Yersiniosis is an important zoonotic disease; however, data are scarce on the resistance of enteropathogenic yersiniae, especially that of Y. pseudotuberculosis. Minimum inhibitory concentrations (MIC) of 21 antibiotics and 3 essential oils (EOs) were determined by broth microdilution for Y. enterocolitica bioserotype 4/O:3 strains isolated from domestic swine (n = 132) and Y. pseudotuberculosis strains isolated from wild boars (n = 46). For 15 of 21 antibiotics, statistically significant differences were found between MIC values of Y. enterocolitica and Y. pseudotuberculosis. While Y. enterocolitica was more resistant to amoxiclav, ampicillin, cefotaxime, cefuroxime, gentamicin, imipenem, meropenem, tetracycline, tobramycin, and trimethoprim, Y. pseudotuberculosis was more resistant to cefepime, ceftazidime, colistin, erythromycin, and nitrofurantoin. Statistically significant differences were found between various essential oils (p < 0.001) and species (p < 0.001). The lowest MICs for multiresistant Y. enterocolitica (n = 12) and Y. pseudotuberculosis (n = 12) were obtained for cinnamon (median 414 and 207 μg/mL, respectively) and oregano EOs (median 379 and 284 μg/mL), whereas thyme EO showed significantly higher MIC values (median 738 and 553 μg/mL; p < 0.001). There was no difference between Y. enterocolitica strains of plant (1A) and animal (4/O:3) origin (p = 0.855). The results show that Y. enterocolitica is generally more resistant to antimicrobials than Y. pseudotuberculosis.

Department of Animal Origin Food and Gastronomic Sciences Faculty of Veterinary Hygiene and Ecology University of Veterinary Sciences Brno 612 42 Brno Czech Republic

Zobrazit více v PubMed

EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control) The European Union One Health 2020 Zoonoses Report. EFSA J. 2021;19:6971. doi: 10.2903/j.efsa.2021.6971. PubMed DOI PMC

Cabanel N., Galimand M., Bouchier C., Chesnokova M., Klimov V., Carniel E. Molecular bases for multidrug resistance in Yersinia pseudotuberculosis. Int. J. Med. Microbiol. 2017;307:371–381. doi: 10.1016/j.ijmm.2017.08.005. PubMed DOI

Bancerz-Kisiel A., Szweda W. Yersiniosis—A zoonotic foodborne disease of relevance to public health. Ann. Agric. Environ. Med. 2015;22:397–402. doi: 10.5604/12321966.1167700. PubMed DOI

Fàbrega A., Ballesté-Delpierre C., Vila J. Antimicrobial Resistance in Yersinia enterocolitica. In: Chen C.-Y., Yan X., Jackson C.R., editors. Antimicrobial Resistance and Food Safety. 1st ed. Elsevier; Amsterdam, The Netherlands: 2015. pp. 77–104. Chapter 5. DOI

Koskinen J., Ortiz-Martinez P., Keto-Timonen R., Joutsen S., Fredriksson-Ahomaa M., Korkeala H. Prudent antimicrobial use is essential to prevent the emergence of antimicrobial resistance in Yersinia enterocolitica 4/O:3 strains in pigs. Front. Microbiol. 2022;13:841. doi: 10.3389/fmicb.2022.841841. PubMed DOI PMC

EUCAST (The European Committee on Antimicrobial Susceptibility Testing) Breakpoint Tables for Interpretation of MICs and Zone Diameters. Version 12.0. 2022. [(accessed on 11 February 2022)]. Available online: https://www.eucast.org/clinical_breakpoints.

Tavassoli M., Afshari A., Drăgănescu D., Arsene A.L., Burykina T.I., Rezaee R. Antimicrobial resistance of Yersinia enterocolitica in different foods. A review. Farmacia. 2018;66:399–407.

Mittal R.P., Rana A., Jaitak V. Essential oils: An impending substitute of synthetic antimicrobial agents to overcome antimicrobial resistance. Curr. Drug Targets. 2019;20:605–624. doi: 10.2174/1389450119666181031122917. PubMed DOI

Bonardi S., Bruini I., D’Incau M., Van Damme I., Carniel E., Brémont S., Cavallini P., Tagliabue S., Brindani F. Detection, seroprevalence and antimicrobial resistance of Yersinia enterocolitica and Yersinia pseudotuberculosis in pig tonsils in Northern Italy. Int. J. Food Microbiol. 2016;235:125–132. doi: 10.1016/j.ijfoodmicro.2016.07.033. PubMed DOI

Verbikova V., Borilova G., Babak V., Moravkova M. Prevalence, characterization and antimicrobial susceptibility of Yersinia enterocolitica and other Yersinia species found in fruits and vegetables from the European Union. Food Control. 2018;85:161–167. doi: 10.1016/j.foodcont.2017.08.038. DOI

EUCAST (The European Committee on Antimicrobial Susceptibility Testing) Broth Microdilution—EUCAST Reading Guide. Version 3.0. 2021. [(accessed on 24 January 2022)]. Available online: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Disk_test_documents/2022_manuals/Reading_guide_BMD_v_4.0_2022.pdf.

Hulankova R. The influence of liquid medium choice in determination of minimum inhibitory concentration of essential oils against pathogenic bacteria. Antibiotics. 2022;11:150. doi: 10.3390/antibiotics11020150. PubMed DOI PMC

R Core Team R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria. 2021. [(accessed on 27 April 2021)]. Available online: https://www.R-project.org/

Christensen R.H.B. Ordinal—Regression Models for Ordinal Data. R Package Version 2019.12-10. 2019. [(accessed on 10 August 2022)]. Available online: https://CRAN.R-project.org/package=ordinal.

Russel L. Emmeans: Estimated Marginal Means, aka Least-Squares Means. R Package Version 1.5.1. 2020. [(accessed on 7 May 2021)]. Available online: https://CRAN.R-project.org/package=emmeans,

Modesto P., De Ciucis C.G., Vencia W., Pugliano M.C., Mignone W., Berio E., Masotti C., Ercolini C., Serracca L., Andreoli T., et al. Evidence of antimicrobial resistance and presence of pathogenicity genes in Yersinia enterocolitica isolate from wild boars. Pathogens. 2021;10:398. doi: 10.3390/pathogens10040398. PubMed DOI PMC

Ossiprandi M.C., Zerbini L. Prevalence and antibiotic susceptibilities of pathogenic Yersinia enterocolitica strains in pigs slaughtered in northern Italy. J. Adv. Biol. 2014;5:603–609. doi: 10.24297/jab.v5i1.5354. DOI

Reinhardt M., Hammerl J.A., Kunz K., Barac A., Nöckler K., Hertwig S. Yersinia pseudotuberculosis prevalence and diversity in wild boars in Northeast Germany. Appl. Environ. Microbiol. 2018;84:e00675. doi: 10.1128/AEM.00675-18. PubMed DOI PMC

Kechagia N., Nicolaou C., Ioannidou V., Kourti E., Ioannidis A., Legakis N.J., Chatzipanagiotou S. Detection of chromosomal and plasmid-encoded virulence determinants in Yersinia enterocolitica and other Yersinia spp. isolated from food animals in Greece. Int. J. Food Microbiol. 2007;118:326–331. doi: 10.1016/j.ijfoodmicro.2007.07.044. PubMed DOI

Terentjeva M., Bẽrziņs A. Prevalence and antimicrobial resistance of Yersinia enterocolitica and Yersinia pseudotuberculosis in slaughter pigs in Latvia. J. Food Prot. 2010;73:1335–1338. doi: 10.4315/0362-028x-73.7.1335. PubMed DOI

Blomme S., Andre E., Delmée M., Verhaegen J. Antimicrobial susceptibility testing of Yersinia enterocolitica and Yersinia pseudotuberculosis; Proceedings of the 27th European Congress of Clinical Microbiology and Infectious Diseases; Vienna, Austria. 22–25 April 2017; p. 0521.

Simonova J., Borilova G., Steinhauserova I. Occurence of pathogenic strains of Yersinia enterocolitica in pigs and their antimicrobial resistance. Bull. Vet. Inst. Pulawy. 2008;52:39–43.

Bengoechea J.A., Lindner B., Seydel U., Díaz R., Moriyón I. Yersinia pseudotuberculosis and Yersinia pestis are more resistant to bactericidal cationic peptides than Yersinia enterocolitica. Microbiology. 1998;144:1509–1515. doi: 10.1099/00221287-144-6-1509. PubMed DOI

Durofil A., Maddela N.R., Naranjo R.A., Radice M. Evidence on antimicrobial activity of essential oils and herbal extracts against Yersinia enterocolitica—A review. Food Biosci. 2022;47:101712. doi: 10.1016/j.fbio.2022.101712. DOI

Ebani V.V., Nardoni S., Bertelloni F., Giovanelli S., Rocchigiani G., Pistelli L., Mancianti F. Antibacterial and antifungal activity of essential oils against some pathogenic bacteria and yeasts shed from poultry. Flavour Fragr. J. 2016;31:302–309. doi: 10.1002/ffj.3318. DOI

Görmez A., Yanmiş D., Bozari S., Gürkök S. Antibacterial activity of essential oils extracted from Satureja hortensis against selected clinical pathogens. AIP Conf. Proc. 2017;1833:020059. doi: 10.1063/1.4981707. DOI

Owen L., Laird K. Synchronous application of antibiotics and essential oils: Dual mechanisms of action as a potential solution to antibiotic resistance. Crit. Rev. Microbiol. 2018;44:414–435. doi: 10.1080/1040841X.2018.1423616. PubMed DOI

Pesingi P.V., Singh B.R., Pesingi P.K., Bhardwaj M., Singh S.V., Kumawat M., Sinha D.K., Gandham K.R. MexAB-OprM efflux pump of Pseudomonas aeruginosa offers resistance to carvacrol: A herbal antimicrobial agent. Front. Microbiol. 2019;10:2664. doi: 10.3389/fmicb.2019.02664. PubMed DOI PMC

Hulankova R., Borilova G. Modeling dependence of growth inhibition of Salmonella Typhimurium and Listeria monocytogenes by oregano or thyme essential oils on the chemical composition of minced pork. J Food Saf. 2020;40:e12818. doi: 10.1111/jfs.12818. DOI

Boskovic M., Djordjevic J., Ivanovic J., Janjic J., Zdravkovic N., Glisic M., Glamoclija N., Baltic B., Djordjevic V., Baltic M. Inhibition of Salmonella by thyme essential oil and its effect on microbiological and sensory properties of minced pork meat packaged under vacuum and modified atmosphere. Int. J. Food Microbiol. 2017;258:58–67. doi: 10.1016/j.ijfoodmicro.2017.07.011. PubMed DOI

Methods for Determination of Antimicrobial Activity of Essential Oils In Vitro-A Review