{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,30]],"date-time":"2026-06-30T04:36:26Z","timestamp":1782794186160,"version":"3.54.5"},"reference-count":48,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2024,3,6]],"date-time":"2024-03-06T00:00:00Z","timestamp":1709683200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of Science, Technological Development and Innovation of the Republic of Serbia","award":["451-03-66\/2024-03\/200031"],"award-info":[{"award-number":["451-03-66\/2024-03\/200031"]}]},{"name":"Ministry of Science, Technological Development and Innovation of the Republic of Serbia","award":["142-451-3498\/2023-01\/01"],"award-info":[{"award-number":["142-451-3498\/2023-01\/01"]}]},{"name":"Provincial Secretariat for Higher Education and Scientific Research, Republic of Serbia, Autonomous Province of Vojvodina","award":["451-03-66\/2024-03\/200031"],"award-info":[{"award-number":["451-03-66\/2024-03\/200031"]}]},{"name":"Provincial Secretariat for Higher Education and Scientific Research, Republic of Serbia, Autonomous Province of Vojvodina","award":["142-451-3498\/2023-01\/01"],"award-info":[{"award-number":["142-451-3498\/2023-01\/01"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Foods"],"abstract":"<jats:p>Yersiniosis, one of the leading foodborne infections in the European Union, is caused by Yersinia enterocolitica. In this study, the antibacterial and antibiofilm effects of cinnamon (Cinnamomum zeylanicum Nees), clove (Syzygium aromaticum L.), oregano (Origanum vulgare L.), rosemary (Rosmarinus officinalis L.), thyme (Thymus vulgaris L.), and winter savory (Satureja montana L.) essential oils were investigated against Y. enterocolitica strains belonging to the bioserotype 4\/O:3. Cinnamon essential oil showed the highest antibacterial activity, with an MIC value 0.09 \u00b5L\/mL, followed by oregano and thyme essential oils, with MIC values from 0.09 to 0.18 \u00b5L\/mL, and from 0.18 to 0.23 \u00b5L\/mL, respectively. Thyme essential oil at 0.23 \u00b5L\/g (MIC) and at 0.46 \u00b5L\/g (2MIC) significantly (p &lt; 0.05) reduced the number of Y. enterocolitica by 0.38 log CFU\/g and 0.64 log CFU\/g, respectively, in minced pork meat during storage at 4 \u00b0C for 4 days. The Y. enterocolitica strains formed biofilms at 15 \u00b0C and 37 \u00b0C in tryptic soy broth and Luria\u2013Bertani broth, while no biofilms were obtained at 5 \u00b0C, and in meat broth nutrient media. Applying the minimum bactericidal concentrations of cinnamon, clove, oregano, rosemary, thyme, and winter savory essential oils on preformed biofilms led to significant reductions being observed in the range from 45.34% to 78.89%. A scanning electron microscopy assay showed the devastating impact of oregano and thyme essential oils on the morphology of Y. enterocolitica bacterial cells. In conclusion, the results of this study show that essential oils possess high anti-Yersinia and antibiofilm effects.<\/jats:p>","DOI":"10.3390\/foods13050806","type":"journal-article","created":{"date-parts":[[2024,3,6]],"date-time":"2024-03-06T05:48:01Z","timestamp":1709704081000},"page":"806","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Using Essential Oils to Reduce Yersinia enterocolitica in Minced Meat and in Biofilms"],"prefix":"10.3390","volume":"13","author":[{"given":"Suzana","family":"Vidakovi\u0107 Kne\u017eevi\u0107","sequence":"first","affiliation":[{"name":"Scientific Veterinary Institute \u201cNovi Sad\u201d, 21000 Novi Sad, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6316-5863","authenticated-orcid":false,"given":"Slobodan","family":"Kne\u017eevi\u0107","sequence":"additional","affiliation":[{"name":"Scientific Veterinary Institute \u201cNovi Sad\u201d, 21000 Novi Sad, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1202-6964","authenticated-orcid":false,"given":"Jelena","family":"Vrane\u0161evi\u0107","sequence":"additional","affiliation":[{"name":"Scientific Veterinary Institute \u201cNovi Sad\u201d, 21000 Novi Sad, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dubravka","family":"Milanov","sequence":"additional","affiliation":[{"name":"Scientific Veterinary Institute \u201cNovi Sad\u201d, 21000 Novi Sad, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7754-7264","authenticated-orcid":false,"given":"Zoran","family":"Ru\u017ei\u0107","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, Faculty of Agriculture, University of Novi Sad, 21000 Novi Sad, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6097-3216","authenticated-orcid":false,"given":"Nedjeljko","family":"Karabasil","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, University of Belgrade, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sun\u010dica","family":"Koci\u0107-Tanackov","sequence":"additional","affiliation":[{"name":"Faculty of Technology Novi Sad, University of Novi Sad, 21000 Novi Sad, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,3,6]]},"reference":[{"key":"ref_1","unstructured":"(2023, December 25). LPSN\u2014List of Prokaryotic Names with Standing in Nomenclature. Available online: https:\/\/lpsn.dsmz.de\/."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"5575","DOI":"10.1099\/ijsem.0.001485","article-title":"Genome-based phylogeny and taxonomy of the \u2018Enterobacteriales\u2019: Proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov","volume":"66","author":"Adeolu","year":"2016","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_3","first-page":"e000301","article-title":"Genus-wide Yersinia core-genome multilocus sequence typing for species identification and strain characterization","volume":"5","author":"Savin","year":"2019","journal-title":"Microb. Genom."},{"key":"ref_4","unstructured":"Hocking, A.D. (2003). Yersinia Enterocolitica, Australian Institute of Food Science and Technology Incorporated (AIFST Inc.). [6th ed.]."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1007\/s10096-014-2276-7","article-title":"Detection of Yersinia enterocolitica in food: An overview","volume":"34","author":"Gupta","year":"2015","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Karlsson, P.A., Tano, E., Jernberg, C., Hickman, R.A., Guy, L., J\u00e4rhult, J.D., and Wang, H. (2021). Molecular characterization of multidrug-resistant Yersinia enterocolitica from foodborne outbreaks in Sweden. Front. Microbiol., 12.","DOI":"10.3389\/fmicb.2021.664665"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"735308","DOI":"10.4061\/2011\/735308","article-title":"Yersinia enterocolitica and Yersinia pseudotuberculosis detection in foods","volume":"2011","author":"Fukushima","year":"2011","journal-title":"J. Pathog."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1089\/fpd.2020.2924","article-title":"Yersinia enterocolitica outbreak associated with pasteurized milk","volume":"18","author":"Gruber","year":"2021","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Hulankova, R. (2022). Higher Resistance of Yersinia enterocolitica in Comparison to Yersinia pseudotuberculosis to Antibiotics and Cinnamon, Oregano and Thyme Essential Oils. Pathogens, 11.","DOI":"10.3390\/pathogens11121456"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Angelovska, M., Zaharieva, M.M., Dimitrova, L.L., Dimova, T., Gotova, I., Urshev, Z., Ilieva, Y., Kaleva, M.D., Kim, T.C., and Naydenska, S. (2023). Prevalence, Genetic Homogeneity, and Antibiotic Resistance of Pathogenic Yersinia enterocolitica Strains Isolated from Slaughtered Pigs in Bulgaria. Antibiotics, 12.","DOI":"10.3390\/antibiotics12040716"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2335","DOI":"10.1007\/s42770-021-00591-3","article-title":"Pathogenic potential and antibiotic resistance of Yersinia enterocolitica, a foodborne pathogen limited to swine tonsils in a pork production chain from Southern Brazil","volume":"52","author":"Pegoraro","year":"2021","journal-title":"Braz. J. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Rivas, L., Strydom, H., Paine, S., Wang, J., and Wright, J. (2021). Yersiniosis in New Zealand. Pathogens, 10.","DOI":"10.3390\/pathogens10020191"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"118","DOI":"10.59393\/amb23390204","article-title":"Yersinia enterocolitica\u2014Isolation, Pathogenicity, and Prevalence in Farms for Slaughtered Pigs","volume":"39","author":"Angelovska","year":"2023","journal-title":"Acta Microbiol. Bulg."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Zdolec, N., and Ki\u0161, M. (2021). Meat Safety from Farm to Slaughter\u2014Risk-Based Control of Yersinia enterocolitica and Toxoplasma gondii. Processes, 9.","DOI":"10.3390\/pr9050815"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"824","DOI":"10.3389\/fchem.2019.00824","article-title":"Bacterial biofilm eradication agents: A current review","volume":"7","author":"Verderosa","year":"2019","journal-title":"Front. Chem."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Gao, C., Tian, L., Lu, J., Zhang, S., Wu, D., Xiao, P., and Gong, G. (2023). Cinnamaldehyde reduces Yersinia enterocolitica activity and biofilm formation by altering membrane permeability and signalling. Food Biosci., 53.","DOI":"10.1016\/j.fbio.2023.102791"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"112307","DOI":"10.1016\/j.jenvman.2021.112307","article-title":"Environmental applications of microbial extracellular polymeric substance (EPS): A review","volume":"287","author":"Siddharth","year":"2021","journal-title":"J. Environ. Manag."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Abebe, G.M. (2020). The role of bacterial biofilm in antibiotic resistance and food contamination. Int. J. Microbiol., 2020.","DOI":"10.1155\/2020\/1705814"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"629","DOI":"10.3390\/applmicrobiol3030044","article-title":"Biofilm formation, and related impacts on healthcare, food processing and packaging, industrial manufacturing, marine industries, and sanitation\u2014A review","volume":"3","author":"Shineh","year":"2023","journal-title":"Appl. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Durofil, A., Maddela, N.R., Naranjo, R.A., and Radice, M. (2022). Evidence on antimicrobial activity of essential oils and herbal extracts against Yersinia enterocolitica\u2014A review. Food Biosci., 47.","DOI":"10.1016\/j.fbio.2022.101712"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Mutlu-Ingok, A., Devecioglu, D., Dikmetas, D.N., Karbancioglu-Guler, F., and Capanoglu, E. (2020). Antibacterial, antifungal, antimycotoxigenic, and antioxidant activities of essential oils: An updated review. Molecules, 25.","DOI":"10.3390\/molecules25204711"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2172","DOI":"10.1080\/10408398.2020.1851169","article-title":"Effectiveness and mechanisms of essential oils for biofilm control on food-contact surfaces: An updated review","volume":"62","author":"Rossi","year":"2022","journal-title":"Crit. Rev. Food Sci. Nutr."},{"key":"ref_23","first-page":"6748052","article-title":"Lamiaceae essential oils, phytochemical profile, antioxidant, and biological activities","volume":"2021","author":"Ferreira","year":"2021","journal-title":"Evid. Based Complement. Altern. Med."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.tifs.2020.04.025","article-title":"Chemistry, bioactivities, mode of action and industrial applications of essential oils","volume":"101","author":"Jugreet","year":"2020","journal-title":"Trends Food Sci. Technol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"127268","DOI":"10.1016\/j.foodchem.2020.127268","article-title":"Essential oils: A promising eco-friendly food preservative","volume":"330","author":"Falleh","year":"2020","journal-title":"Food Chem."},{"key":"ref_26","first-page":"4","article-title":"In vitro antibacterial activity of some essential oils against Salmonella Enteritidis and Salmonella Typhimurium isolated from meat","volume":"72","author":"Karabasil","year":"2021","journal-title":"J. Food Saf. Food Qual."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.rvsc.2022.08.007","article-title":"Risk factors and the overall characterization of Yersinia enterocolitica as an initial model of pathogen surveillance in the pig production system in Serbia","volume":"152","author":"Karabasil","year":"2022","journal-title":"Res. Vet. Sci."},{"key":"ref_28","first-page":"88","article-title":"Antibacterial activity essential oils against Escherichia coli, Salmonella enterica and Listeria monocytogenes","volume":"68","author":"Blagojev","year":"2017","journal-title":"J. Food Saf. Food Qual."},{"key":"ref_29","unstructured":"(2017). Microbiology of the Food Chain\u2014Horizontal Method for the Detection of Pathogenic Yersinia enterocolitica (Standard No. ISO 10273:2017)."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Vidakovi\u0107 Kne\u017eevi\u0107, S., Kne\u017eevi\u0107, S., Vrane\u0161evi\u0107, J., Kravi\u0107, S.\u017d., Laki\u0107evi\u0107, B., Koci\u0107-Tanackov, S., and Karabasil, N. (2023). Effects of Selected Essential Oils on Listeria monocytogenes in Biofilms and in a Model Food System. Foods, 12.","DOI":"10.3390\/foods12101930"},{"key":"ref_31","first-page":"891","article-title":"Quantification of biofilm in microtiter plates: Overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci","volume":"115","author":"Hola","year":"2007","journal-title":"APMIS J. Pathol. Microbiol. Immunol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1016\/j.foodres.2018.07.014","article-title":"Essential oils as natural additives to prevent oxidation reactions in meat and meat products: A review","volume":"113","author":"Pateiro","year":"2018","journal-title":"Food Res. Int."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2626","DOI":"10.4315\/0362-028X-70.11.2626","article-title":"Effects of essential oils of oregano and nutmeg on growth and survival of Yersinia enterocolitica and Listeria monocytogenes in barbecued chicken","volume":"70","author":"Firouzi","year":"2007","journal-title":"J. Food Prot."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e10812","DOI":"10.1016\/j.heliyon.2022.e10812","article-title":"Effect of Thymus vulgaris L. essential oil and thymol on the microbiological properties of meat and meat products: A review","volume":"8","author":"Posgay","year":"2022","journal-title":"Heliyon"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Yu, H.H., Chin, Y.-W., and Paik, H.-D. (2021). Application of Natural Preservatives for Meat and Meat Products against Food-Borne Pathogens and Spoilage Bacteria: A Review. Foods, 10.","DOI":"10.3390\/foods10102418"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1146\/annurev-food-032818-121727","article-title":"Improving the efficacy of essential oils as antimicrobials in foods: Mechanisms of action","volume":"10","author":"Rao","year":"2019","journal-title":"Annu. Rev. Food Sci. Technol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"113930","DOI":"10.1016\/j.lwt.2022.113930","article-title":"Stress tolerance and transcriptomic response analysis of Yersinia enterocolitica adapted to Origanum vulgare L. essential oil","volume":"168","author":"Li","year":"2022","journal-title":"LWT Food Sci. Technol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1007\/s40291-013-0080-1","article-title":"Detection of biofilm production of Yersinia enterocolitica strains isolated from infected children and comparative antimicrobial susceptibility of biofilm versus planktonic forms","volume":"18","author":"Ioannidis","year":"2014","journal-title":"Mol. Diagn. Ther."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1016\/j.lwt.2016.10.007","article-title":"Prevalence, biofilm formation and virulence markers of Salmonella sp. and Yersinia enterocolitica in food of animal origin in Poland","volume":"75","author":"Zadernowska","year":"2017","journal-title":"LWT"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1016\/j.foodcont.2016.08.033","article-title":"Biofilm formation of Yersinia enterocolitica and its persistence following treatment with different sanitation agents","volume":"73","author":"Wang","year":"2017","journal-title":"Food Control"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"136","DOI":"10.14202\/vetworld.2019.136-140","article-title":"Features of formation of biofilms","volume":"12","author":"Lenchenko","year":"2019","journal-title":"Vet. World"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1683","DOI":"10.4315\/0362-028X.JFP-19-018","article-title":"Function of pYV plasmid on biofilm formation of Yersinia enterocolitica ERL032123 in the presence of Ca2+","volume":"82","author":"Wang","year":"2019","journal-title":"J. Food Prot."},{"key":"ref_43","unstructured":"Wang, H. (2016). Factors Contributing to Biofilm Formation of Yersinia enterocolitica. [Ph.D. Thesis, Massey University]."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"448","DOI":"10.5658\/WOOD.2022.50.6.448","article-title":"Inhibition of biofilm formation in Yersinia enterocolitica by edible plant extracts including Polygoni Multiflori Radix","volume":"50","author":"Ham","year":"2022","journal-title":"J. Korean Wood Sci. Technol."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Chen, K., Peng, C., Chi, F., Yu, C., Yang, Q., and Li, Z. (2022). Antibacterial and antibiofilm activities of chlorogenic acid against Yersinia enterocolitica. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.885092"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1199","DOI":"10.1016\/j.foodcont.2010.02.003","article-title":"Antimicrobial herb and spice compounds in food","volume":"21","author":"Tajkarimi","year":"2010","journal-title":"Food Control"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"4863","DOI":"10.1021\/jf0636465","article-title":"Membrane toxicity of antimicrobial compounds from essential oils","volume":"55","author":"Betts","year":"2007","journal-title":"J. Agric. Food Chem."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1451","DOI":"10.3390\/ph6121451","article-title":"Effect of essential oils on pathogenic bacteria","volume":"6","author":"Nazzaro","year":"2013","journal-title":"Pharmaceuticals"}],"container-title":["Foods"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2304-8158\/13\/5\/806\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:09:47Z","timestamp":1760105387000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2304-8158\/13\/5\/806"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,3,6]]},"references-count":48,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2024,3]]}},"alternative-id":["foods13050806"],"URL":"https:\/\/doi.org\/10.3390\/foods13050806","relation":{},"ISSN":["2304-8158"],"issn-type":[{"value":"2304-8158","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,3,6]]}}}