Phenotypic and Genotypic Characterization of Extended-Spectrum -Lactamase Producing Escherichia coli Isolated from Pig Feces in Farms, Muang Phayao


Narong Nuanmuang Pareeya Baiubon Nudchanard Wannathong Benjamas Nunta Niphaphorn Suriya Parisa Chaingam Aksarakorn Kummasook


     Extended-Spectrum β-Lactamase (ESBL)-producing Escherichia coli has been reported increasingly worldwide. This study aimed to investigate the prevalence, phenotypic and genotypic resistance of ESBL-producing E. coli isolated from pig feces in Muang District, Phayao Province. Pig feces were screened on MacConkey agar supplemented with (1 µg/mL) cefotaxime or ceftazidime. Suspected ESBL isolates on screening media were identified with biochemical tests. Then, suspected-ESBL-producing E. coli isolates were confirmed ESBL phenotype with combination disk method. Antimicrobial susceptibility and detection of ESBL genes were performed in a total 47 confirmed-ESBL-producing E. coli with 21 antimicrobial agents by disk diffusion and PCR methods, respectively. The results showed the prevalence of ESBL-producing E. coli, 58.8% (47/80). All 47 isolates were multidrug resistance (MDR), with resistant to AMP, CTX, CRO and CPD. However, they were still susceptible to AMC, FOX, ETP, IMP, MEM, FOS and TGC. Moreover, the phenotypic β-lactam resistance can be grouped into 6 patterns, with the predominance of AMP CTX CRO CPD ATM FEP in 48.9% (23/47). Genotypic characterization showed that all isolates possessed blaCTX-M-9 and 7 genotypic-resistant patterns have been divided. The most frequently genotypic-resistant pattern was blaCTX-M-9 (31.9%), followed by blaCTX-M-1 + CTX-M-9 (21.3%) and blaCTX-M-1 + CTX-M-9 + TEM (19.1%). However, there was no blaSHV gene found.High prevalence of ESBL-producing E. coli in pig farms indicated that pigs were an important reservoir of MDR. Therefore, increasing of ESBL isolates in pig farms might increase the risk of transmission ESBL from feces to the human.

Keywords: Escherichia coli, ESBL, Antimicrobial Resistance, Pig Feces


Chang, Q., Wang, W., Regev-Yochay, G., Lipsitch, M., & Hanage, W. P. (2015). Antibiotics in agriculture and the risk to human health: how worried should we be?. Evolutionary Applications, 8(3), 240-247.
Dahms, C., Hübner, N.-O., Kossow, A., Mellmann, A., Dittmann, K., & Kramer, A. (2015). Occurrence of ESBL-producing Escherichia coli in livestock and farm workers in Mecklenburg-Western Pomerania, Germany. PLoS One, 10(11), 0143326.
Dallenne, C., Da Costa, A., Decre, D., Favier, C., & Arlet, G. (2010). Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae. Journal of Antimicrobial Chemotherapy, 65(3), 490-495.
Dohmen, W., Bonten, M. J. M., Bos, M. E. H., Van Marm, S., Scharringa, J., Wagenaar, J. A., & Heederik, D. J. J. (2015). Carriage of extended-spectrum β-lactamases in pig farmers is associated with occurrence in pigs. Clinical Microbiology and Infection, 21(10), 917-923.
Ewers, C., Bethe, A., Semmler, T., Guenther, S. & Wieler, L. H. (2012). Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clinical Microbiology and Infection, 18(7), 646-655.
Gao, L., Tan, Y., Zhang, X., Hu, J., Miao, Z., Wei, L., & Chai, T. (2015). Emissions of Escherichia coli carrying extended-spectrum β-lactamase resistance from pig farms to the surrounding environment. International Journal of Environmental Research and Public Health, 12(4), 4203–4213.
Hammerum, A. M., Larsen, J., Andersen, V. D., Lester, C. H., Skovgaard Skytte, T. S., Hansen, F., … Agersø, Y. (2014). Characterization of extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli obtained from Danish pigs, pig farmers and their families from farms with high or no consumption of third- or fourth-generation cephalosporins. Journal of Antimicrobial Chemotherapy, 69(10), 2650-2657.
Hanson, R., Kaneene, J. B., Padungtod, P., Hirokawa, K., & Zeno, C. (2002). Prevalence of Salmonella and E. coli, and their resistance to antimicrobial agents, in farming communities in northern Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health, 33(3), 120-126.
Hu, Y.-Y., Cai, J.-C., Zhou, H.-W., Chi, D., Zhang, X.-F., Chen, W.-L., … Chen, G.-X. (2013). Molecular typing of CTX-M-producing Escherichia coli isolates from environmental water, swine feces, specimens from healthy humans, and human patients. Applied and Environmental Microbiology, 79(19), 5988-5996.
Lee, W.-C., & Yeh, K.-S. (2017). Characteristics of extended-spectrum β-lactamase–producing Escherichia coli isolated from fecal samples of piglets with diarrhea in central and southern Taiwan in 2015. BMC Veterinary Research, 13(1), 66.
Li, S., Song, W., Zhou, Y., Tang, Y., Gao, Y., & Miao, Z. (2015). Spread of extended-spectrum beta-lactamase-producing Escherichia coli from a swine farm to the receiving river. Environmental Science and Pollution Research, 22(17), 13033-13037.

Liebana, E., Carattoli, A., Coque, T. M., Hasman, H., Magiorakos, A. P., Mevius, D., ... Threlfall, J. (2013). Public health risks of enterobacterial isolates producing extended-spectrum beta-lactamases or AmpC beta-lactamases in food and food-producing animals: an EU perspective of epidemiology, analytical methods, risk factors, and control options. Clinical Infectious Diseases, 56(7), 1030-1037.
Luvsansharav, U.-O., Hirai, I., Niki, M., Sasaki, T., Makimoto, K., Komalamisra, C., … Indrawattana, N. (2011). Analysis of risk factors for a high prevalence of extended-spectrum β-lactamase-producing Enterobacteriaceae in asymptomatic individuals in rural Thailand. Journal of Medical Microbiology, 60(5), 619-624.
Marshall, B. M., & Levy, S. B. (2011). Food animals and antimicrobials: Impacts on human health. Clinical Microbiology Reviews, 24(4), 718-733.
Nuangmek, A., Rojanathien, S., Chotinun, S., Yamsakul, P., Tadee, P., Thamlikitkul, V., … Patchanee, P. (2018). Antimicrobial resistance in ESBL-producing Escherichia coli isolated from layer and pig farms in Thailand. Acta Scientiae Veterinariae, 46, 1538.
Van Duin, D., & Paterson, D. (2016). Multidrug resistant bacteria in the community: trends and lessons learned. Infectious Disease Clinics of North America, 30(2), 377-390.
Smet, A., Martel, A., Persoons, D., Dewulf, J., Heyndrickx, M., Herman, L., … Butaye, P. (2010). Broad-spectrum beta-lactamases among Enterobacteriaceae of animal origin: molecular aspects, mobility and impact on public health. FEMS Microbiology Reviews, 34(3), 295-316.
Srisangkaew, S., & Vorachit, M. (2004). The optimum agent for screening and confirmatory tests for extended-spectrum beta-lactamases in Escherichia coli and Klebsiella pneumoniae in Ramathibodi Hospital, Thailand. Journal of Infectious Diseases and Antimicrobial Agents. 21(1), 1-5.
Tzouvelekis, L. S., Vatopoulos, A. C., Katsanis, G., Tzelepi, E. (1999). Rare case of failure by an automated system to detect extended-spectrum beta-lactamase in a cephalosporin-resistant Klebsiella pneumoniae isolate. Journal of Clinical Microbiology, 37(7), 2388.
Ur Rahman, S., Ali, T., Ali, I., Khan, N. A., Han, B., & Gao, J. (2018). The growing genetic and functional diversity of extended spectrum beta-lactamases. BioMed Research International, 2018(9519718), 14. https://doi. org/10.1155/2018/9519718.
Xu, G., An, W., Wang, H. & Zhang, X. (2015). Prevalence and characteristics of extended-spectrum β-lactamase genes in Escherichia coli isolated from piglets with post-weaning diarrhea in Heilongjiang province, China. Frontiers in Microbiology, 6, 1103.
Zhang, H., Zhai, Z., Li, Q., Liu, L., Guo, S., Li, Q., … Zhai, J. (2016). Characterization of extended-spectrum β-lactamase–producing Escherichia coli isolates from pigs and farm workers. Journal of Food Protection, 79(9), 1630-1634.

Research Articles


How to Cite
NUANMUANG, Narong et al. Phenotypic and Genotypic Characterization of Extended-Spectrum -Lactamase Producing Escherichia coli Isolated from Pig Feces in Farms, Muang Phayao. Naresuan University Journal: Science and Technology (NUJST), [S.l.], v. 26, n. 4, p. 17-25, nov. 2018. ISSN 2539-553X. Available at: <>. Date accessed: 15 apr. 2024. doi: