Antimicrobial Resistance in ESBL-Producing Escherichia coli Isolated from Layer and Pig Farms in Thailand


  • Aniroot Nuangmek Graduate Program in Veterinary Science, Faculty of Veterinary Medicine (FVM), Chiang Mai University (CMU), Chiang Mai, Thailand. Phayao Provincial Livestock Office, Phayao, Thailand.
  • Suvichai Rojanasthien Integrative Research Center for Veterinary Preventive Medicine, FVM-CMU, Chiang Mai.
  • Suwit Chotinun Integrative Research Center for Veterinary Preventive Medicine, FVM-CMU, Chiang Mai.
  • Panuwat Yamsakul Integrative Research Center for Veterinary Preventive Medicine, FVM-CMU, Chiang Mai.
  • Pakpoom Tadee Integrative Research Center for Veterinary Preventive Medicine, FVM-CMU, Chiang Mai.
  • Visanu Thamlikitkul Division of Infectious Diseases and Tropical Medicine, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University (MU), Bangkok, Thailand.
  • Nattasit Tansakul Department of Pharmacology, FVM, Kasetsart University (KU), Bangkok.
  • Prapas Patchanee Integrative Research Center for Veterinary Preventive Medicine, FVM-CMU, Chiang Mai.



Background: Study of drug resistance of commensal bacteria in both humans and animals can determine the scale of the drug resistance problem. Usage of antimicrobials to treat infections in humans and animals has generated extensive antimicrobial pressure not only on targeted pathogens but also on commensal bacteria. Commensal Escherichia coli appears to be the major reservoir for resistant genes implicated in the transmission of genetic traits from one bacterium to another. Antimicrobial resistance in Enterobacteriaceae has increased dramatically worldwide in the last decade. An increasing number of community-onset extended-spectrum beta-lactamase (ESBL)-producing bacterial infections, especially those caused by ESBL-producing E. coli, have been reported in many countries, including Thailand. Moreover, ESBL-producing E. coli have been widely detected in food-producing animals and the environment. The increased use of ESBLs in food animals is a serious public health problem. The objective of the study was to determine the prevalence and antimicrobial resistance pattern of ESBL-producing E. coli isolated from pigs, layers, farm workers and stagnant water, in order to increase awareness about antimicrobial usage on farms and to minimize the expansion of the antimicrobial resistance phenomenon in farm settings.

Materials, Methods & Results: A total of 588 samples were collected from 107 pig farms and 89 layer farms in Chiang Mai–Lamphun and Chon Buri provinces during May 2015-April 2016. Double-disk diffusion method according to EUCAST (European Committee on Antimicrobial Susceptibility Testing) guidelines was used for detection. The results demonstrated that 36.7% (216/588) of samples were ESBL-producing E. coli-positive, including rectal swabs 74.8% (80/107), pig farm worker stool swabs 57.0% (61/107), stagnant water on pig farms 21.5% (23/107), healthy layer rectal swabs 6.7% (6/89) and layer farm worker stool swabs 51.7% (46/89). Most of the isolates were resistant against ampicillin (99.5%), followed by erythromycin (98.6%) and ceftriaxone (96.3%). All of them were classified as multidrug-resistant strains. Moreover, AMP-CRO-E-TE-C-SXT-CN was the most frequent phenotype pattern detected in animals, humans and the environment, followed by AMP-CRO-E-TE-C-SXT-NA-CN.

Discussion: The present study offers clear evidence that the prevalence of ESBL-producing E. coli in healthy pigs is higher than in layers. One possible explanation is that a large amount and variety of antimicrobials are used on pig farms, resulting in a common and significant source of drug-resistant ESBL-producing E. coli. The lower incidence of ESBL-producing E. coli in samples from a pig farm environment than in samples of animal origin indicate that pigs are a reservoir of a reservoir for resistant bacteria and a source of environmental contamination. Antimicrobial resistance patterns of ESBLproducing E. coli detected in all sample types and study locations were quite similar. In almost all ESBL-producing E. coli isolates, resistance was shown against ampicillin, erythromycin, ceftriaxone, tetracycline and chloramphenicol. Moreover, multidrug resistance was found in all isolates of ESBL-producing E. coli. The differences in antimicrobial agent resistance patterns can be used to differentiate sources by employing analytical tools such as discriminant function analysis. A molecular typing protocol is recommended for use in a discriminant function analysis for pattern determination of pathogen spreading. However, genetic fingerprinting techniques for microbial source tracking are more expensive, and facilities with appropriate equipment and expertise are required.


Download data is not yet available.


Animal Health Products Association. 2013. AHPA Market information. Samut Sakhon: A.T. Printing Co., 451p.

Biswas S., Brunel J.M., Dubus J.C., Reynaud-Gaubert M. & Rolain J.M. 2012. Colistin: an update on the antibiotic of the 21st century. Expert Review of Anti-Infective Therapy. 10(8): 917-934.

Boonyasiri A., Tangkoskul T., Seenama C., Saiyarin J., Tiengrim S. & Thamlikitkul V. 2014. Prevalence of antibiotic resistant bacteria in healthy adults, foods, food animals, and the environment in selected areas in Thailand. Pathogens and Global Health. 108(5): 235-245.

Cameron A. & McAllister T.A. 2016. Antimicrobial usage and resistance in beef production. Journal of Animal Science and Biotechnology. 7: 68.

Cantón R., Novais A., Valverde A., Machado E., Peixe L., Baquero F. & Coque T.M. 2008. Prevalence and spread of extended-spectrum beta-lactamase-producing Enterobacteriaceae in Europe. Clinical Microbiology and Infection. 14(1): 144-153.

Carattoli A. 2008. Animal reservoirs for extended spectrum beta-lactamase producers. Clinical Microbiology and Infection. 14(1): 117-123.

Centers for Disease Control and Prevention. Epi Info™. 2014. Available at: < htm.>. [Accessed online in December 2014].

Clinical and Laboratory Standards Institute. 2013. Performance standards for antimicrobial susceptibility testing; twenty-first informational supplement (CLSI document M100-S21). Wayne: CLSI, 163p.

Coque T.M., Baquero F. & Canton R. 2008. Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe. Eurosurveillance. 13(47): 19044.

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).

Department of Livestock Development, Thailand. 2013. Thai livestock farmer database system. Available at: . [Accessed online in December 2016].

European Committee on Antimicrobial Susceptibility Testing. 2013. EUCAST guidelines for detection of resistance mechanisms and specific resistances of clinical and/or epidemiological importance. pp.11-19. Available at: . [Accessed online in September 2014].

Gandra S., Barter D.M. & Laxminarayan R. 2014. Economic burden of antibiotic resistance: how much do we really know? Clinical Microbiology and Infection. 20(10): 973-980.

Geser N., Stephan R. & Hächler H. 2012. Occurrence and characteristics of extended-spectrum β-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Veterinary Research. 8: 21.

Hiroi M., Yamazaki F., Harada T., Takahashi N., Iida N., Noda Y., Yagi M., Nishio T., Kanda T., Kawamori F., Sugiyama K., Masuda T., Hara-Kudo Y. & Ohashi N. 2012. Prevalence of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae in food-producing animals. Journal of Veterinary Medical Science. 74(2): 189-195.

Horton R.A., Randall L.P., Snary E.L., Cockrem H., Lotz S., Wearing H., Duncan D., Rabie A., McLaren I., Watson E., La Ragione R.M. & Coldham N.G. 2011. Fecal carriage and shedding density of CTX-M extended-spectrum ß-lactamase-producing Escherichia coli in cattle, chickens, and pigs: implications for environmental contamination and food production. Applied and Environmental Microbiology. 77(11): 3715-3719.

Kelly B.G, Vespermann A. & Bolton D.J. 2009. The role of horizontal gene transfer in the evolution of selected foodborne bacterial pathogens. Food and Chemical Toxicology. 47(5): 951-968.

Liu Y.Y., Wang Y., Walsh T.R., Yi L.X., Zhang R., Spencer J., Doi Y., Tian G., Dong B., Huang X., Yu L.F., Gu D., Ren H., Chen X., Lv L., He D., Zhou H., Liang Z., Liu J.H. & Shen J. 2016. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infectious Diseases. 16(2): 161-168.

Luvsansharav U.O., Hirai I., Niki M., Sasaki T., Makimoto K., Komalamisra C., Maipanich W., Kusolsuk T., Sa-Nguankiat S., Pubampen S. & Yamamoto Y. 2011. Analysis of risk factors for a high prevalence of extendedspectrum β-lactamase-producing Enterobacteriaceae in asymptomatic individuals in rural Thailand. Journal of Medical Microbiology. 60: 619-624.

Ministry of Agriculture and Cooperatives, Thailand. 2002. Announcement of the Ministry of Agriculture and Cooperatives. B.E. 2545. Dated 4th June B.E. 2545 (2002), 2p. Available at: < law/announce_animalfeed2545.pdf>. [Accessed online in March 2017].

Ministry of Agriculture and Cooperatives, Thailand. 2003. Announcement of the Ministry of Agriculture and Cooperatives. B.E. 2546. Dated 4th June B.E. 2546 (2003). Available at:: <>. [Accessed online in December 2016].

Sasaki T., Hirai I., Niki M., Nakamura T., Komalamisra C., Maipanich W., Kusolsuk T., Sa-Nguankiat S., Pubampen S. & Yamamoto Y. 2010. High prevalence of CTX-M beta-lactamase-producing Enterobacteriaceae in stool specimens obtained from healthy individuals in Thailand. Journal of Antimicrobial Chemotherapy. 65(4): 666-668.

Sayah R.S., Kaneene J.B., Johnson Y., Miller R. 2005. Patterns of antimicrobial resistance observed in Escherichia coli isolates obtained from domestic- and wild-animal fecal samples, human septage, and surface water. Applied and Environmental Microbiology. 71(3): 1394-1404.

Smet A., Martel A., Persoons D., Dewulf J., Heyndrickx M., Herman L., Haesebrouck F. & Butaye P. 2010. Broad-spectrum β-lactamases among Enterobacteriaceae of animal origin: molecular aspects, mobility and impact on public health. FEMS Microbiology Reviews. 34(3): 295-316.

World Health Organization. 2001. Global Strategy for Containment of Antimicrobial Resistance. Geneva: WHO, 99p.



How to Cite

Nuangmek, A., Rojanasthien, S., Chotinun, S., Yamsakul, P., Tadee, P., Thamlikitkul, V., Tansakul, N., & Patchanee, P. (2018). Antimicrobial Resistance in ESBL-Producing Escherichia coli Isolated from Layer and Pig Farms in Thailand. Acta Scientiae Veterinariae, 46(1), 8.