Antimicrobial resistance of Shiga toxin‐producing Escherichia coli isolated from sheep
DOI:
https://doi.org/10.11606/issn.1678-4456.bjvras.2022.196807Keywords:
STEC, Antibiotic, Beta-lactamases, Zoonoses, ToxinsAbstract
The presence of Shiga toxin-producing Escherichia coli (STEC) and resistance to beta-lactams in healthy sheep represents a potential public health risk. This study aimed to characterize STEC isolates in sheep feces for toxin production and resistance to beta lactam antibiotics. In the present study, among the 40 isolates, we found a predominance of subtype Stx1 (22/40), followed by subtype Stx1 + Stx2 (11/40), while the less prevalent group was Stx2 (7/40). Also, we found phenotypical resistance to beta-lactam antibiotics in 50% (20/40) of the strains analyzed, forming two groups, one with resistant isolates and the other with non-resistant isolates. The cytotoxicity of the isolates did not vary among the groups. In addition to having this characteristic, some multiresistant isolates produced significant amounts of toxins. This leads to the conclusion that the mechanisms of antimicrobial resistance via beta lactamases are present in sheep STEC and that the cytotoxicity of those isolates is variable regarding such resistance.
Downloads
References
Amézquita-López BA, Soto-Beltrán M, Lee BG, Yambao JC, Quiñones B. Isolation, genotyping and antimicrobial resistance of Shiga toxin-producing Escherichia coli. J Microbiol Immunol Infect. 2018;51(4):425-34. http://dx.doi.org/10.1016/j.jmii.2017.07.004. PMid:28778595.
Beceiro A, Tomás M, Bou G. Antimicrobial resistance and virulence: a successful or deleterious association in the bacterial world? Clin Microbiol Rev. 2013;26(2):185-230. http://dx.doi.org/10.1128/CMR.00059-12. PMid:23554414.
Caldorin M, Almeida I, Peresi JTM, Alves EC. Ocorrência de Escherichia coli produtora de toxina Shiga (STEC) no Brasil e sua importância em saúde pública. BEPA, Bol Epidemiol Paul [Internet]. 2013 Feb [cited 2022 Oct 24];10(110):4-20. Available from: http://www.saude.sp.gov.br/resources/ccd/homepage/bepa/edicoes-2013/bepa_110.pdf.
Clinical and Laboratory Standards Institute. M100: performance standards for antimicrobial susceptibility testing. 28th ed. Malvern (PA, USA): Clinical and Laboratory Standards Institute; 2018. Colello R, Etcheverría AI, Conza JAD, Gutkind GO, Padola NL. Antibiotic resistance and integrons in Shiga toxin-producing Escherichia coli (STEC). Braz J Microbiol. 2015;46(1):1- 5. http://dx.doi.org/10.1590/S1517-838246120130698. PMid:26221083.
Coura FM, Lage AP, Heinemann MB. Patotipos de Escherichia coli causadores de diarreia em bezerros: uma atualização. Pesq Vet Bras. 2014;34(9):811-8. http://dx.doi.org/10.1590/S0100736X2014000900001.
Escobar‐Páramo P, Menac’h A, Gall T, Amorin C, Gouriou S, Picard B, Skurnik D, Denamur E. Identification of forces shaping the commensal Escherichia coli genetic structure by comparing animal and human isolates. Environ Microbiol. 2006;8(11):1975-84. http://dx.doi.org/10.1111/j.1462-2920.2006.01077.x. PMid:17014496.
Ferhat L, Chahed A, Hamrouche S, Korichi‐Ouar M, Hamdi TM. Research and molecular characteristic of Shiga toxin‐ producing Escherichia coli isolated from sheep carcasses. Lett Appl Microbiol. 2019;68(6):546-52. http://dx.doi.org/10.1111/lam.13142. PMid:30801745.
Furlan JPR, Gallo IFL, Campos ACLP, Navarro A, Kobayashi RKT, Nakazato G, Stehling EG. Characterization of non-O157 Shiga toxin-producing Escherichia coli (STEC) obtained from feces of sheep in Brazil. World J Microbiol Biotechnol. 2019;35(9):134. http://dx.doi.org/10.1007/s11274-019-2712-z. PMid:31432266.
Holt GS, Lodge JK, Mccarthy AJ, Graham AK, Young G, Bridge SH, Brown AK, Veses-Garcia M, Lanyon CV, Sails A, Allison HE, Smith DL. Shigatoxin encoding Bacteriophage ϕ24 B modulates bacterial metabolism to raise antimicrobial tolerance. Sci Rep. 2017;7(1):40424. http://dx.doi.org/10.1038/srep40424. PMid:28106081.
Jajarmi M, Fooladi AAI, Badouei MA, Ahmadi A. Virulence genes, Shiga toxin subtypes, major O-serogroups, and phylogenetic background of Shiga toxin-producing Escherichia coli strains isolated from cattle in Iran. Microb Pathog. 2017;109:274-9. http://dx.doi.org/10.1016/j.micpath.2017.05.041. PMid:28578089.
Kong L-C, Wang B, Wang Y-M, Hu R-G, Atiewin A, Gao D, Gao Y-H, Ma H-X. Characterization of bacterial community changes and antibiotic resistance genes in lamb manure of different incidence. Sci Rep. 2019;9(1):10101. http://dx.doi.org/10.1038/s41598-019-46604-y. PMid:31300748.
Leekitcharoenphon P, Johansson MHK, Munk P, Malorny B, Skarżyńska M, Wadepohl K, Moyano G, Hesp A, Veldman KT, Bossers A, Zając M, Wasyl D, Sanders P, GonzalezZorn B, Brouwer MSM, Wagenaar JA, Heederik DJJ, Mevius D, Aarestrup FM. Genomic evolution of antimicrobial resistance in Escherichia coli. Sci Rep. 2021;11(1):15108. http://dx.doi.org/10.1038/s41598-021-93970-7. PMid:34301966.
Liebana E, Carattoli A, Coque TM, Hasman H, Magiorakos A-P, Mevius D, Peixe L, Poirel L, Schuepbach-Regula G, Torneke K, Torren-Edo J, Torres C, Threlfall J. Public health risks of enterobacterial isolates producing extended-spectrum β-lactamases or AmpC β-lactamases in food and foodproducing animals: an EU perspective of epidemiology, analytical methods, risk factors, and control options. Clin Infect Dis. 2013;56(7):1030-7. http://dx.doi.org/10.1093/cid/cis1043. PMid:23243183.
Liu Y, Li H, Chen X, Tong P, Zhang Y, Zhu M, Su Z, Yao G, Li G, Cai W. Characterization of Shiga toxin‐producing Escherichia coli isolated from Cattle and Sheep in Xinjiang province, China, using whole‐genome sequencing. Transbound Emerg Dis. 2022;69(2):413-22. http://dx.doi.org/10.1111/tbed.13999. PMid:33480086.
Loiko MR, Paula CMD, Langone ACJ, Rodrigues RQ, Cibulski S, Rodrigues RO, Camargo AC, Nero LA, Mayer FQ, Tondo EC. Genotypic and antimicrobial characterization of pathogenic bacteria at different stages of cattle slaughtering in southern Brazil. Meat Sci. 2016;116:193-200. http://dx.doi.org/10.1016/j.meatsci.2016.01.010. PMid:26896744.
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, OlssonLiljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268- 81. http://dx.doi.org/10.1111/j.1469691.2011.03570.x. PMid:21793988.
Martins FH, Guth BEC, Piazza RM, Leao SC, Ludovico A, Ludovico MS, Dahbi G, Marzoa J, Mora A, Blanco J, Pelayo JS. Diversity of Shiga toxin-producing Escherichia coli in sheep flocks of Paraná State, southern Brazil. Vet Microbiol. 2015;175(1):150-6. http://dx.doi.org/10.1016/j.vetmic.2014.11.003. PMid:25465174.
Melton-Celsa AR. Shiga toxin (Stx) classification, structure, and function. Microbiol Spectr. 2014;2(4):2-4. http://dx.doi.org/10.1128/microbiolspec.EHEC-0024-2013. PMid:25530917.
Oporto B, Ocejo M, Alkorta M, Marimón JM, Montes M, Hurtado A. Zoonotic approach to Shiga toxin-producing Escherichia coli: integrated analysis of virulence and antimicrobial resistance in ruminants and humans. Epidemiol Infect. 2019;147:e164. http://dx.doi.org/10.1017/S0950268819000566. PMid:31063106.
Otero V, Sánchez S, Herrera-León S, Rodríguez-Calleja JM, Otero A, García-López ML, Santos JA. Detection and characterization of Shiga toxin-producing Escherichia coli (STEC) in bulk tank ewes’ milk and sheep farm environment. Small Rumin Res. 2017;154:110-4. http://dx.doi.org/10.1016/j.smallrumres.2017.08.002.
Pereira MCS, Rigueiro ALN, Ono RK, Rigobelo EC. Evaluation of antimicrobial resistance patterns in Escherichia coli strains, carriers or not carriers of stx1, stx2 and eae genes. Rev Acad.: C. Agrar. Amb. 2014;12(4):270-6.
Puii LH, Dutta TK, Roychoudhury P, Kylla H, Chakraborty S, Mandakini R, Kawlni L, Samanta I, Bandopaddhay S, Singh SB. Extended spectrum beta‐lactamase producing Shiga‐toxin producing‐Escherichia coli in piglets, humans and water sources in North East region of India. Lett Appl Microbiol. 2019;69(5):373-8. http://dx.doi.org/10.1111/lam.13216. PMid:31506974.
Rocha LB, Luz DE, Moraes CTP, Caravelli A, Fernandes I, Guth BEC, Horton DSPQ, Piazza RMF. Interaction between Shiga toxin and monoclonal antibodies: binding characteristics and in vitro neutralizing abilities. Toxins. 2012;4(9):729-47. http://dx.doi.org/10.3390/toxins4090729. PMid:23105978.
Santana TCFS, Maião RC, Monteiro SG, Carmo MS, Figueiredo PDMS. Perfil de resistência de Escherichia coli e Klebsiella spp isoladas de urocultura de comunidade do município de São Luis-MA no período de 2005-2008. Rev Patol Trop. 2012;41(3):295-303. http://dx.doi.org/10.5216/rpt.v41i3.20754.
Skarżyńska M, Leekitcharoenphon P, Hendriksen RS, Aarestrup FM, Wasyl D. A metagenomic glimpse into the gut of wild and domestic animals: quantification of antimicrobial resistance and more. PLoS One. 2020;15(12):e0242987. http://dx.doi.org/10.1371/journal.pone.0242987. PMid:33270717.
Stella AE, Luz D, Piazza RMF, Spira B. ppGpp and cytotoxicity diversity in Shiga toxin-producing Escherichia coli (STEC) isolates. Epidemiol Infect. 2017;145(11):2204-11. http://dx.doi.org/10.1017/S0950268817001091. PMid:28587697.
Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Teillant A, Laxminarayan R. Global trends in antimicrobial use in food animals. Proc Natl Acad Sci USA. 2015;112(18):5649-54. http://dx.doi.org/10.1073/pnas.1503141112. PMid:25792457.
Van Den Brom R, Jong AD, Van Engelen E, Heuvelink A, Vellema P. Zoonotic risks of pathogens from sheep and their milk borne transmission. Small Rumin Res. 2020;189:106123. http://dx.doi.org/10.1016/j.smallrumres.2020.106123. PMid:32427176.
Vidal M, Kruger E, Durán C, Lagos R, Levine M, Prado V, Toro C, Vidal R. Single multiplex PCR assay to identify simultaneously the six categories of diarrheagenic Escherichia coli associated with enteric infections. J Clin Microbiol. 2005;43(10):5362-5. http://dx.doi.org/10.1128/JCM.43.10.5362-5365.2005. PMid:16208019.
Woodford N, Fagan EJ, Ellington MJ. Multiplex PCR for rapid detection of genes encoding CTX-M extended-spectrum β-lactamases. J Antimicrob Chemother. 2006;57(1):154- 5. http://dx.doi.org/10.1093/jac/dki412. PMid:16284100.
Yang R, Abraham S, Gardner GE, Ryan U, Jacobson C. Salmonella enterica and Escherichia coli O157/O145 serogroup in sheep faeces collected at sale yards and in abattoir effluent in Western Australia. Aust Vet J. 2017;95(5):143-8. http://dx.doi.org/10.1111/avj.12572. PMid:28444752.
Yu X, Tang X, Zuo J, Zhang M, Chen L, Li Z. Distribution and persistence of cephalosporins in cephalosporin producing wastewater using SPE and UPLC–MS/MS method. Sci Total Environ. 2016;569-570:23-30. http://dx.doi.org/10.1016/j.scitotenv.2016.06.113. PMid:27328396.
Zaheri H, Ghanbarpour R, Jajarmi M, Bagheri M, Ghanadian A, Badouei MA. Public health aspects of Shiga toxinproducing Escherichia coli (STEC) strains in sheep and goats of Bakhtiari pastoral tribe, Iran. Trop Anim Health Prod. 2020;52(5):2721-4. http://dx.doi.org/10.1007/s11250-020-02245-2. PMid:32125596.
Downloads
Published
Issue
Section
License
Copyright (c) 2023 Brazilian Journal of Veterinary Research and Animal Science
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
The journal content is authorized under the Creative Commons BY-NC-SA license (summary of the license: https://