{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:56:57Z","timestamp":1787029017267,"version":"build-2736575974"},"reference-count":42,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2021,6,12]],"date-time":"2021-06-12T00:00:00Z","timestamp":1623456000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Listeria monocytogenes, the causative agent of listeriosis, is amongst the major food-borne pathogens in the world that affect mammal species, including humans. This microorganism has been associated with both sporadic episodes and large outbreaks of human listeriosis worldwide, with high mortality rates. In this study, the main sequence types (STs) and clonal complexes (CCs) were investigated in all of the 13 L. monocytogenes strains originating from different sources in the Republic of Serbia in 2004\u20132019 and that were available in the BIGSdb-Lm database. We found at least 13 STs belonging to the phylogenetic lineages I and II. These strains were represented by ST1\/ST3\/ST9 of CC1\/CC3\/CC9, which were common in the majority of the European countries and worldwide, as well as by eight novel STs (ST1232\/ST1233\/ST1234\/ST1235\/ST1238\/ST1236\/ST1237\/ST1242) of CC19\/CC155\/CC5\/CC21\/CC3\/CC315\/CC37, and the rare ST32 (clonal complex ST32) and ST734 (CC1), reported in the Republic of Serbia, the EU, for the first time. Our study confirmed the association of CC1 with cases of neuroinfection and abortions among small ruminants, and of CC3 and CC9 with food products of animal origin. The strains isolated in 2019 carried alleles of the internalin genes (inlA\/inlB\/inlC\/inlE) characteristic of the most virulent strains from the hypervirulent CC1. These findings demonstrated the genetic relatedness between L. monocytogenes strains isolated in the Republic of Serbia and worldwide. Our study adds further information about the diversity of the L. monocytogenes genotypes of small ruminants and food products, as the strain distribution in these sources in Serbia had not previously been evaluated.<\/jats:p>","DOI":"10.3390\/microorganisms9061289","type":"journal-article","created":{"date-parts":[[2021,6,14]],"date-time":"2021-06-14T22:25:46Z","timestamp":1623709546000},"page":"1289","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Novel Sequence Types of Listeria monocytogenes of Different Origin Obtained in the Republic of Serbia"],"prefix":"10.3390","volume":"9","author":[{"given":"Tatiana Yu.","family":"Bespalova","sequence":"first","affiliation":[{"name":"Federal Research Center for Virology and Microbiology, Branch in Samara, 443013 Samara, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tatiana V.","family":"Mikhaleva","sequence":"additional","affiliation":[{"name":"Federal Research Center for Virology and Microbiology, Branch in Samara, 443013 Samara, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadezhda Yu","family":"Meshcheryakova","sequence":"additional","affiliation":[{"name":"Federal Research Center for Virology and Microbiology, Branch in Samara, 443013 Samara, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olga V.","family":"Kustikova","sequence":"additional","affiliation":[{"name":"Federal Research Center for Virology and Microbiology, Branch in Samara, 443013 Samara, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kazimir","family":"Matovic","sequence":"additional","affiliation":[{"name":"Department for Laboratory Diagnostic, Veterinary Specialized Institute Kraljevo, 36000 Kraljevo, Serbia"},{"name":"Department of Food Safety, Veterinary Specialized Institute Kraljevo, 36000 Kraljevo, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marko","family":"Dmitri\u0107","sequence":"additional","affiliation":[{"name":"Department for Laboratory Diagnostic, Veterinary Specialized Institute Kraljevo, 36000 Kraljevo, Serbia"},{"name":"Department of Food Safety, Veterinary Specialized Institute Kraljevo, 36000 Kraljevo, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sergey S.","family":"Zaitsev","sequence":"additional","affiliation":[{"name":"Federal Research Center for Virology and Microbiology, Branch in Saratov, 410028 Saratov, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7053-8322","authenticated-orcid":false,"given":"Maria A.","family":"Khizhnyakova","sequence":"additional","affiliation":[{"name":"Federal Research Center for Virology and Microbiology, Branch in Saratov, 410028 Saratov, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Valentina A.","family":"Feodorova","sequence":"additional","affiliation":[{"name":"Federal Research Center for Virology and Microbiology, Branch in Saratov, 410028 Saratov, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,6,12]]},"reference":[{"key":"ref_1","first-page":"235","article-title":"Genetically related Listeria monocytogenes strains isolated from lethal human cases and wild animals","volume":"9","author":"Adgamov","year":"2012","journal-title":"Genet. Divers. Microorg."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"36419","DOI":"10.1038\/srep36419","article-title":"Listeria monocytogenes sequence type 1 is predominant in ruminant rhombencephalitis","volume":"6","author":"Dreyer","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"e1","DOI":"10.4102\/ojvr.v87i1.1869","article-title":"A review of Listeria monocytogenes from meat and meat products: Epidemiology, virulence factors, antimicrobial resistance and diagnosis","volume":"87","author":"Matle","year":"2020","journal-title":"Onderstepoort J. Vet. Res."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1080\/87559129.2016.1175017","article-title":"Listeria monocytogenes in retail establishments: Contamination routes and control strategies","volume":"33","author":"Lakicevic","year":"2017","journal-title":"Food Rev. Int."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Psareva, E.K., Egorova, I.Y., Liskova, E.A., Razheva, I.V., Gladkova, N.A., Sokolova, E.V., Potemkin, E.A., Zhurilov, P.A., Mikhaleva, T.V., and Blokhin, A.A. (2019). Retrospective Study of Listeria Monocytogenes Isolated in the Territory of Inner Eurasia from 1947 to 1999. Pathogens, 8.","DOI":"10.3390\/pathogens8040184"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"632513","DOI":"10.1155\/2010\/632513","article-title":"Rhombencephalitis Caused by Listeria monocytogenes in Humans and Ruminants: A Zoonosis on the Rise?","volume":"2010","author":"Oevermann","year":"2010","journal-title":"Interdiscip. Perspect. Infect. Dis."},{"key":"ref_7","unstructured":"ECDC (2019, December 12). The European Union One Health 2018 Zoonoses Report. Available online: https:\/\/www.ecdc.europa.eu\/en\/publications-data\/european-union-one-health-2018-zoonoses-report."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"3059","DOI":"10.1128\/AEM.00219-13","article-title":"Ruminant rhombencephalitis-associated Listeria monocytogenes strains constitute a genetically homogeneous group related to human outbreak strains","volume":"79","author":"Rocha","year":"2013","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"319","DOI":"10.17236\/sat00022","article-title":"Listeria monocytogenes infection in ruminants: Is there a link to the environment, food and human health? A review","volume":"157","author":"Walland","year":"2015","journal-title":"Schweiz. Arch. Tierheilkd."},{"key":"ref_10","first-page":"e05134","article-title":"Listeria monocytogenes contamination of ready-to-eat foods and the risk for human health in the EU","volume":"16","author":"Ricci","year":"2018","journal-title":"EFSA J."},{"key":"ref_11","unstructured":"Whitworth, J. (2020, May 14). Officials Report More Patients in Listeria Outbreak Linked to Cheese. Available online: https:\/\/www.foodsafetynews.com\/2020\/05\/more-patients-reported-in-listeria-outbreak-linked-to-cheese."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1089\/fpd.2018.2586","article-title":"Outbreak of Listeria monocytogenes in South Africa, 2017\u20132018: Laboratory Activities and Experiences Associated with Whole-Genome Sequencing Analysis of Isolates","volume":"16","author":"Smith","year":"2019","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1016\/S1473-3099(14)70870-9","article-title":"The global burden of listeriosis: A systematic review and meta-analysis","volume":"14","author":"Devleesschauwer","year":"2014","journal-title":"Lancet Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"W728","DOI":"10.1093\/nar\/gki415","article-title":"The multilocus sequence typing network: Mlst.net","volume":"33","author":"Aanensen","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1007\/978-1-0716-0982-8_7","article-title":"Multilocus Sequence Typing (MLST) and Whole Genome Sequencing (WGS) of Listeria monocytogenes and Listeria innocua","volume":"2220","author":"Stessl","year":"2021","journal-title":"Methods Mol. Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1110","DOI":"10.3201\/eid\/1706.101778","article-title":"Worldwide distribution of major clones of Listeria monocytogenes","volume":"17","author":"Lopez","year":"2011","journal-title":"Emerg. Infect. Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1128\/JCM.41.2.757-762.2003","article-title":"Development of a multilocus sequence typing method for analysis of Listeria monocytogenes clones","volume":"41","author":"Salcedo","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Ragon, M., Wirth, T., Hollandt, F., Lavenir, R., Lecuit, M., Le Monnier, A., and Brisse, S. (2008). A new perspective on Listeria monocytogenes evolution. PLoS Pathog., 4.","DOI":"10.1371\/journal.ppat.1000146"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.ijmm.2010.05.002","article-title":"Listeria monocytogenes lineages: Genomics, evolution, ecology, and phenotypic characteristics","volume":"301","author":"Orsi","year":"2011","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1089\/fpd.2015.2115","article-title":"The Continuous Challenge of Characterizing the Foodborne Pathogen Listeria monocytogenes","volume":"13","author":"Camargo","year":"2016","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.fm.2009.09.001","article-title":"Amplified Fragment Length Polymorphism and Multi-Locus Sequence Typing for high-resolution genotyping of Listeria monocytogenes from foods and the environment","volume":"27","author":"Parisi","year":"2010","journal-title":"Food Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Matereke, L.T., and Okoh, A.I. (2020). Listeria monocytogenes Virulence, Antimicrobial Resistance and Environmental Persistence: A Review. Pathogens, 9.","DOI":"10.3390\/pathogens9070528"},{"key":"ref_23","unstructured":"Petrovic, V., Petrovic, M., Dragovac, G., Ristic, M., Medic, S., Ilic, S., Rachevic, S., and Shtrbac, M. (2019). Infectious Diseases in Vojvodina in 2018, Institute of Public Health of Vojvod."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Banovic, F., Schroten, H., and Schwerk, C. (2020). Potential Roles and Functions of Listerial Virulence Factors during Brain Entry. Toxins, 12.","DOI":"10.3390\/toxins12050297"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/B978-0-12-394590-7.00007-5","article-title":"Chapter 3\u2014Virulence Factors That Modulate the Cell Biology of Listeria Infection and the Host Response","volume":"Volume 113","author":"Mostowy","year":"2012","journal-title":"Advances in Immunology"},{"key":"ref_26","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_27","first-page":"266","article-title":"New Methods for Identification of Listeria monocytogenes","volume":"3","author":"Karpova","year":"2001","journal-title":"Clin. Microbiol. Antimicrob. Chemother."},{"key":"ref_28","first-page":"5","article-title":"Diversity and Pathogenic Potential of Listeria monocytogenes Isolated from Environmental Sources in the Russian Federation","volume":"5","author":"Voronina","year":"2015","journal-title":"IJMER"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1395","DOI":"10.1101\/gr.232397.117","article-title":"GrapeTree: Visualization of core genomic relationships among 100,000 bacterial pathogens","volume":"28","author":"Zhou","year":"2018","journal-title":"Genome Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1093\/molbev\/msw054","article-title":"MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets","volume":"33","author":"Kumar","year":"2016","journal-title":"Mol. Biol. Evol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"3299","DOI":"10.1093\/molbev\/msx248","article-title":"DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets","volume":"34","author":"Rozas","year":"2017","journal-title":"Mol. Biol. Evol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Papic, B., Pate, M., Felix, B., and Kusar, D. (2019). Genetic diversity of Listeria monocytogenes strains in ruminant abortion and rhombencephalitis cases in comparison with the natural environment. BMC Microbiol., 19.","DOI":"10.1186\/s12866-019-1676-3"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"104047","DOI":"10.1016\/j.meegid.2019.104047","article-title":"Retrospective investigation of listeriosis outbreaks in small ruminants using different analytical approaches for whole genome sequencing-based typing of Listeria monocytogenes","volume":"77","author":"Papic","year":"2020","journal-title":"Infect. Genet. Evol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"5720","DOI":"10.1128\/AEM.00583-16","article-title":"Population Genetic Structure of Listeria monocytogenes Strains as Determined by Pulsed-Field Gel Electrophoresis and Multilocus Sequence Typing","volume":"82","author":"Henri","year":"2016","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"684","DOI":"10.3389\/fmicb.2018.00684","article-title":"Population Genetic Structure of Listeria monocytogenes Strains Isolated From the Pig and Pork Production Chain in France","volume":"9","author":"Feurer","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Fagerlund, A., Langsrud, S., and Moretro, T. (2020). In-Depth Longitudinal Study of Listeria monocytogenes ST9 Isolates from the Meat Processing Industry: Resolving Diversity and Transmission Patterns Using Whole-Genome Sequencing. Appl. Environ. Microbiol., 86.","DOI":"10.1128\/AEM.00579-20"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Guidi, F., Orsini, M., Chiaverini, A., Torresi, M., Centorame, P., Acciari, V.A., Salini, R., Palombo, B., Brandi, G., and Amagliani, G. (2021). Hypo- and Hyper-Virulent Listeria monocytogenes Clones Persisting in Two Different Food Processing Plants of Central Italy. Microorganisms, 9.","DOI":"10.3390\/microorganisms9020376"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"6152","DOI":"10.1073\/pnas.0401434101","article-title":"Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: Role of internalin interaction with trophoblast E-cadherin","volume":"101","author":"Lecuit","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1186\/s40168-019-0726-2","article-title":"The occurrence of Listeria monocytogenes is associated with built environment microbiota in three tree fruit processing facilities","volume":"7","author":"Tan","year":"2019","journal-title":"Microbiome"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"12170","DOI":"10.1038\/s41598-019-48597-0","article-title":"Survival of outbreak, food, and environmental strains of Listeria monocytogenes on whole apples as affected by cultivar and wax coating","volume":"9","author":"Macarisin","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1017\/S0950268816003083","article-title":"Multistate outbreak of Listeria monocytogenes infections linked to whole apples used in commercially produced, prepackaged caramel apples: United States, 2014\u20132015","volume":"145","author":"Angelo","year":"2017","journal-title":"Epidemiol. Infect."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"966","DOI":"10.1038\/s41559-019-0878-2","article-title":"The genetic history of admixture across inner Eurasia","volume":"3","author":"Jeong","year":"2019","journal-title":"Nat. Ecol. Evol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/6\/1289\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:13:45Z","timestamp":1760163225000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/6\/1289"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,12]]},"references-count":42,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2021,6]]}},"alternative-id":["microorganisms9061289"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms9061289","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,12]]}}}