{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T16:48:52Z","timestamp":1786121332465,"version":"build-2736575974"},"reference-count":49,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2026,8,5]],"date-time":"2026-08-05T00:00:00Z","timestamp":1785888000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000780","name":"European Union","doi-asserted-by":"crossref","award":["101112724"],"award-info":[{"award-number":["101112724"]}],"id":[{"id":"10.13039\/501100000780","id-type":"DOI","asserted-by":"crossref"}]},{"award":["101112724"],"award-info":[{"award-number":["101112724"]}],"id":[{"id":"https:\/\/ror.org\/019w4f821","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>This study aimed to identify circulating lineages of the most prevalent human-associated Salmonella serotypes identified through routine surveillance in Romania between 2023 and 2025 and assess their role in the spread of antimicrobial resistance (AMR). A total of 271 isolates (217 S. Enteritidis, 28 monophasic S. Typhimurium, and 26 S. Typhimurium) were investigated using Illumina short-read sequencing. The isolates were assigned to 9 MLST sequence types (STs) and 109 core genome MLST complex types. The predominant STs were ST11 (96% in S. Enteritidis), ST19 (77% in S. Typhimurium), and ST34 (79% in monophasic S. Typhimurium). Overall, 148 isolates carried at least one AMR determinant, including 28 acquired genes and 6 gene mutations, conferring resistance to ten antimicrobial classes. Four percent of all isolates were predicted to be multidrug-resistant, often associated with determinants conferring tolerances to biocides and\/or heavy metals. The most prevalent resistance markers were GyrA_D87Y in S. Enteritidis ST11 (94\/217) and blaTEM-1 in S. Typhimurium ST19 (7\/26). Among monophasic S. Typhimurium ST34 isolates, the co-occurrence of blaTEM-1, aph(3\u201d)-Ib, aph(6)-Id, sul2, and tet(B) genes was common (17\/28). The 43 predicted AMR plasmids were not shared across serotypes, except among those carrying the qnrB19 gene. These results provide a genomic baseline for AMR surveillance in Romania and strengthen the human surveillance component of national One Health efforts to control resistant Salmonella.<\/jats:p>","DOI":"10.3390\/microorganisms14081716","type":"journal-article","created":{"date-parts":[[2026,8,5]],"date-time":"2026-08-05T09:16:22Z","timestamp":1785921382000},"page":"1716","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Genomic Insights into the Population Structure and Antimicrobial Resistance of the Most Prevalent Human-Associated Non-Typhoidal Salmonella Serotypes in Romania"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7673-5957","authenticated-orcid":false,"given":"Mihaela","family":"Oprea","sequence":"first","affiliation":[{"name":"Cantacuzino National Military Medical Institute for Research and Development, 103 Splaiul Independentei, 050096 Bucharest, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura-Ioana","family":"Popa","sequence":"additional","affiliation":[{"name":"Cantacuzino National Military Medical Institute for Research and Development, 103 Splaiul Independentei, 050096 Bucharest, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniela","family":"Cristea","sequence":"additional","affiliation":[{"name":"Cantacuzino National Military Medical Institute for Research and Development, 103 Splaiul Independentei, 050096 Bucharest, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6762-2718","authenticated-orcid":false,"given":"Sorin","family":"Dinu","sequence":"additional","affiliation":[{"name":"Cantacuzino National Military Medical Institute for Research and Development, 103 Splaiul Independentei, 050096 Bucharest, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andreea","family":"Ghi\u021b\u0103","sequence":"additional","affiliation":[{"name":"Cantacuzino National Military Medical Institute for Research and Development, 103 Splaiul Independentei, 050096 Bucharest, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7399-2379","authenticated-orcid":false,"given":"Catherine","family":"Ragimbeau","sequence":"additional","affiliation":[{"name":"Luxembourg National Health Laboratory, 1 Rue Louis Rech, L-3555 Dudelange, Luxembourg"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-8348-4297","authenticated-orcid":false,"given":"Lavinia-Cipriana","family":"Rusu","sequence":"additional","affiliation":[{"name":"National Institute of Public Health, 1\u20133 Dr. Leonte Anastasievici Street, 050463 Bucharest, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5442-0500","authenticated-orcid":false,"given":"Codru\u021ba-Romani\u021ba","family":"Usein","sequence":"additional","affiliation":[{"name":"Cantacuzino National Military Medical Institute for Research and Development, 103 Splaiul Independentei, 050096 Bucharest, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,8,5]]},"reference":[{"key":"ref_1","unstructured":"European Centre for Disease Prevention and Control (2025). Salmonellosis. ECDC. Annual Epidemiological Report for 2023, ECDC."},{"key":"ref_2","unstructured":"European Centre for Disease Prevention and Control (2019). ECDC Strategic Framework for Integrating Molecular and Genomic Typing into European Surveillance and Multi-Country Outbreak Investigations\u20142019\u20132021, ECDC."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Khoury, M.J., Armstrong, G.L., Bunnell, R.E., Cyril, J., and Iademarco, M.F. (2020). The intersection of genomics and big data with public health: Opportunities for precision public health. PLoS Med., 17.","DOI":"10.1371\/journal.pmed.1003373"},{"key":"#cr-split#-ref_4.1","unstructured":"EUR-Lex (2025). Commission Implementing Regulation"},{"key":"#cr-split#-ref_4.2","unstructured":"(EU) 2025\/179 of 31 January 2025 on the collection and transmission of molecular analytical data within the frame of epidemiological investigations of food-borne outbreaks in accordance with Directive 2003\/99\/EC of the European Parliament and of the Council. Off. J. Eur. Union, 179, 1-3. Available online: https:\/\/eur-lex.europa.eu\/eli\/reg_impl\/2025\/179\/oj\/eng."},{"key":"ref_5","unstructured":"European Centre for Disease Prevention and Control (2025). Fourteenth External Quality Assessment for Salmonella Typing, ECDC."},{"key":"ref_6","unstructured":"The European Committee on Antimicrobial Susceptibility Testing (2026). Breakpoint Tables for Interpretation of MICs and Zone Diameters, Version 16.0, EUCAST. Available online: http:\/\/www.eucast.org."},{"key":"ref_7","unstructured":"(2025, November 20). Food- and Waterborne Diseases Antimicrobial Resistance\u2014Reference Laboratory Capacity. Available online: https:\/\/www.fwdamr-reflabcap.eu\/."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Achtman, M., Wain, J., Weill, F.X., Nair, S., Zhou, Z., Sangal, V., Krauland, M.G., Hale, J.L., Harbottle, H., and Uesbeck, A. (2012). Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog., 8, Erratum in PLoS Pathog.\u00a02020, 21, e1009040. https:\/\/doi.org\/10.1371\/journal.ppat.1009040.","DOI":"10.1371\/journal.ppat.1009040"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Alikhan, N.F., Zhou, Z., Sergeant, M.J., and Achtman, M. (2018). A genomic overview of the population structure of Salmonella. PLoS Genet., 14.","DOI":"10.1371\/journal.pgen.1007261"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"European Centre for Disease Prevention and Control, European Food Safety Authority (2022). Multi-country outbreak of Salmonella Enteritidis sequence type (ST)11 infections linked to eggs and egg products\u20148 February 2022. EFSA Support. Publ., 19, 7180E.","DOI":"10.2903\/sp.efsa.2022.EN-7180"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1007\/s10534-010-9393-2","article-title":"Bacterial gold sensing and resistance","volume":"24","author":"Soncini","year":"2011","journal-title":"Biometals"},{"key":"ref_12","unstructured":"(2026, January 20). European Observatory on Health Systems and Policies. Available online: https:\/\/eurohealthobservatory.who.int\/monitors\/health-systems-monitor\/updates\/hspm\/romania-2016\/measure-to-reduce-antimicrobial-resistance."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"European Food Safety Authority (EFSA), and European Centre for Disease Prevention and Control (ECDC) (2025). The European Union One Health 2024 Zoonoses Report. EFSA J., 23, e9759.","DOI":"10.2903\/j.efsa.2025.9759"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1016\/S1473-3099(19)30047-7","article-title":"An international outbreak of Salmonella enterica serotype Enteritidis linked to eggs from Poland: A microbiological and epidemiological study","volume":"19","author":"Pijnacker","year":"2019","journal-title":"Lancet Infect. Dis."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1016\/j.ijantimicag.2005.02.006","article-title":"Mechanisms of quinolone resistance in Escherichia coli and Salmonella: Recent developments","volume":"25","author":"Hopkins","year":"2005","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2587","DOI":"10.1128\/AEM.71.5.2587-2591.2005","article-title":"Clonal expansion may account for high levels of quinolone resistance in Salmonella enterica serovar enteritidis","volume":"71","author":"Kilmartin","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"e00738-24","DOI":"10.1128\/aac.00738-24","article-title":"Molecular epidemiology of Salmonella Enteritidis in humans and animals in Spain","volume":"69","author":"Maex","year":"2025","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_18","first-page":"001394","article-title":"Genomic epidemiology of Salmonella Enteritidis human infections in the Netherlands, 2019 to 2023","volume":"11","author":"Franz","year":"2025","journal-title":"Microb. Genom."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Forgaciu, A., Tabaran, A., Colobatiu, L., Mihaiu, R., Dan, S.D., and Mihaiu, M. (2022). Concerning Increase in Antimicrobial Resistance Patterns of Pathogenic Strains of Salmonella Isolated in Poultry Meat Products. Antibiotics, 11.","DOI":"10.3390\/antibiotics11111469"},{"key":"ref_20","first-page":"246","article-title":"Genetic outlook of Colistin resistant Salmonella enterica Serovar Typhimurium recovered from Poultry-Environment Interface: A One Health Standpoint","volume":"45","author":"Mahmood","year":"2025","journal-title":"Pak. Vet. J."},{"key":"ref_21","first-page":"55","article-title":"Identification of plasmid-mediated quinolone resistance qnr-like genes in Romanian clinical isolates of Escherichia coli and Klebsiella pneumoniae","volume":"68","author":"Usein","year":"2009","journal-title":"Roum. Arch. Microbiol. Immunol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1186\/s13099-015-0063-3","article-title":"First description of plasmid-mediated quinolone resistance determinants and \u03b2-lactamase encoding genes in non-typhoidal Salmonella isolated from humans, one companion animal and food in Romania","volume":"7","author":"Colobatiu","year":"2015","journal-title":"Gut Pathog."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Doma, A.O., Popescu, R., Mitule\u021bu, M., Muntean, D., D\u00e9gi, J., Boldea, M.V., Radulov, I., Dumitrescu, E., Muselin, F., and Puva\u010da, N. (2020). Comparative Evaluation of qnrA, qnrB, and qnrS Genes in Enterobacteriaceae Ciprofloxacin-Resistant Cases, in Swine Units and a Hospital from Western Romania. Antibiotics, 9.","DOI":"10.3390\/antibiotics9100698"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1089\/mdr.2011.0068","article-title":"First report on IncN plasmid-mediated quinolone resistance gene qnrS1 in porcine Escherichia coli in Europe","volume":"17","author":"Szmolka","year":"2011","journal-title":"Microb. Drug Resist."},{"key":"ref_25","unstructured":"WHO (2024). WHO Bacterial Priority Pathogens List, 2024: Bacterial Pathogens of Public Health Importance to Guide Research, Development and Strategies to Prevent and Control Antimicrobial Resistance, World Health Organization."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1093\/jac\/dkn470","article-title":"Characterization of plasmids harbouring qnrS1, qnrB2 and qnrB19 genes in Salmonella","volume":"63","author":"Fortini","year":"2009","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1821","DOI":"10.1128\/AAC.06036-11","article-title":"Small plasmids harboring qnrB19: A model for plasmid evolution mediated by site-specific recombination at oriT and Xer sites","volume":"56","author":"Tran","year":"2012","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/j.diagmicrobio.2019.02.015","article-title":"Subtyping of plasmid-mediated quinolone resistance among Salmonella serotypes by whole genome sequencing","volume":"94","author":"Soares","year":"2019","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1111\/j.1574-6968.2010.02119.x","article-title":"Characterization of antimicrobial resistance in Salmonella enterica food and animal isolates from Colombia: Identification of a qnrB19-mediated quinolone resistance marker in two novel serovars","volume":"313","author":"Karczmarczyk","year":"2010","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2785","DOI":"10.1021\/acsinfecdis.4c00150","article-title":"Interplay between Amino Acid Substitution in GyrA and QnrB19: Elevating Fluoroquinolone Resistance in Salmonella Typhimurium","volume":"10","author":"Suwanthada","year":"2024","journal-title":"ACS Infect. Dis."},{"key":"ref_31","unstructured":"European Centre for Disease Prevention and Control (2024). Salmonellosis. ECDC. Annual Epidemiological Report for 2022, ECDC."},{"key":"ref_32","unstructured":"(2026, January 28). Enterobase. Available online: https:\/\/enterobase.warwick.ac.uk\/."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2500224","DOI":"10.2807\/1560-7917.ES.2025.30.41.2500224","article-title":"Insights into recurring multi-country outbreaks of Salmonella Strathcona associated with tomatoes, Europe, 2011 to 2024","volume":"30","author":"Brait","year":"2025","journal-title":"Eurosurveillance"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Leeper, M.M., Tolar, B.M., Griswold, T., Vidyaprakash, E., Hise, K.B., Williams, G.M., Im, S.B., Chen, J.C., Pouseele, H., and Carleton, H.A. (2023). Evaluation of whole and core genome multilocus sequence typing allele schemes for Salmonella enterica outbreak detection in a national surveillance network, PulseNet USA. Front. Microbiol., 14.","DOI":"10.3389\/fmicb.2023.1254777"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ijfoodmicro.2018.02.023","article-title":"Comparative analysis of core genome MLST and SNP typing within a European Salmonella serovar Enteritidis outbreak","volume":"274","author":"Pearce","year":"2018","journal-title":"Int. J. Food Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1093\/jac\/dkr391","article-title":"Nucleotide sequence of the chromosomal region conferring multidrug resistance (R-type ASSuT) in Salmonella Typhimurium and monophasic Salmonella Typhimurium strains","volume":"67","author":"Lucarelli","year":"2012","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"E11","DOI":"10.2807\/esm.12.06.00719-en","article-title":"Outbreaks of monophasic Salmonella enterica serovar 4,[5],12:i:- in Luxembourg, 2006","volume":"12","author":"Mossong","year":"2007","journal-title":"Eurosurveillance"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3109\/1040841X.2015.1136261","article-title":"Macrolide resistance mechanisms in Enterobacteriaceae: Focus on azithromycin","volume":"43","author":"Gomes","year":"2017","journal-title":"Crit. Rev. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"e00853-19","DOI":"10.1128\/mBio.00853-19","article-title":"Identification of Novel Mobilized Colistin Resistance Gene mcr-9 in a Multidrug-Resistant, Colistin-Susceptible Salmonella enterica Serotype Typhimurium Isolate","volume":"10","author":"Carroll","year":"2019","journal-title":"mBio"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"e0010522","DOI":"10.1128\/msystems.00105-22","article-title":"Global Distribution of mcr Gene Variants in 214K Metagenomic Samples","volume":"7","author":"Martiny","year":"2022","journal-title":"mSystems"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Dossouvi, K.M., Sellera, F.P., Ibadin, E.E., Bouyo, T., Kanzin, D., Ba, B.S., Dossim, S., El Kelish, A., and Camara, M. (2026). Global distribution of mcr-carrying bacteria: An analysis of genomic data. BMC Med. Genom., 19.","DOI":"10.1186\/s12920-026-02383-w"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1856.e7","DOI":"10.1016\/j.cmi.2021.04.020","article-title":"Silent spread of mobile colistin resistance gene mcr-9.1 on IncHI2 \u2018superplasmids\u2019 in clinical carbapenem-resistant Enterobacterales","volume":"27","author":"Macesic","year":"2021","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_43","first-page":"mgen001002","article-title":"A global survey of Salmonella plasmids and their associations with antimicrobial resistance","volume":"9","author":"Robertson","year":"2023","journal-title":"Microb. Genom."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Clark, C.G., Landgraff, C., Robertson, J., Pollari, F., Parker, S., Nadon, C., Gannon, V.P.J., Johnson, R., and Nash, J. (2020). Distribution of heavy metal resistance elements in Canadian Salmonella 4,[5],12:i:- populations and association with the monophasic genotypes and phenotype. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0236436"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Diaconu, E.L., Alba, P., Feltrin, F., Di Matteo, P., Iurescia, M., Chelli, E., Donati, V., Marani, I., Giacomi, A., and Franco, A. (2021). Emergence of IncHI2 Plasmids with Mobilized Colistin Resistance (mcr)-9 Gene in ESBL-Producing, Multidrug-Resistant Salmonella Typhimurium and Its Monophasic Variant ST34 From Food-Producing Animals in Italy. Front. Microbiol., 12.","DOI":"10.3389\/fmicb.2021.705230"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"11482","DOI":"10.1038\/s41598-021-90299-z","article-title":"Genomic analysis and phylogenetic position of the complex IncC plasmid found in the Spanish monophasic clone of Salmonella enterica serovar Typhimurium","volume":"11","author":"Ladero","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Paganini, J.A., Plantinga, N.L., Arredondo-Alonso, S., Willems, R.J.L., and Sch\u00fcrch, A.C. (2021). Recovering Escherichia coli Plasmids in the Absence of Long-Read Sequencing Data. Microorganisms, 9.","DOI":"10.3390\/microorganisms9081613"},{"key":"ref_48","unstructured":"Council of the European Union (2023). Council Recommendation of 13 June 2023 on stepping up EU actions to combat antimicrobial resistance in a One Health approach (2023\/C 220\/01). Off. J. Eur. Union, 220, 1\u201320. Available online: https:\/\/eur-lex.europa.eu\/legal-content\/EN\/TXT\/PDF\/?uri=OJ:JOC_2023_220_R_0001."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/14\/8\/1716\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T04:23:14Z","timestamp":1786076594000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/14\/8\/1716"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,5]]},"references-count":49,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2026,8]]}},"alternative-id":["microorganisms14081716"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms14081716","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,5]]}}}