{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T10:52:26Z","timestamp":1777459946528,"version":"3.51.4"},"reference-count":50,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2020,6,2]],"date-time":"2020-06-02T00:00:00Z","timestamp":1591056000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["UIDB\/04469\/2020"],"award-info":[{"award-number":["UIDB\/04469\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100014439","name":"Partnership for Research and Innovation in the Mediterranean Area","doi-asserted-by":"publisher","award":["PRIMA\/0001\/2018"],"award-info":[{"award-number":["PRIMA\/0001\/2018"]}],"id":[{"id":"10.13039\/100014439","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100008530","name":"European Regional Development Fund","doi-asserted-by":"publisher","award":["NORTE-01-0145-FEDER-000004"],"award-info":[{"award-number":["NORTE-01-0145-FEDER-000004"]}],"id":[{"id":"10.13039\/501100008530","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Foods"],"abstract":"<jats:p>The growing intention to replace chemical food preservatives with plant-based antimicrobials that pose lower risks to human health has produced numerous studies describing the bactericidal properties of biopreservatives such as essential oils (EOs) in a variety of products, including cheese. This study aimed to perform a meta-analysis of literature data that could summarize the inactivation of Escherichia coli in cheese achieved by added EOs; and compare its inhibitory effectiveness by application method, antimicrobial concentration, and specific antimicrobials. After a systematic review, 362 observations on log reduction data and study characteristics were extracted from 16 studies. The meta-regression model suggested that pathogenic E. coli is more resistant to EO action than the non-pathogenic type (p &lt; 0.0001), although in both cases the higher the EO dose, the greater the mean log reduction achieved (p &lt; 0.0001). It also showed that, among the factual application methods, EOs\u2019 incorporation in films render a steadier inactivation (p &lt; 0.0001) than when directly applied to milk or smeared on cheese surface. Lemon balm, sage, shallot, and anise EOs showed the best inhibitory outcomes against the pathogen. The model also revealed the inadequacy of inoculating antimicrobials in cheese purposely grated for performing challenge studies, as this non-realistic application overestimates (p &lt; 0.0001) the inhibitory effects of EOs.<\/jats:p>","DOI":"10.3390\/foods9060716","type":"journal-article","created":{"date-parts":[[2020,6,2]],"date-time":"2020-06-02T09:19:27Z","timestamp":1591089567000},"page":"716","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Effects of Essential Oils on Escherichia coli Inactivation in Cheese as Described by Meta-Regression Modelling"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7571-031X","authenticated-orcid":false,"given":"Beatriz","family":"Nunes Silva","sequence":"first","affiliation":[{"name":"Centro de Investiga\u00e7\u00e3o de Montanha (CIMO), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia, 5300-253 Bragan\u00e7a, Portugal"},{"name":"CEB \u2013 Centre of Biological Engineering, University of Minho, Campus Gualtar, 4710\u2013057 Braga, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3077-7414","authenticated-orcid":false,"given":"Vasco","family":"Cadavez","sequence":"additional","affiliation":[{"name":"Centro de Investiga\u00e7\u00e3o de Montanha (CIMO), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia, 5300-253 Bragan\u00e7a, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4918-3704","authenticated-orcid":false,"given":"Jos\u00e9 Ant\u00f3nio","family":"Teixeira","sequence":"additional","affiliation":[{"name":"CEB \u2013 Centre of Biological Engineering, University of Minho, Campus Gualtar, 4710\u2013057 Braga, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8462-9775","authenticated-orcid":false,"given":"Ursula","family":"Gonzales-Barron","sequence":"additional","affiliation":[{"name":"Centro de Investiga\u00e7\u00e3o de Montanha (CIMO), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia, 5300-253 Bragan\u00e7a, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2020,6,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1016\/j.foodcont.2009.11.015","article-title":"Prevalence and sources of cheese contamination with pathogens at farm and processing levels","volume":"21","author":"Kousta","year":"2010","journal-title":"Food Control"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"307","DOI":"10.5713\/ajas.15.0332","article-title":"Cheese microbial risk assessments - A Review","volume":"29","author":"Choi","year":"2016","journal-title":"Asian Australas. J. Anim. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"European Food Safety Authority (EFSA), and European Centre for Disease Prevention (ECDC) (2018). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J., 16, 233\u2013239.","DOI":"10.2903\/j.efsa.2018.5500"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"European Food Safety Authority (EFSA), and European Centre for Disease Prevention (ECDC) (2019). The European Union One Health 2018 Zoonoses Report. EFSA J., 17, 201\u2013204.","DOI":"10.2903\/j.efsa.2019.5926"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.cofs.2017.10.002","article-title":"Foodborne pathogens in raw milk and cheese of sheep and goat origin: A meta-analysis approach","volume":"18","author":"Rodrigues","year":"2017","journal-title":"Curr. Opin. Food Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1007\/s11947-011-0653-0","article-title":"Counteracting recontamination of pasteurized milk by methylated soybean protein","volume":"6","author":"Mahgoub","year":"2013","journal-title":"Food Bioprocess Technol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1475","DOI":"10.4315\/0362-028X.JFP-11-065","article-title":"Inhibition of growth of pathogenic bacteria in raw milk by legume protein esters","volume":"74","author":"Mahgoub","year":"2011","journal-title":"J. Food Prot."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/j.ijfoodmicro.2010.10.004","article-title":"Occurrence of foodborne pathogens and characterization of Staphylococcus aureus in cheese produced on farm-dairies","volume":"144","author":"Rosengren","year":"2010","journal-title":"Int. J. Food Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1016\/S0956-7135(03)00121-X","article-title":"Incidence of Escherichia coli O157 in raw milk and white pickled cheese manufactured from raw milk in Turkey","volume":"15","author":"Arici","year":"2004","journal-title":"Food Control"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2561","DOI":"10.3168\/jds.2008-1055","article-title":"Prevalence and characteristics of Shiga toxin-producing Escherichia coli in Swiss raw milk cheeses collected at producer level","volume":"91","author":"Stephan","year":"2008","journal-title":"J. Dairy Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.ijfoodmicro.2016.01.009","article-title":"Prevalence and pathogenic potential of Escherichia coli isolates from raw milk and raw milk cheese in Egypt","volume":"221","author":"Ombarak","year":"2016","journal-title":"Int. J. Food Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"325","DOI":"10.4315\/0362-028X.JFP-17-283","article-title":"Outbreak of Escherichia coli O157:H7 infections linked to aged raw milk Gouda cheese, Canada, 2013","volume":"81","author":"Currie","year":"2018","journal-title":"J. Food Prot."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1759","DOI":"10.4315\/0362-028X.JFP-12-136","article-title":"Multistate outbreak of Escherichia coli O157:H7 infections associated with in-store sampling of an aged raw-milk Gouda cheese, 2010","volume":"75","author":"McCollum","year":"2012","journal-title":"J. Food Prot."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1900305","DOI":"10.2807\/1560-7917.ES.2019.24.22.1900305","article-title":"Outbreak of Shiga toxin-producing Escherichia coli (STEC) O26 paediatric haemolytic uraemic syndrome (HUS) cases associated with the consumption of soft raw cow\u2019s milk cheeses, France, March to May 2019","volume":"24","author":"Jones","year":"2019","journal-title":"Euro Surveill."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1007\/BF03403686","article-title":"An outbreak of E. coli O15:H7 hemorrhagic colitis associated with unpasteurized Gouda cheese","volume":"96","author":"Honish","year":"2005","journal-title":"Can. J. Public Heal."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1017\/S0950268805004887","article-title":"Escherichia coli O157 outbreak associated with fresh unpasteurized goats\u2019 cheese","volume":"134","author":"Vaillant","year":"2006","journal-title":"Epidemiol. Infect."},{"key":"ref_17","first-page":"1372","article-title":"Pathogenesis, Virulence, and Infective Dose","volume":"3","author":"Frank","year":"2007","journal-title":"PLoS Pathog."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1111\/jfs.12277","article-title":"Properties of Bunium Persicum essential oil and its application in Iranian white cheese against Listeria monocytogenes and Escherichia coli O157:H7","volume":"36","author":"Ehsani","year":"2016","journal-title":"J. Food Saf."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1080\/0972060X.2012.10662606","article-title":"Phytochemical properties and hygienic effects of Allium ascalonicum and Pimpinella anisum essential oils in Iranian white brined cheese","volume":"15","author":"Ehsani","year":"2012","journal-title":"J. Essent. Oil Bear. Plants"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"50","DOI":"10.2174\/1874070700903010050","article-title":"Use of antimicrobial and genotoxicity potentiality for evaluation of essential oils as food preservatives","volume":"3","author":"Hamedo","year":"2009","journal-title":"Open Biotechnol. J."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1111\/jfs.12078","article-title":"Cold pressed Nigella sativa oil inhibits the growth of foodborne pathogens and improves the quality of Domiati cheese","volume":"33","author":"Mahgoub","year":"2013","journal-title":"J. Food Saf."},{"key":"ref_22","first-page":"1","article-title":"Evaluation rosemary essential oil in the control of multidrug-resistant Escherichia coli in Coalho cheese","volume":"4","author":"Ribeiro","year":"2013","journal-title":"J. Biotec. Biodivers."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1016\/j.foodres.2013.11.024","article-title":"Meta-analysis of the incidence of foodborne pathogens in Portuguese meats and their products","volume":"55","author":"Xavier","year":"2014","journal-title":"Food Res. Int."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e12476","DOI":"10.1111\/jfs.12476","article-title":"Antimicrobial effects of Zataria multiflora essential oil and Lactobacillus acidophilus on Escherichia coli O157 stability in the Iranian probiotic white-brined cheese","volume":"38","author":"Mehdizadeh","year":"2018","journal-title":"J. Food Saf."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1016\/j.sjbs.2013.10.005","article-title":"Soft cheese supplemented with black cumin oil: Impact on food borne pathogens and quality during storage","volume":"21","author":"Hassanien","year":"2014","journal-title":"Saudi J. Biol. Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1590\/S1517-83822010005000005","article-title":"Antimicrobial activity of essential oils against Vancomycin-Resistant Enterococci (VRE) and Escherichia coli O157:H7 in feta soft cheese and minced beef meat","volume":"42","author":"Selim","year":"2011","journal-title":"Braz. J. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.foodchem.2018.10.093","article-title":"Eugenol and carvacrol migration from PHBV films and antibacterial action in different food matrices","volume":"277","author":"Requena","year":"2019","journal-title":"Food Chemistry"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1016\/j.foodcont.2014.02.022","article-title":"Evaluation of two antimicrobial packaging films against Escherichia coli O157: H7 strains in vitro and during storage of a Spanish ripened sheep cheese (Zamorano)","volume":"42","author":"Otero","year":"2014","journal-title":"Food Control"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"99","DOI":"10.15567\/mljekarstvo.2016.0202","article-title":"Use of egg white protein powder based films fortified with sage and lemon balm essential oils in the storage of lor cheese","volume":"66","author":"Kavas","year":"2016","journal-title":"Mljekarstvo"},{"key":"ref_30","first-page":"30","article-title":"Essential oil of tarragon (Artemisia dracunculus) antibacterial activity on Staphylococcus aureus and Escherichia coli in culture media and Iranian white cheese","volume":"4","author":"Raeisi","year":"2012","journal-title":"Iran. J. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1177\/8756087911407391","article-title":"Antimicrobial effectiveness of chitosan-essential oil coated plastic films against foodborne pathogens","volume":"27","author":"Torlak","year":"2011","journal-title":"J. Plast. Film Sheeting"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1240","DOI":"10.1016\/j.lwt.2010.09.022","article-title":"Antibacterial activity of oregano and thyme essential oils against Listeria monocytogenes and Escherichia coli O157:H7 in feta cheese packaged under modified atmosphere","volume":"44","author":"Govaris","year":"2011","journal-title":"LWT-Food Sci. Technol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2014","DOI":"10.5897\/AJB2014.13992","article-title":"Application of zein antimicrobial edible film incorporating Zataria multiflora boiss essential oil for preservation of Iranian ultrafiltered Feta cheese","volume":"14","author":"Ghasemi","year":"2015","journal-title":"Afr. J. Biotechnol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1028","DOI":"10.31925\/farmacia.2018.6.16","article-title":"Evaluation of antimicrobial potential of Nigella sativa oil in a model food matrix","volume":"66","author":"Georgescu","year":"2018","journal-title":"Farmacia"},{"key":"ref_35","unstructured":"R Core Team (2019, March 21). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available online: https:\/\/www.R-project.org\/."},{"key":"ref_36","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"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"6531","DOI":"10.1128\/AEM.01702-16","article-title":"Cinnamon oil inhibits Shiga toxin type 2 phage induction and Shiga toxin type 2 production in Escherichia coli O157:H7","volume":"82","author":"Sheng","year":"2016","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Kim, Y.-G., Lee, J.-H., Gwon, G., Kim, S.-I., Park, J.G., and Lee, J. (2016). Essential oils and eugenols inhibit biofilm formation and the virulence of Escherichia coli O157:H7. Sci. Rep.","DOI":"10.1038\/srep36377"},{"key":"ref_39","unstructured":"International Organization for Standardization (ISO) (2020, April 20). ISO 20976-1:2019 - Microbiology of the Food Chain\u2014Requirements and Guidelines for Conducting Challenge Tests of Food and Feed Products\u2014Part 1: Challenge Tests to Study Growth Potential, Lag Time and Maximum Growth Rate. Available online: https:\/\/www.iso.org\/standard\/69673.html."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.foodhyd.2018.06.003","article-title":"Retention and release properties of cinnamon essential oil in antimicrobial films based on chitosan and gum arabic","volume":"84","author":"Xu","year":"2018","journal-title":"Food Hydrocoll."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"76","DOI":"10.3389\/fmicb.2015.00076","article-title":"Bioactivity of essential oils: A review on their interaction with food components","volume":"6","author":"Perricone","year":"2015","journal-title":"Front. Microbiol."},{"key":"ref_42","unstructured":"Nunes Silva, B., Cadavez, V., Teixeira, J.A., and Gonzales-Barron, U. Meta-regression models describing the effects of essential oils and added lactic acid bacteria on pathogen inactivation in cheese. Microb. Risk Anal., under review."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Soto-Hernandez, M., Palma-Tenango, M., and Garcia-Mateos, M. (2017). Application of Phenolic Compounds for Food Preservation: Food Additive and Active Packaging. Phenolic Compounds - Biological Activity, InTechOpen.","DOI":"10.5772\/63693"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"829","DOI":"10.3389\/fmicb.2019.00829","article-title":"Antibacterial properties of polyphenols: Characterization and QSAR (Quantitative structure-activity relationship) models","volume":"10","author":"Forquet","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_45","unstructured":"(2020, April 20). World Flora Online. Available online: http:\/\/www.worldfloraonline.org\/."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1459","DOI":"10.1002\/ptr.6098","article-title":"Antimicrobial activity of extracts and phthalides occurring in Apiaceae plants","volume":"32","author":"Pannek","year":"2018","journal-title":"Phytother. Res."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Tzima, K., Brunton, N.P., and Rai, D.K. (2018). Qualitative and quantitative analysis of polyphenols in Lamiaceae plants\u2014A review. Plants, 7.","DOI":"10.3390\/plants7020025"},{"key":"ref_48","first-page":"119","article-title":"In Vitro antioxidant and antibacterial activity of Lamiaceae phenolic extracts: A correlation study","volume":"52","author":"Skroza","year":"2014","journal-title":"Food Technol. Biotechnol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.fct.2018.05.050","article-title":"Phytochemicals of herbs and spices: Health versus toxicological effects","volume":"119","author":"Guldiken","year":"2018","journal-title":"Food Chem. Toxicol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"4943","DOI":"10.1016\/j.bmcl.2017.09.052","article-title":"Antibacterial constituents of the plant family Amaryllidaceae","volume":"27","author":"Nair","year":"2017","journal-title":"Bioorg. Med. Chem. Lett."}],"container-title":["Foods"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2304-8158\/9\/6\/716\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:34:53Z","timestamp":1760175293000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2304-8158\/9\/6\/716"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,6,2]]},"references-count":50,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2020,6]]}},"alternative-id":["foods9060716"],"URL":"https:\/\/doi.org\/10.3390\/foods9060716","relation":{},"ISSN":["2304-8158"],"issn-type":[{"value":"2304-8158","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,6,2]]}}}