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Molecular characteristics of ESBL-producing Escherichia coli isolated from chickens with colibacillosis

  • Yoon, Sunghyun (College of Veterinary Medicine & Zoonoses Research Institute, Kyungpook National University) ;
  • Lee, Young Ju (College of Veterinary Medicine & Zoonoses Research Institute, Kyungpook National University)
  • Received : 2021.04.18
  • Accepted : 2022.02.03
  • Published : 2022.05.31

Abstract

Background: Avian pathogenic Escherichia coli (APEC) causes colibacillosis, resulting in significant economic losses in the poultry industry. Objectives: In this study, the molecular characteristics of two extended-spectrum beta-lactamase (ESBL)-producing APEC isolates were compared with previously reported ESBL-producing E. coli isolates. Methods: The molecular characteristics of E. coli isolates and the genetic environments of the ESBL genes were investigated using whole genome sequencing. Results: The two ESBL-producing APEC were classified into the phylogenetic groups C and B1 and ST410 and ST162, respectively. Moreover, the ESBL genes of the two isolates were harbored in different Inc plasmids. The EC1809182 strain, harboring the blaCTX-M-55 gene on the plasmid, exhibited extensive homology to IncFIB (98.4%) and IncFIC(FII) (95.8%). The EC1809191 strain, harboring the blaCTX-M-1 gene, was homologous to IncI1-I (Gamma) (99.3%). All chromosomes carried the multidrug transporter, mdf(A) gene. Mobile genetic elements, adjacent to CTX-M genes, facilitated the dissemination of genes in the two isolates, analogous to other ESBL-producing E. coli isolates. Conclusions: This study clarifies the transmission dynamics of CTX-M genes and supports strengthened surveillance to prevent the transmission of the antimicrobial-resistant genes to humans via the food chain.

Keywords

Acknowledgement

This work was supported by the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry (IPET) through the Agriculture, Food and Rural Affairs Convergence Technologies Program for Educating Creative Global Leader, funded by the Ministry of Agriculture, Food and Rural Affairs (MAFRA; 716002-7).

References

  1. Dziva F, Stevens MP. Colibacillosis in poultry: unravelling the molecular basis of virulence of avian pathogenic Escherichia coli in their natural hosts. Avian Pathol. 2008;37(4):355-366. https://doi.org/10.1080/03079450802216652
  2. Jeong YW, Kim TE, Kim JH, Kwon HJ. Pathotyping avian pathogenic Escherichia coli strains in Korea. J Vet Sci. 2012;13(2):145-152. https://doi.org/10.4142/jvs.2012.13.2.145
  3. Kwon HJ, Seong WJ, Kim JH. Molecular prophage typing of avian pathogenic Escherichia coli. Vet Microbiol. 2013;162(2-4):785-792. https://doi.org/10.1016/j.vetmic.2012.10.005
  4. Sola-Gines M, Cameron-Veas K, Badiola I, Dolz R, Majo N, Dahbi G, et al. Diversity of multi-drug resistant avian pathogenic Escherichia coli (APEC) Causing outbreaks of colibacillosis in broilers during 2012 in Spain. PLoS One. 2015;10(11):e0143191. https://doi.org/10.1371/journal.pone.0143191
  5. Ozaki H, Matsuoka Y, Nakagawa E, Murase T. Characteristics of Escherichia coli isolated from broiler chickens with colibacillosis in commercial farms from a common hatchery. Poult Sci. 2017;96(10):3717-3724. https://doi.org/10.3382/ps/pex167
  6. Roth N, Kasbohrer A, Mayrhofer S, Zitz U, Hofacre C, Domig KJ. The application of antibiotics in broiler production and the resulting antibiotic resistance in Escherichia coli: a global overview. Poult Sci. 2019;98(4):1791-1804. https://doi.org/10.3382/ps/pey539
  7. Adator EH, Walker M, Narvaez-Bravo C, Zaheer R, Goji N, Cook SR, et al. Whole genome sequencing differentiates presumptive extended spectrum beta-lactamase producing Escherichia coli along segments of the one health continuum. Microorganisms. 2020;8(3):E448.
  8. Carattoli A, Villa L, Fortini D, Garcia-Fernandez A. Contemporary IncI1 plasmids involved in the transmission and spread of antimicrobial resistance in Enterobacteriaceae. Plasmid. 2021;118:102392. https://doi.org/10.1016/j.plasmid.2018.12.001
  9. Quainoo S, Coolen JP, van Hijum SA, Huynen MA, Melchers WJ, van Schaik W, et al. Whole-genome sequencing of bacterial pathogens: the future of nosocomial outbreak analysis. Clin Microbiol Rev. 2017;30(4):1015-1063. https://doi.org/10.1128/CMR.00016-17
  10. Kim YB, Yoon MY, Ha JS, Seo KW, Noh EB, Son SH, et al. Molecular characterization of avian pathogenic Escherichia coli from broiler chickens with colibacillosis. Poult Sci. 2020;99(2):1088-1095. https://doi.org/10.1016/j.psj.2019.10.047
  11. Clinical and Laboratory Standards Institute. Clinical and Laboratory Standards Institute Standards Development Policies and Process [Internet]. Wayne: Clinical and Laboratory Standards Institute; https://clsi.org/media/1711/clsistandardsdevelopmentpoliciesandprocessesfinal.pdf. Updated 2013. Accessed 2020 Oct 1.
  12. Pitout JD, Hossain A, Hanson ND. Phenotypic and molecular detection of CTX-M-β-lactamases produced by Escherichia coli and Klebsiella spp. J Clin Microbiol. 2004;42(12):5715-5721. https://doi.org/10.1128/JCM.42.12.5715-5721.2004
  13. Brinas L, Zarazaga M, Saenz Y, Ruiz-Larrea F, Torres C. β-lactamases in ampicillin-resistant Escherichia coli isolates from foods, humans, and healthy animals. Antimicrob Agents Chemother. 2002;46(10):3156-3163. https://doi.org/10.1128/AAC.46.10.3156-3163.2002
  14. Zhang J, Zheng B, Zhao L, Wei Z, Ji J, Li L, et al. Nationwide high prevalence of CTX-M and an increase of CTX-M-55 in Escherichia coli isolated from patients with community-onset infections in Chinese county hospitals. BMC Infect Dis. 2014;14(1):659. https://doi.org/10.1186/s12879-014-0659-0
  15. Tadesse DA, Li C, Mukherjee S, Hsu CH, Bodeis Jones S, Gaines SA, et al. Whole-genome sequence analysis of CTX-M containing Escherichia coli isolates from retail meats and cattle in the United States. Microb Drug Resist. 2018;24(7):939-948. https://doi.org/10.1089/mdr.2018.0206
  16. Tamang MD, Nam HM, Gurung M, Jang GC, Kim SR, Jung SC, et al. Molecular characterization of CTX-M β-lactamase and associated addiction systems in Escherichia coli circulating among cattle, farm workers, and the farm environment. Appl Environ Microbiol. 2013;79(13):3898-3905. https://doi.org/10.1128/AEM.00522-13
  17. Hayashi W, Ohsaki Y, Taniguchi Y, Koide S, Kawamura K, Suzuki M, et al. High prevalence of blaCTX-M-14 among genetically diverse Escherichia coli recovered from retail raw chicken meat portions in Japan. Int J Food Microbiol. 2018;284(August):98-104. https://doi.org/10.1016/j.ijfoodmicro.2018.08.003
  18. Hoang TA, Nguyen TN, Ueda S, Le QP, Tran TT, Nguyen TN, et al. Common findings of blaCTX-M-55-encoding 104-139 kbp plasmids harbored by extended-spectrum β-lactamase-producing Escherichia coli in pork meat, wholesale market workers, and patients with urinary tract infection in Vietnam. Curr Microbiol. 2017;74(2):203-211. https://doi.org/10.1007/s00284-016-1174-x
  19. Bennett PM. Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. Br J Pharmacol. 2008;153(Suppl 1):S347-S357. https://doi.org/10.1038/sj.bjp.0707607
  20. Cormier A, Zhang PL, Chalmers G, Weese JS, Deckert A, Mulvey M, et al. Diversity of CTX-M-positive Escherichia coli recovered from animals in Canada. Vet Microbiol. 2019;231(February):71-75. https://doi.org/10.1016/j.vetmic.2019.02.031
  21. Agyepong N, Govinden U, Owusu-Ofori A, Amoako DG, Allam M, Janice J, et al. Genomic characterization of multidrug-resistant ESBL-producing Klebsiella pneumoniae isolated from a Ghanaian teaching hospital. Int J Infect Dis. 2019;85(85):117-123. https://doi.org/10.1016/j.ijid.2019.05.025
  22. Rozwandowicz M, Brouwer MS, Fischer J, Wagenaar JA, Gonzalez-Zorn B, Guerra B, et al. Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. J Antimicrob Chemother. 2018;73(5):1121-1137. https://doi.org/10.1093/jac/dkx488
  23. Leverstein-van Hall MA, Dierikx CM, Cohen Stuart J, Voets GM, van den Munckhof MP, van Essen-Zandbergen A, et al. Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect. 2011;17(6):873-880. https://doi.org/10.1111/j.1469-0691.2011.03497.x
  24. Coburn PS, Baghdayan AS, Dolan GT, Shankar N. Horizontal transfer of virulence genes encoded on the Enterococcus faecalis pathogenicity island. Mol Microbiol. 2007;63(2):530-544. https://doi.org/10.1111/j.1365-2958.2006.05520.x
  25. Vidana R, Rashid MU, Ozenci V, Weintraub A, Lund B. The origin of endodontic Enterococcus faecalis explored by comparison of virulence factor patterns and antibiotic resistance to that of isolates from stool samples, blood cultures and food. Int Endod J. 2016;49(4):343-351. https://doi.org/10.1111/iej.12464
  26. Guabiraba R, Schouler C. Avian colibacillosis: still many black holes. FEMS Microbiol Lett. 2015;362(15):fnv118. https://doi.org/10.1093/femsle/fnv118
  27. Huang J, Ma S, Yu Q, Fu M, Shao L, Shan X, et al. Whole genome sequence of an Escherichia coli ST410 isolate co-harbouring blaNDM-5, blaOXA-1, blaCTX-M-15, blaCMY-2, aac(3)-IIa and aac(6')-Ib-cr genes isolated from a patient with bloodstream infection in China. J Glob Antimicrob Resist. 2019;19:354-355. https://doi.org/10.1016/j.jgar.2019.10.027
  28. Roer L, Overballe-Petersen S, Hansen F, Schonning K, Wang M, Roder BL, et al. Escherichia coli sequence type 410 is causing new international high-risk clones. MSphere. 2018;3(4):e00337-18.
  29. Zurita J, Yanez F, Sevillano G, Ortega-Paredes D, Paz Y Mino A. Ready-to-eat street food: a potential source for dissemination of multidrug-resistant Escherichia coli epidemic clones in Quito, Ecuador. Lett Appl Microbiol. 2020;70(3):203-209. https://doi.org/10.1111/lam.13263
  30. Guzman-Otazo J, Gonzales-Siles L, Poma V, Bengtsson-Palme J, Thorell K, Flach CF, et al. Diarrheal bacterial pathogens and multi-resistant enterobacteria in the Choqueyapu River in La Paz, Bolivia. PLoS One. 2019;14(1):e0210735. https://doi.org/10.1371/journal.pone.0210735