{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T05:42:04Z","timestamp":1788846124297,"version":"build-2803163510"},"reference-count":48,"publisher":"MDPI AG","issue":"18","license":[{"start":{"date-parts":[[2021,9,15]],"date-time":"2021-09-15T00:00:00Z","timestamp":1631664000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100011697","name":"R\u00e9gion Bretagne","doi-asserted-by":"publisher","award":["18004512"],"award-info":[{"award-number":["18004512"]}],"id":[{"id":"10.13039\/501100011697","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Molecules"],"abstract":"<jats:p>The regulation of intestinal colonization in livestock by means of non-bactericidal additives is an important management lever for zoonotic bacteria such as Salmonella spp. Caenorhabditis elegans is proposed here as a model for the evaluation of five essential oils (EOs) as anti-colonization products against Salmonella Typhimurium. An evaluation of the toxicity of EOs for C. elegans showed LD50 values ranging from 74.5 \u00b1 9.6 \u00b5g\/mL for Cinnamomum cassia (CEO) to 271.6 \u00b1 14.9 \u00b5g\/mL for Syzygium aromaticum (SyEO). Both EOs significantly inhibited bacterial colonization in the digestive tract of C. elegans with reductions of 0.88 and 0.70 log CFU\/nematode at nontoxic concentrations of 50 \u00b5g\/mL and 150 \u00b5g\/mL, respectively. With the minimal bactericidal concentrations of CEO and SyEO against S. Typhimurium being 312.5 \u00b5g\/mL and 625 \u00b5g\/mL, respectively, an antibacterial effect can be excluded to explain the inhibition of the bacterial load. The anti-colonizing activity of these two EOs could, however, be related to an inhibition of the swimming motility, which was significantly reduced by 23.47% for CEO at 50 \u00b5g\/mL and 19.56% for SyEO at 150 \u00b5g\/mL. This study shows the potential of C. elegans as a predictive in vivo model of anti-colonizing activities that is suitable for the evaluation of essential oils.<\/jats:p>","DOI":"10.3390\/molecules26185598","type":"journal-article","created":{"date-parts":[[2021,9,15]],"date-time":"2021-09-15T12:00:44Z","timestamp":1631707244000},"page":"5598","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Cinnamomum cassia and Syzygium aromaticum Essential Oils Reduce the Colonization of Salmonella Typhimurium in an In Vivo Infection Model Using Caenorhabditis elegans"],"prefix":"10.3390","volume":"26","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4324-9167","authenticated-orcid":false,"given":"Marie","family":"Lang","sequence":"first","affiliation":[{"name":"BioArmor S.A., Z.I de la Gare, F-22940 Plaintel, France"},{"name":"Laboratoire de Biotechnologie et Chimie Marines EA 3884, Universit\u00e9 Bretagne Sud, F-56100 Lorient, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aude","family":"Montjarret","sequence":"additional","affiliation":[{"name":"BioArmor S.A., Z.I de la Gare, F-22940 Plaintel, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emmanuel","family":"Duteil","sequence":"additional","affiliation":[{"name":"BioArmor S.A., Z.I de la Gare, F-22940 Plaintel, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4108-1073","authenticated-orcid":false,"given":"Gilles","family":"Bedoux","sequence":"additional","affiliation":[{"name":"Laboratoire de Biotechnologie et Chimie Marines EA 3884, Universit\u00e9 Bretagne Sud, F-56100 Lorient, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,9,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1016\/j.foodres.2011.04.052","article-title":"Control of Salmonella in foods by using essential oils: A review","volume":"45","author":"Bajpai","year":"2012","journal-title":"Food Res. Int."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1016\/j.foodres.2017.11.024","article-title":"Biofilm formation by Salmonella sp. in the poultry industry: Detection, control and eradication strategies","volume":"119","author":"Merino","year":"2019","journal-title":"Food Res. Int."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"119","DOI":"10.2323\/jgam.60.119","article-title":"Effect of cinnamon essential oil and cinnamaldehyde on Salmonella Saintpaul biofilm on a stainless steel surface","volume":"60","author":"Piovezan","year":"2014","journal-title":"J. Gen. Appl. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"353","DOI":"10.3382\/japr.2014-00944","article-title":"Integrated farm management to prevent Salmonella Enteritidis contamination of eggs","volume":"23","author":"Trampel","year":"2014","journal-title":"J. Appl. Poult. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1080\/10412905.2010.9700269","article-title":"Chemical composition, and antioxidant and antimicrobial activities of essential oil of spearmint (Mentha spicata L.) from pakistan","volume":"22","author":"Hussain","year":"2010","journal-title":"J. Essent. Oil Res."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"9252","DOI":"10.3390\/molecules15129252","article-title":"Antioxidant and anti-inflammatory activities of essential oils: A short review","volume":"15","author":"Miguel","year":"2010","journal-title":"Molecules"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1227","DOI":"10.3390\/molecules18011227","article-title":"A review on anti-inflammatory activity of monoterpenes","volume":"18","author":"Andrade","year":"2013","journal-title":"Molecules"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Astani, A., Reichling, J., and Schnitzler, P. (2011). Screening for antiviral activities of isolated compounds from essential oils. Evidence-based Complement. Altern. Med., 2011.","DOI":"10.1093\/ecam\/nep187"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1616","DOI":"10.1590\/S1517-83822011000400049","article-title":"Antiviral activity of the Lippia graveolens (Mexican oregano) essential oil and its main compound carvacrol against human and animal viruses","volume":"42","author":"Pilau","year":"2011","journal-title":"Braz. J. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1186\/s40104-015-0055-7","article-title":"In vitro antibacterial activity of thymol and carvacrol and their effects on broiler chickens challenged with Clostridium perfringens","volume":"6","author":"Du","year":"2015","journal-title":"J. Anim. Sci. Biotechnol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1016\/j.indcrop.2013.07.052","article-title":"Chemical composition and in vitro antibacterial properties of essential oils of four Thymus species from organic growth","volume":"50","author":"Sendra","year":"2013","journal-title":"Ind. Crop. Prod."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1111\/j.1745-4565.2007.00064.x","article-title":"The antibacterial effect of cinnamaldehyde, thymol, carvacrol and their combinations against the foodborne pathogen Salmonella typhimurium","volume":"27","author":"Zhou","year":"2007","journal-title":"J. Food Saf."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"205","DOI":"10.4315\/0362-028X.JFP-12-196","article-title":"Inhibition and inactivation of Salmonella typhimurium biofilms from polystyrene and stainless steel surfaces by essential oils and phenolic constituent carvacrol","volume":"76","author":"Soni","year":"2013","journal-title":"J. Food Prot."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"6404","DOI":"10.1128\/AEM.00704-07","article-title":"Influence of lactic acid bacteria on longevity of Caenorhabditis elegans and host defense against Salmonella enterica serovar Enteritidis","volume":"73","author":"Ikeda","year":"2007","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"10414","DOI":"10.1073\/pnas.0604055103","article-title":"Identification of novel antimicrobials using a live-animal infection model","volume":"103","author":"Moy","year":"2006","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.tim.2005.01.003","article-title":"The worm has turned-Microbial virulence modeled in Caenorhabditis elegans","volume":"13","author":"Sifri","year":"2005","journal-title":"Trends Microbiol."},{"key":"ref_17","first-page":"403","article-title":"Models of Caenorhabditis elegans infection by bacterial and fungal pathogens","volume":"415","author":"Powell","year":"2008","journal-title":"Methods Mol. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1528","DOI":"10.1099\/jmm.0.000385","article-title":"Inhibition of quorum-sensing-controlled virulence factors of Pseudomonas aeruginosa by Murraya koenigii essential oil: A study in a Caenorhabditis elegans infectious model","volume":"65","author":"Ganesh","year":"2016","journal-title":"J. Med. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"485","DOI":"10.4161\/viru.21808","article-title":"Burkholderia pseudomallei kills Caenorhabditis elegans through virulence mechanisms distinct from intestinal lumen colonization","volume":"3","author":"Ooi","year":"2012","journal-title":"Virulence"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1956","DOI":"10.3389\/fmicb.2016.01956","article-title":"Beyond Traditional Antimicrobials: A Caenorhabditis elegans Model for Discovery of Novel Anti-infectives","volume":"7","author":"Kong","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.coi.2018.06.003","article-title":"Caenorhabditis elegans in high-throughput screens for anti-infective compounds","volume":"54","author":"Peterson","year":"2018","journal-title":"Curr. Opin. Immunol."},{"key":"ref_22","first-page":"1","article-title":"A High-throughput, High-content, Liquid-based C. elegans Pathosystem","volume":"2018","author":"Anderson","year":"2018","journal-title":"J. Vis. Exp."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/S1369-5274(99)00047-8","article-title":"Caenorhabditis elegans: A model genetic host to study Pseudomonas aeruginosa pathogenesis","volume":"3","author":"Tan","year":"2000","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1543","DOI":"10.1016\/S0960-9822(00)00833-2","article-title":"Caenorhabditis elegans is a model host for Salmonella typhimurium","volume":"10","author":"Labrousse","year":"2000","journal-title":"Curr. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0045417","article-title":"Pathogenicity of Salmonella enterica in Caenorhabditis elegans Relies on Disseminated Oxidative Stress in the Infected Host","volume":"7","author":"Sem","year":"2012","journal-title":"PLoS ONE"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"12462","DOI":"10.1073\/pnas.1822018116","article-title":"Salmonella biofilms program innate immunity for persistence in Caenorhabditis elegans","volume":"116","author":"Desai","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"421","DOI":"10.3389\/fmicb.2016.00421","article-title":"Red Seaweeds Sarcodiotheca gaudichaudii and Chondrus crispus down Regulate Virulence Factors of Salmonella Enteritidis and Induce Immune Responses in Caenorhabditis elegans","volume":"7","author":"Kulshreshtha","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"e12739","DOI":"10.1111\/cmi.12739","article-title":"Flagellin phase-dependent swimming on epithelial cell surfaces contributes to productive Salmonella gut colonisation","volume":"19","author":"Horstmann","year":"2017","journal-title":"Cell. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1142\/S0192415X06004041","article-title":"Antimicrobial Activities of Cinnamon Oil and Cinnamaldehyde from the Chinese Medicinal Herb Cinnamomum cassia Blume","volume":"34","author":"Ooi","year":"2006","journal-title":"Am. J. Chin. Med."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.fitote.2014.04.003","article-title":"Antibacterial activity of essential oils, their blends and mixtures of their main constituents against some strains supporting livestock mastitis","volume":"96","author":"Fratini","year":"2014","journal-title":"Fitoterapia"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1134\/S000368381301002X","article-title":"Antiradical properties of oregano, thyme, and savory essential oils","volume":"49","author":"Alinkina","year":"2012","journal-title":"Appl. Biochem. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1080\/10412905.2013.860409","article-title":"Antimicrobial activity of essential oils","volume":"26","year":"2014","journal-title":"J. Essent. Oil Res."},{"key":"ref_33","first-page":"1","article-title":"Bioactivities and compositions of Betula nigra essential oils","volume":"2","author":"Woods","year":"2013","journal-title":"J. Med. Act. Plants"},{"key":"ref_34","first-page":"1777","article-title":"Bioactivities and compositional analyses of Cinnamomum essential oils from Nepal: C. camphora, C. tamala, and C. glaucescens","volume":"8","author":"Satyal","year":"2013","journal-title":"Nat. Prod. Commun."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Dosoky, N., Satyal, P., Gautam, T., and Setzer, W. (2016). Composition and Biological Activities of Murraya paniculata (L.) Jack Essential Oil from Nepal. Medicines, 3.","DOI":"10.3390\/medicines3010007"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"835","DOI":"10.1007\/s12038-013-9385-9","article-title":"Influence of clove oil on certain quorum-sensing-regulated functions and biofilm of Pseudomonas aeruginosa and Aeromonas hydrophila","volume":"38","author":"Husain","year":"2013","journal-title":"J. Biosci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fmicb.2015.00420","article-title":"Sub-MICs of Mentha piperita essential oil and menthol inhibits AHL mediated quorum sensing and biofilm of Gram-negative bacteria","volume":"6","author":"Husain","year":"2015","journal-title":"Front. Microbiol."},{"key":"ref_38","first-page":"1143","article-title":"The mode of antibacterial action of essential oils","volume":"3","year":"2011","journal-title":"Science against Microbial Pathogens: Communicating Current Research and Technological Advances"},{"key":"ref_39","first-page":"1","article-title":"Variations in motility and biofilm formation of Salmonella enterica serovar Typhi","volume":"6","author":"Chai","year":"2014","journal-title":"Gut Pathog."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"12","DOI":"10.3389\/fmicb.2012.00012","article-title":"Essential Oils in Food Preservation: Mode of Action, Synergies, and Interactions with Food Matrix Components","volume":"3","author":"Hyldgaard","year":"2012","journal-title":"Front. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1111\/j.1365-2672.2005.02789.x","article-title":"Antimicrobial activity of essential oils and structurally related synthetic food additives towards selected pathogenic and beneficial gut bacteria","volume":"100","author":"Si","year":"2006","journal-title":"J. Appl. Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1016\/j.foodcont.2005.11.009","article-title":"Inhibitory effects of selected plant essential oils on the growth of four pathogenic bacteria: E. coli O157:H7, Salmonella Typhimurium, Staphylococcus aureus and Listeria monocytogenes","volume":"18","author":"Oussalah","year":"2007","journal-title":"Food Control"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"6951","DOI":"10.1128\/AEM.70.12.6951-6956.2004","article-title":"Colorimetric Method for Identifying Plant Essential Oil Components That Affect Biofilm Formation and Structure","volume":"70","author":"Niu","year":"2004","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2981","DOI":"10.1128\/AEM.07643-11","article-title":"Reduction of Salmonella enterica serovar enteritidis colonization in 20-day-old broiler chickens by the plant-derived compounds trans-cinnamaldehyde and eugenol","volume":"78","author":"Mattson","year":"2012","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_45","first-page":"e4019","article-title":"Basic Caenorhabditis elegans methods: Synchronization and observation","volume":"64","author":"Fontrodona","year":"2012","journal-title":"J. Vis. Exp."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1002\/9780470559277.ch130160","article-title":"High-Throughput Screening for Novel Anti-Infectives Using a C. elegans Pathogenesis Model","volume":"6","author":"Conery","year":"2014","journal-title":"Curr. Protoc. Chem. Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1063\/1.4895251","article-title":"Identification of potential anti-infectives against staphylococcus aureus using a Caenorhabditis elegans infection model","volume":"1614","author":"Konga","year":"2014","journal-title":"AIP Conf. Proc."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/j.jbiotec.2019.07.010","article-title":"Evaluation of immunomodulatory activities of essential oils by high content analysis","volume":"303","author":"Lang","year":"2019","journal-title":"J. Biotechnol."}],"container-title":["Molecules"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1420-3049\/26\/18\/5598\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:00:11Z","timestamp":1760166011000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1420-3049\/26\/18\/5598"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,9,15]]},"references-count":48,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2021,9]]}},"alternative-id":["molecules26185598"],"URL":"https:\/\/doi.org\/10.3390\/molecules26185598","relation":{},"ISSN":["1420-3049"],"issn-type":[{"value":"1420-3049","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,15]]}}}