{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T18:55:33Z","timestamp":1789584933327,"version":"build-2803163510"},"reference-count":39,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,1,27]],"date-time":"2023-01-27T00:00:00Z","timestamp":1674777600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Institute of Public Health\u2013National Institute of Hygiene","award":["5\/EM.1-2018"],"award-info":[{"award-number":["5\/EM.1-2018"]}]},{"name":"National Institute of Public Health\u2013National Institute of Hygiene","award":["BB-1\/2019"],"award-info":[{"award-number":["BB-1\/2019"]}]},{"name":"National Institute of Public Health\u2013National Institute of Hygiene","award":["BB-1\/2020"],"award-info":[{"award-number":["BB-1\/2020"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Salmonellosis remains the second most common zoonosis in Europe. Resistance to fluoroquinolones (FQs) in Salmonella has been increasing worldwide, with WHO considering FQ-resistant Salmonella spp. as high-priority pathogens. The aim of this study was a retrospective analysis of the molecular mechanisms of FQ resistance, detected among clinical ciprofloxacin-resistant Salmonella enterica belonging to the most common serotypes. The whole genome sequences (WGS) of tested isolates were also analysed for the occurrence of other antimicrobial resistance determinants. Out of a total of 1051 Salmonella collected in the years 2018\u20132019, 447 strains belonging to the most common serotypes in Poland were selected were screened for FQ resistance using the pefloxacin disc test according to EUCAST recommendations. All pefloxacin-resistant isolates were confirmed as ciprofloxacin-resistant using the E-test. A total of 168 (37.6%) Salmonella enterica, which belonged to seven serotypes, were resistant to ciprofloxacin (mostly Hadar, Virchow and Newport). A hundred randomly selected Salmonella were investigated by WGS. A total of 127 QRDR mutations in GyrA and ParC were identified in 93 isolates. The qnr genes were the only PMQR determinants detected and were found in 19% of the sequenced isolates. Moreover, 19 additional resistance genes (including: bla,,tet, sul, aad, aac-, ant-, aph-, floR, cmlA) were identified among the FQ-resistant Salmonella tested that confer resistance to clinically important antibiotics such as \u03b2-lactams, tetracyclines, sulphonamides, aminoglycosides and phenicol, respectively). In conclusion, FQ resistance of human Salmonella in Poland is rising towards a critical level and needs to be tightly monitored.<\/jats:p>","DOI":"10.3390\/pathogens12020193","type":"journal-article","created":{"date-parts":[[2023,1,30]],"date-time":"2023-01-30T02:54:37Z","timestamp":1675047277000},"page":"193","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["The Mechanisms Involved in the Fluoroquinolone Resistance of Salmonella enterica Strains Isolated from Humans in Poland, 2018\u20132019: The Prediction of Antimicrobial Genes by In Silico Whole-Genome Sequencing"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1763-3475","authenticated-orcid":false,"given":"Katarzyna","family":"Piekarska","sequence":"first","affiliation":[{"name":"Department of Bacteriology and Biocontamination Control, National Institute of Public Health NIH\u2014National Research Institute, 00-791 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8897-4210","authenticated-orcid":false,"given":"Tomasz","family":"Wo\u0142kowicz","sequence":"additional","affiliation":[{"name":"Department of Bacteriology and Biocontamination Control, National Institute of Public Health NIH\u2014National Research Institute, 00-791 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1476-2172","authenticated-orcid":false,"given":"Katarzyna","family":"Zacharczuk","sequence":"additional","affiliation":[{"name":"Department of Bacteriology and Biocontamination Control, National Institute of Public Health NIH\u2014National Research Institute, 00-791 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Agata","family":"Stepuch","sequence":"additional","affiliation":[{"name":"Department of Bacteriology and Biocontamination Control, National Institute of Public Health NIH\u2014National Research Institute, 00-791 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2106-1203","authenticated-orcid":false,"given":"Rafa\u0142","family":"Gierczy\u0144ski","sequence":"additional","affiliation":[{"name":"Department of Bacteriology and Biocontamination Control, National Institute of Public Health NIH\u2014National Research Institute, 00-791 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,1,27]]},"reference":[{"key":"ref_1","unstructured":"Grimont, P.A.D., and Weill, F.X. (2007). Antigenic Formulae of the Salmonella Serovars, WHO Collaborating Centre for Reference and Research on Salmonella, Pasteur Institute. [9th ed.]."},{"key":"ref_2","first-page":"e06490","article-title":"European Centre for Disease Prevention and Control the European Union Summary Report on Antimicrobial Resistance in Zoonotic and Indicator Bacteria from Humans, Animals and Food in 2018\/2019","volume":"19","author":"Authority","year":"2021","journal-title":"EFSA J."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"7","DOI":"10.3201\/eid1701.P11101","article-title":"Foodborne Illness Acquired in the United States\u2014Major Pathogens","volume":"17","author":"Scallan","year":"2011","journal-title":"Emerg. Infect. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1093\/jac\/dkt469","article-title":"Resistance to Third-Generation Cephalosporins in Human Non-Typhoidal Salmonella enterica Isolates from England and Wales, 2010\u201312","volume":"69","author":"Burke","year":"2014","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_5","unstructured":"World Health Organization (2019). Critically Important Antimicrobials for Human Medicine, World Health Organization. [6th ed.]."},{"key":"ref_6","unstructured":"Medicine, C., and For, V. (2022). Extralabel Use and Antimicrobials."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.ijfoodmicro.2011.12.032","article-title":"The Antibiotic Resistance Characteristics of Non-Typhoidal Salmonella Enterica Isolated from Food-Producing Animals, Retail Meat and Humans in South East Asia","volume":"154","author":"Van","year":"2012","journal-title":"Int. J. Food Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1007\/s10096-016-2847-x","article-title":"Plasmid-Mediated Quinolone Resistance in Enterobacteriaceae: A Systematic Review with a Focus on Mediterranean Countries","volume":"36","author":"Yanat","year":"2017","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis. Off. Publ. Eur. Soc. Clin. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2885","DOI":"10.2147\/IDR.S210961","article-title":"Molecular Epidemiology and Antimicrobial Resistance of Invasive Non-Typhoidal Salmonella in China, 2007\u20132016","volume":"12","author":"Zhan","year":"2019","journal-title":"Infect. Drug Resist."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1016\/S1473-3099(17)30753-3","article-title":"Discovery, Research, and Development of New Antibiotics: The WHO Priority List of Antibiotic-Resistant Bacteria and Tuberculosis","volume":"18","author":"Tacconelli","year":"2018","journal-title":"Lancet Infect. Dis."},{"key":"ref_11","first-page":"38","article-title":"Mechanisms of Fluoroquinolone Resistance","volume":"2","author":"Hooper","year":"1999","journal-title":"Drug Resist. Updat. Rev. Comment. Antimicrob. Anticancer Chemother."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1016\/j.ijantimicag.2014.09.019","article-title":"Co-Existence of Plasmid-Mediated Quinolone Resistance Determinants and Mutations in GyrA and ParC among Fluoroquinolone-Resistant Clinical Enterobacteriaceae Isolated in a Tertiary Hospital in Warsaw, Poland","volume":"45","author":"Piekarska","year":"2015","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1128\/microbiolspec.PLAS-0006-2013","article-title":"Plasmid-Mediated Quinolone Resistance","volume":"2","author":"Jacoby","year":"2014","journal-title":"Microbiol. Spectr."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Fang, S.-B., Lauderdale, T.-L.Y., Huang, C.-H., Chang, P.-R., Wang, Y.-H., Shigemura, K., Lin, Y.-H., Chang, W.-C., Wang, K.-C., and Huang, T.-W. (2021). Genotypic Diversity of Ciprofloxacin Nonsusceptibility and Its Relationship with Minimum Inhibitory Concentrations in Nontyphoidal Salmonella Clinical Isolates in Taiwan. Antibiotics, 10.","DOI":"10.3390\/antibiotics10111383"},{"key":"ref_15","unstructured":"(2022, October 24). Salmonellosis-Annual Epidemiological Report for 2017. Available online: https:\/\/www.ecdc.europa.eu\/en\/publications-data\/salmonellosis-annual-epidemiological-report-2017."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Wo\u0142kowicz, T., Zacharczuk, K., Gierczy\u0144ski, R., Nowakowska, M., and Piekarska, K. (2021). Antimicrobial Resistance and Whole-Genome Characterisation of High-Level Ciprofloxacin-Resistant Salmonella Enterica Serovar Kentucky ST 198 Strains Isolated from Human in Poland. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22179381"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1685","DOI":"10.1128\/JCM.00323-15","article-title":"Salmonella Serotype Determination Utilizing High-Throughput Genome Sequencing Data","volume":"53","author":"Zhang","year":"2015","journal-title":"J. Clin. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1355","DOI":"10.1128\/JCM.06094-11","article-title":"Multilocus Sequence Typing of Total-Genome-Sequenced Bacteria","volume":"50","author":"Larsen","year":"2012","journal-title":"J. Clin. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3491","DOI":"10.1093\/jac\/dkaa345","article-title":"ResFinder 4.0 for Predictions of Phenotypes from Genotypes","volume":"75","author":"Bortolaia","year":"2020","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Kaas, R.S., Leekitcharoenphon, P., Aarestrup, F.M., and Lund, O. (2014). Solving the Problem of Comparing Whole Bacterial Genomes across Different Sequencing Platforms. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0104984"},{"key":"ref_21","unstructured":"Official Journal of the European Union (2018). Commission Implementing Decision (EU) 2018\/945 of 22 June 2018 on the Communicable Diseases and Related Special Health Issues to Be Covered by Epidemiological Surveillance as Well as Relevant Case Definitions (Text with EEA Relevance), Official Journal of the European Union."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3355","DOI":"10.1007\/s11356-021-17374-w","article-title":"Antibiotic Residues in Environment: Antimicrobial Resistance Development, Ecological Risks, and Bioremediation","volume":"29","author":"Apreja","year":"2022","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Pikkemaat, M.G., Yassin, H., Fels-Klerx, H.J., and Berendsen, B.J.A. (2016). RIKILT-BU Toxicology Bioassays & Novel Foods, VLAG, RIKILT-Business unit Dierbehandelingsmiddelen. Antibiotic Residues and Resistance in the Environment, RIKILT Wageningen UR.","DOI":"10.18174\/388253"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.diagmicrobio.2014.01.010","article-title":"Prevalence of Quinolone Resistance Determinants in Non-Typhoidal Salmonella Isolates from Human Origin in Extremadura, Spain","volume":"79","author":"Campos","year":"2014","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"3832","DOI":"10.1128\/AAC.00121-09","article-title":"Mechanisms of Resistance in Nontyphoidal Salmonella Enterica Strains Exhibiting a Nonclassical Quinolone Resistance Phenotype","volume":"53","author":"Gunell","year":"2009","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"663731","DOI":"10.3389\/fmicb.2021.663731","article-title":"Contribution of Different Mechanisms to Ciprofloxacin Resistance in Salmonella Spp.","volume":"12","author":"Chang","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.drup.2016.09.001","article-title":"Plasmid-Mediated Quinolone Resistance: Two Decades On","volume":"29","author":"Machuca","year":"2016","journal-title":"Drug Resist. Updat."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Acheampong, G., Owusu, M., Owusu-Ofori, A., Osei, I., Sarpong, N., Sylverken, A., Kung, H.-J., Cho, S.-T., Kuo, C.-H., and Park, S.E. (2019). Chromosomal and Plasmid-Mediated Fluoroquinolone Resistance in Human Salmonella Enterica Infection in Ghana. BMC Infect. Dis., 19.","DOI":"10.1186\/s12879-019-4522-1"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"838","DOI":"10.1111\/zph.12507","article-title":"Plasmid-Mediated Quinolone Resistance in Human Nontyphoidal Salmonella Infections: An Emerging Public Health Problem in the United States","volume":"65","author":"Karp","year":"2018","journal-title":"Zoonoses Public Health"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1605","DOI":"10.4014\/jmb.1602.02063","article-title":"Analysis of the Fluoroquinolone Antibiotic Resistance Mechanism of Salmonella Enterica Isolates","volume":"26","author":"Kim","year":"2016","journal-title":"J. Microbiol. Biotechnol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1186\/s13099-021-00431-7","article-title":"Presence of Plasmid-Mediated Quinolone Resistance (PMQR) Genes in Non-Typhoidal Salmonella Strains with Reduced Susceptibility to Fluoroquinolones Isolated from Human Salmonellosis in Gyeonggi-Do, South Korea from 2016 to 2019","volume":"13","author":"Lee","year":"2021","journal-title":"Gut Pathog."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1039\/C5MD00344J","article-title":"Mechanisms of Resistance to Aminoglycoside Antibiotics: Overview and Perspectives","volume":"7","author":"Labby","year":"2016","journal-title":"MedChemComm"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1864","DOI":"10.3389\/fmicb.2020.01864","article-title":"Frequency of Antimicrobial Resistance Genes in Salmonella from Brazil by in Silico Whole-Genome Sequencing Analysis: An Overview of the Last Four Decades","volume":"11","author":"Rodrigues","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e00966","DOI":"10.1128\/AAC.00966-21","article-title":"A One-Health Genomic Investigation of Gentamicin Resistance in Salmonella from Human and Chicken Sources in Canada, 2014 to 2017","volume":"65","author":"Cox","year":"2021","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"5649","DOI":"10.1073\/pnas.1503141112","article-title":"Global Trends in Antimicrobial Use in Food Animals","volume":"112","author":"Brower","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.ijfoodmicro.2018.07.007","article-title":"Occurrence, Antimicrobial Resistance and Whole-Genome Sequencing Analysis of Salmonella Isolates from Chicken Carcasses Imported into Iraq from Four Different Countries","volume":"284","author":"Harb","year":"2018","journal-title":"Int. J. Food Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1093\/jac\/dkh070","article-title":"Antibiotic Resistance Genes, Integrons and Multiple Antibiotic Resistance in Thirty-Five Serotypes of Salmonella Enterica Isolated from Humans and Animals in the UK","volume":"53","author":"Randall","year":"2004","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2430","DOI":"10.1128\/AAC.43.10.2430","article-title":"Propagation of TEM- and PSE-Type \u03b2-Lactamases among Amoxicillin-Resistant Salmonella Spp. Isolated in France","volume":"43","author":"Llanes","year":"1999","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.3201\/eid1809.111515","article-title":"Control of Fluoroquinolone Resistance through Successful Regulation, Australia","volume":"18","author":"Cheng","year":"2012","journal-title":"Emerg. Infect. Dis."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/12\/2\/193\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:17:24Z","timestamp":1760120244000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/12\/2\/193"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,27]]},"references-count":39,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["pathogens12020193"],"URL":"https:\/\/doi.org\/10.3390\/pathogens12020193","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,1,27]]}}}