chemother. 58(4), 741-747.

Thepmanee, J., Rodroo, J., Awaiwanont, N., Intanon, M., Na Lampang, K., Thitaram, N.,Thongkorn, K., (2018). Prevalence and antibiotic resistance of extended-spectrum beta-lactamase (ESBL) producing Escherichia coli in healthy dogs in Chiang Mai Jirapa. Vet. Integr. Sci. 16(3), 233–245.

Toro, C., Farfán, M., Contreras, I., Flores, O., Navarro, N., Mora, G., Prado, V., 2005. Genetic analysis of antibiotic-resistance determinants in multidrug-resistant Shigella strains isolated from Chilean children. Epidemiol. Infect. 133(1), 81-86.

Valentin, L., Sharp, H., Hille, K., Seibt, U., Fischer, J., Pfeifer, Y., Michael, G.B., Nickel, S.,Schmiedel, J., Falgenhauer, L., 2014. Subgrouping of ESBL-producing Escherichia coli from animal and human sources: an approach to quantify the distribution of ESBL types between different reservoirs. Inte. J. Med. Microbiol.304(7), 805-816.

Van, T.T.H., Chin, J., Chapman, T., Tran, L.T., Coloe, P.J., 2008. Safety of raw meat and shellfish in Vietnam: an analysis of Escherichia coli isolations for antibiotic resistance and virulence genes. Int. J. Food Microbiol. 124(3), 217-223.

Weill, F.X., Perrier-Gros-Claude, J.-D., Demartin, M., Coignard, S., Grimont, P.A., 2004. Characterization of extended-spectrum-β-lactamase (CTX-M-15)-producing strains of Salmonella enterica isolated in France and Senegal. FEMS Microbiol. Lett.238(2), 353-358.

Worley, J.N., Flores, K.A., Yang, X., Chase, J.A., Cao, G., Tang, S., Meng, J., Atwill, E.R., 2017. Prevalence and genomic characterization of Escherichia coli O157: H7 in cow-calf herds throughout California. Appl. Environ. Microbiol. 83(16),e00734-00717.

Yamamoto, S., Nakano, M., Kitagawa, W., Tanaka, M., Sone, T., Hirai, K., Asano, K., 2014. Characterization of multi-antibiotic-resistant Escherichia coli isolated from beef cattle in Japan. Microbes Environ. 29(2), 136-144.