{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T18:39:39Z","timestamp":1788374379965,"version":"build-2803163510"},"reference-count":48,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2019,3,7]],"date-time":"2019-03-07T00:00:00Z","timestamp":1551916800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Listeria monocytogenes can persist in food production facilities, resulting in serious threats to consumers due to the high mortality associated with listeriosis, especially in the very young, old and pregnant. We subtyped 124 strains of L. monocytogenes isolated from a meat processing facility in Switzerland by serotyping, multi locus sequence typing (MLST) typing and whole genome sequencing. We then analyzed their ability to form biofilms and their resistance to the disinfectants benzalkonium chloride (BC) and peracetic acid (PAA). The genotyping results of the strains showed that several clonal populations of L. monocytogenes belonging to CC9, CC204 and CC121 had persisted in this meat processing facility for at least four years. All of the strains showed biofilm forming capacity comparable to a known high biofilm forming strain. Known efflux pumps for BC were present in CC204, CC9 (brcABC) and CC121 (qacH) strains, while strains from other CC showed very low minimal inhibitory concentrations (MICs) for BC. For PAA, minimal bactericidal concentrations of 1.2\u20131.6% for 20 min and minimal inhibitory concentrations between 0.1 and 0.2% were observed. These values were close to or above the recommended concentration for use (0.5\u20131%), suggesting that PAA might be ineffective at controlling L. monocytogenes in this and potentially other meat processing facilities.<\/jats:p>","DOI":"10.3390\/pathogens8010032","type":"journal-article","created":{"date-parts":[[2019,3,8]],"date-time":"2019-03-08T04:58:35Z","timestamp":1552021115000},"page":"32","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":76,"title":["Characteristics of Listeria Monocytogenes Strains Persisting in a Meat Processing Facility over a 4-Year Period"],"prefix":"10.3390","volume":"8","author":[{"given":"Andrea","family":"Stoller","sequence":"first","affiliation":[{"name":"Institute for Food Safety and Hygiene, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marc","family":"Stevens","sequence":"additional","affiliation":[{"name":"Institute for Food Safety and Hygiene, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1002-4762","authenticated-orcid":false,"given":"Roger","family":"Stephan","sequence":"additional","affiliation":[{"name":"Institute for Food Safety and Hygiene, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claudia","family":"Guldimann","sequence":"additional","affiliation":[{"name":"Institute for Food Safety and Hygiene, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,3,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1093\/infdis\/jir263","article-title":"Deaths associated with bacterial pathogens transmitted commonly through food: Foodborne diseases active surveillance network (FoodNet), 1996\u20132005","volume":"204","author":"Jones","year":"2011","journal-title":"J. Infect. Dis."},{"key":"ref_2","first-page":"251","article-title":"Surveillance of Listeria infections in Europe","volume":"10","author":"Jacquet","year":"2005","journal-title":"Euro Surveill."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1089\/fpd.2013.1697","article-title":"Listeria: An Australian perspective (2001\u20132010)","volume":"11","author":"Popovic","year":"2014","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1017\/S0950268812001550","article-title":"Years of potential life lost for six major enteric pathogens, Germany, 2004\u20132008","volume":"141","author":"Werber","year":"2012","journal-title":"Epidemiol. Infect."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2795","DOI":"10.1017\/S0950268814003185","article-title":"An assessment of the human health impact of seven leading foodborne pathogens in the United States using disability adjusted life years","volume":"143","author":"Scallan","year":"2015","journal-title":"Epidemiol. Infect."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"962","DOI":"10.1086\/428575","article-title":"Multistate outbreak of Listeria monocytogenes infection linked to delicatessen turkey meat","volume":"40","author":"Olsen","year":"2005","journal-title":"Clin. Infect. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Orsi, R.H., Borowsky, M.L., Lauer, P., Young, S.K., Nusbaum, C., Galagan, J.E., Birren, B.W., Ivy, R.A., Sun, Q., and Graves, L.M. (2008). Short-term genome evolution of Listeria monocytogenes in a non-controlled environment. BMC Genom., 9.","DOI":"10.1186\/1471-2164-9-539"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.fm.2013.02.012","article-title":"Persistent Listeria monocytogenes subtypes isolated from a smoked fish processing facility included both phage susceptible and resistant isolates","volume":"35","author":"Vongkamjan","year":"2013","journal-title":"Food Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"436","DOI":"10.3389\/fmicb.2014.00436","article-title":"Monitoring occurrence and persistence of Listeria monocytogenes in foods and food processing environments in the Republic of Ireland","volume":"5","author":"Leong","year":"2014","journal-title":"Front. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2869","DOI":"10.1128\/JCM.01193-15","article-title":"Defining and Evaluating a Core Genome Multilocus Sequence Typing Scheme for Whole-Genome Sequence-Based Typing of Listeria monocytogenes","volume":"53","author":"Ruppitsch","year":"2015","journal-title":"J. Clin. Microbol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"7336","DOI":"10.1128\/AEM.69.12.7336-7342.2003","article-title":"Variation in Biofilm Formation among Strains of Listeria monocytogenes","volume":"69","author":"Borucki","year":"2003","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Agresti, A. (2002). Categorical Data Analysis, John Wiley & Sons, Inc.","DOI":"10.1002\/0471249688"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"8231","DOI":"10.1128\/AEM.02056-10","article-title":"Genetic characterization of plasmid-associated benzalkonium chloride resistance determinants in a Listeria monocytogenes strain from the 1998-1999 outbreak","volume":"76","author":"Elhanafi","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Muller, A., Rychli, K., Muhterem-Uyar, M., Zaiser, A., Stessl, B., Guinane, C.M., Cotter, P.D., Wagner, M., and Schmitz-Esser, S. (2013). Tn6188\u2014A novel transposon in Listeria monocytogenes responsible for tolerance to benzalkonium chloride. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0076835"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1128\/AEM.03741-15","article-title":"Tolerance of Listeria monocytogenes to Quaternary Ammonium Sanitizers Is Mediated by a Novel Efflux Pump Encoded by emrE","volume":"82","author":"Kovacevic","year":"2015","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1038\/ng.3501","article-title":"Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity","volume":"48","author":"Maury","year":"2016","journal-title":"Nat. Genet."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.fm.2014.05.014","article-title":"Diversity and distribution of Listeria monocytogenes in meat processing plants","volume":"44","author":"Perich","year":"2014","journal-title":"Food Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Ebner, R., Stephan, R., Althaus, D., Brisse, S., Maury, M., and Tasara, T. (2015). Phenotypic and genotypic characteristics of Listeria monocytogenes strains isolated during 2011\u20132014 from different food matrices in Switzerland. Food Control, 321\u2013326.","DOI":"10.1016\/j.foodcont.2015.04.030"},{"key":"ref_19","first-page":"539","article-title":"Closing gaps for performing a risk assessment on Listeria monocytogenes in ready-to-eat (RTE) foods: Activity 3, the comparison of isolates from different compartments along the food chain, and from humans using whole genome sequencing (WGS) analysis","volume":"14","author":"Nielsen","year":"2017","journal-title":"EFSA Support. Publ."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1089\/fpd.2014.1747","article-title":"Characterization of Listeria monocytogenes Strains Isolated During 2011\u20132013 from Human Infections in Switzerland","volume":"11","author":"Althaus","year":"2014","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"380","DOI":"10.1016\/j.fm.2006.06.006","article-title":"Assessing biofilm formation by Listeria monocytogenes strains","volume":"24","author":"Harvey","year":"2007","journal-title":"Food Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.ijfoodmicro.2018.03.026","article-title":"Listeria monocytogenes strains show large variations in competitive growth in mixed culture biofilms and suspensions with bacteria from food processing environments","volume":"275","author":"Heir","year":"2018","journal-title":"Int. J. Food Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1204","DOI":"10.4315\/0362-028X-63.9.1204","article-title":"Persistent Listeria monocytogenes strains show enhanced adherence to food contact surface after short contact times","volume":"63","author":"Miettinen","year":"2000","journal-title":"J. Food Prot."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2950","DOI":"10.1128\/AEM.68.6.2950-2958.2002","article-title":"Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation","volume":"68","author":"Djordjevic","year":"2002","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"150","DOI":"10.4315\/0362-028X.JFP-13-150","article-title":"Listeria monocytogenes persistence in food-associated environments: Epidemiology, strain characteristics, and implications for public health","volume":"77","author":"Ferreira","year":"2014","journal-title":"J. Food Prot."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"397","DOI":"10.3389\/fmicb.2017.00397","article-title":"Comparative Phenotypic and Genotypic Analysis of Swiss and Finnish Listeria monocytogenes Isolates with Respect to Benzalkonium Chloride Resistance","volume":"8","author":"Meier","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1089\/mdr.2009.0120","article-title":"Does the wide use of quaternary ammonium compounds enhance the selection and spread of antimicrobial resistance and thus threaten our health?","volume":"16","author":"Hegstad","year":"2010","journal-title":"Microb. Drug Resist."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.3389\/fmicb.2018.01103","article-title":"Virulence Gene Sequencing Highlights Similarities and Differences in Sequences in Listeria monocytogenes Serotype 1\/2a and 4b Strains of Clinical and Food Origin From 3 Different Geographic Locations","volume":"9","author":"Poimenidou","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1007\/s10123-018-0002-5","article-title":"Comparison of selected disinfectants efficiency against Listeria monocytogenes biofilm formed on various surfaces","volume":"21","author":"Skowron","year":"2018","journal-title":"Int. Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1128\/AEM.02038-18","article-title":"Behavior of Foodborne Pathogens Listeria monocytogenes and Staphylococcus aureus in Mixed-Species Biofilms Exposed to Biocides","volume":"84","author":"Oxaran","year":"2018","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1016\/j.fm.2010.09.014","article-title":"Resistance to benzalkonium chloride, peracetic acid and nisin during formation of mature biofilms by Listeria monocytogenes","volume":"28","author":"Herrera","year":"2011","journal-title":"Food Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.ijfoodmicro.2015.01.003","article-title":"Behavior of Listeria monocytogenes in a multi-species biofilm with Enterococcus faecalis and Enterococcus faecium and control through sanitation procedures","volume":"200","author":"Kabuki","year":"2015","journal-title":"Int. J. Food Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1006\/fmic.1997.0103","article-title":"Minimum inhibitory concentrations of antimicrobials against micro-organisms related to citrus juice","volume":"14","author":"Winniczuk","year":"1997","journal-title":"Food Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1139\/m92-104","article-title":"Bactericidal properties of peracetic acid and hydrogen peroxide, alone and in combination, and chlorine and formaldehyde against bacterial water strains","volume":"38","author":"Alasri","year":"1992","journal-title":"Can. J. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1186\/s13756-018-0307-3","article-title":"In vitro studies of the antibacterial activity of Copaifera spp. oleoresins, sodium hypochlorite, and peracetic acid against clinical and environmental isolates recovered from a hemodialysis unit","volume":"7","author":"Vieira","year":"2018","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.ijfoodmicro.2012.09.009","article-title":"Industrial disinfectants do not select for resistance in Listeria monocytogenes following long term exposure","volume":"160","author":"Kastbjerg","year":"2012","journal-title":"Int. J. Food Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.mcp.2012.10.001","article-title":"Real-time PCRs assay for serogrouping Listeria monocytogenes and differentiation from other Listeria spp.","volume":"27","author":"Vitullo","year":"2013","journal-title":"Mol. Cell. Probes"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/0378-1119(85)90120-9","article-title":"Improved M13 phage cloning vectors and host strains: Nucleotide sequences of the M13mpl8 and pUC19 vectors","volume":"33","author":"Vieira","year":"1985","journal-title":"Gene"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Ragon, M., Wirth, T., Hollandt, F., Lavenir, R., Lecuit, M., Le, M.A., and Brisse, S. (2008). A new perspective on Listeria monocytogenes evolution. PLoS Pathog., 4.","DOI":"10.1371\/journal.ppat.1000146"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1089\/cmb.2012.0021","article-title":"SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing","volume":"19","author":"Bankevich","year":"2012","journal-title":"J. Comput. Biol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1016\/S0964-8305(03)00039-8","article-title":"Bacterial disinfectant resistance\u2014A challenge for the food industry","volume":"51","author":"Langsrud","year":"2003","journal-title":"Int. J. Biodeter. Biodegrad."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1093\/nar\/25.17.3389","article-title":"Gapped BLAST and PSI-BLAST: A new generation of protein database search programs","volume":"25","author":"Altschul","year":"1997","journal-title":"Nucleic Acids Res."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Jordan, K., Fox, E.M., and Wagner, M. (2014). Listeria monocytogenes\u2014Methods and Protocols, Springer.","DOI":"10.1007\/978-1-4939-0703-8"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1038\/nprot.2007.521","article-title":"Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances","volume":"3","author":"Wiegand","year":"2008","journal-title":"Nat. Protoc."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Kuznetsova, A., Bruun Brockhoff, P., and Bojesen Christensen, H. (2018, December 14). lmerTest: Tests in Linear Mixed Effects Models. Available online: https:\/\/CRAN. R-project. org\/package=lmerTest.","DOI":"10.18637\/jss.v082.i13"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v069.i01","article-title":"Least-Squares Means: The RPackage lsmeans","volume":"69","author":"Lenth","year":"2016","journal-title":"J. Stat. Softw."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Venable, W.N., and Ripley, B.D. (2002). Modern Applied Statistics with S, Springer. [4th ed.].","DOI":"10.1007\/978-0-387-21706-2"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Wickham, H. (2009). ggplot2: Elegant graphics for data analysis. ggplot2: Elegant Graphics for Data Analysis, Springer.","DOI":"10.1007\/978-0-387-98141-3"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/8\/1\/32\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T12:37:04Z","timestamp":1760186224000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/8\/1\/32"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,3,7]]},"references-count":48,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2019,3]]}},"alternative-id":["pathogens8010032"],"URL":"https:\/\/doi.org\/10.3390\/pathogens8010032","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,3,7]]}}}