{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,3]],"date-time":"2026-07-03T23:12:50Z","timestamp":1783120370639,"version":"3.54.6"},"reference-count":42,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2020,11,16]],"date-time":"2020-11-16T00:00:00Z","timestamp":1605484800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>This work aimed to evaluate the antimicrobial susceptibility of 87 Salmonella Infantis strains isolated in Italy from 2016 to 2019 along the food chain of broiler meat production and in humans and to determine the genetic profiles of the strains in order to establish a possible correlation with the antimicrobial pattern. All isolates were tested by the disk diffusion method to evaluate antimicrobial susceptibility toward sixteen antimicrobials, and the broth microdilution method was used to confirm extended spectrum \u03b2-lactamase (ESBL) production. PCR and pulsed field gel electrophoresis (PFGE) were applied to characterize ESBL-encoding and AmpC \u03b2-lactamase genes and to analyze the S. Infantis strains genetic profiles respectively. S. Infantis isolates showed high prevalence of resistance, in particular toward nalidixic acid (97.7%), tetracycline (96.5%), sulphamethoxazole\/trimethoprim (91%) and cefepime (72.4%). The 80.5% of isolates were ESBL, cefotaxime-resistant, carrying the blaCTX-M1 gene. The most prevalent PFGE profile was XbaI.0126 (35.6%). The remaining strains had a genetic homology from 81% to 97% with the XbaI.0126 profile. The strains belonging to these profiles were isolated from different matrices collected along the broiler food chain independently on the year and from the region and there was no correlation between the PFGE profiles and resistance patterns. We found two ESBL-producing S. Infantis strains with the same XbaI.2621 profile isolated from humans and from poultry feces, not yet reported in Italy. Our findings confirmed the diffusion of ESBL-multi drug resistant (MDR) S. Infantis along the broiler food chain and in humans and underlined the importance of continuous monitoring to control and to reduce the prevalence of this bacterium, applying a global One Health approach.<\/jats:p>","DOI":"10.3390\/antibiotics9110814","type":"journal-article","created":{"date-parts":[[2020,11,16]],"date-time":"2020-11-16T11:04:20Z","timestamp":1605524660000},"page":"814","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":27,"title":["Genetic Profiles and Antimicrobial Resistance Patterns of Salmonella Infantis Strains Isolated in Italy in the Food Chain of Broiler Meat Production"],"prefix":"10.3390","volume":"9","author":[{"given":"Patrizia Casagrande","family":"Proietti","sequence":"first","affiliation":[{"name":"Department of Veterinary Medicine, Via S. Costanzo 4, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9621-3315","authenticated-orcid":false,"given":"Valentina","family":"Stefanetti","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, Via S. Costanzo 4, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1106-2130","authenticated-orcid":false,"given":"Laura","family":"Musa","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, Via S. Costanzo 4, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alessia","family":"Zicavo","sequence":"additional","affiliation":[{"name":"Istituto Zooprofilattico Sperimentale dell\u2019Umbria e delle Marche \u201cTogo Rosati\u201d, Via G. Salvemini, 1, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna Maria","family":"Dionisi","sequence":"additional","affiliation":[{"name":"Istituto Superiore di Sanit\u00e0, Viale Regina Elena, 299, 00161 Roma, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sara","family":"Bellucci","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, Via S. Costanzo 4, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9344-2881","authenticated-orcid":false,"given":"Agnese La","family":"Mensa","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, Via S. Costanzo 4, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8500-7970","authenticated-orcid":false,"given":"Laura","family":"Menchetti","sequence":"additional","affiliation":[{"name":"Department of Agricultural and Food Sciences, Viale Fanin 42, 40127 Bologna, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4428-9016","authenticated-orcid":false,"given":"Raffaella","family":"Branciari","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, Via S. Costanzo 4, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roberta","family":"Ortenzi","sequence":"additional","affiliation":[{"name":"Istituto Zooprofilattico Sperimentale dell\u2019Umbria e delle Marche \u201cTogo Rosati\u201d, Via G. Salvemini, 1, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria Pia","family":"Franciosini","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, Via S. Costanzo 4, 06126 Perugia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,11,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"EFSA (2019). The European Union One Health 2018 zoonoses report. EFSA J., 17, e05926.","DOI":"10.2903\/j.efsa.2019.5926"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1016\/j.cmi.2015.12.004","article-title":"Salmonellosis: The role of poultry meat","volume":"22","author":"Antunes","year":"2016","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_3","unstructured":"European Food Safety Authority (EFSA), and European Centre for Disease Prevention and Control (ECDC) (2018). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J., Available online: https:\/\/www.ecdc.europa.eu\/sites\/portal\/files\/documents\/zoonoese-food-borne-outbreaks-surveillance-2017-updated.pdf."},{"key":"ref_4","first-page":"e000365","article-title":"Molecular epidemiology of salmonella infantis in europe: Insights into the success of the bacterial host and its parasitic pesi-like megaplasmid","volume":"6","author":"Alba","year":"2020","journal-title":"Microb. Genom."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Authority, E.F. (2018). The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2016. EFSA J., 16.","DOI":"10.2903\/j.efsa.2018.5182"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2767","DOI":"10.1128\/JCM.01916-05","article-title":"Clonality and antimicrobial resistance gene profiles of multidrug-resistant Salmonella enterica serovar infantis isolates from four public hospitals in Rio de Janeiro, Brazil","volume":"44","author":"Fonseca","year":"2006","journal-title":"J. Clin. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.3201\/eid1611.100100","article-title":"Multidrug resistant salmonella enterica serovar infantis, Israel","volume":"16","author":"Valinsky","year":"2010","journal-title":"Emerg. Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Hindermann, D., Gopinath, G., Chase, H., Negrete, F., Althaus, D., Zurfluh, K., Tall, B.D., Stephan, R., and N\u00fcesch-Inderbinen, M. (2017). Salmonella enterica serovar infantis from food and human infections, Switzerland, 2010\u20132015: Poultry-related multidrug resistant clones and an emerging ESBL producing clonal lineage. Front. Microbiol., 8.","DOI":"10.3389\/fmicb.2017.01322"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Pate, M., Mi\u010dunovi\u010d, J., Golob, M., Vestby, L.K., and Ocepek, M. (2019). Salmonella Infantis in Broiler Flocks in Slovenia: The Prevalence of Multidrug Resistant Strains with High Genetic Homogeneity and Low Biofilm-Forming Ability. Biomed. Res. Int., 2019.","DOI":"10.1155\/2019\/4981463"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.ijfoodmicro.2012.04.007","article-title":"Multidrug resistant clones of Salmonella Infantis of broiler origin in Europe","volume":"157","author":"Davies","year":"2012","journal-title":"Int. J. Food Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1741","DOI":"10.3389\/fmicb.2020.01741","article-title":"Emergence of Multidrug-Resistant Salmonella enterica Subspecies enterica Serovar Infantis of Multilocus Sequence Type 2283 in German Broiler Farms","volume":"11","author":"Tomaso","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Franco, A., Leekitcharoenphon, P., Feltrin, F., Alba, P., Cordaro, G., Iurescia, M., Tolli, R., D\u2019Incau, M., Staffolani, M., and Di Giannatale, E. (2015). Emergence of a Clonal Lineage of Multidrug-Resistant ESBL-Producing Salmonella Infantis Transmitted from Broilers and Broiler Meat to Humans in Italy between 2011 and 2014. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0144802"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1016\/j.ijantimicag.2011.07.001","article-title":"Molecular characterisation of multidrug-resistant Salmonella enterica serotype Infantis from humans, animals and the environment in Italy","volume":"38","author":"Dionisi","year":"2011","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"490","DOI":"10.3201\/eid0805.010267","article-title":"Excess mortality associated with antimicrobial drug-resistant Salmonella typhimurium","volume":"8","author":"Helms","year":"2002","journal-title":"Emerg. Infect. Dis."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"EFSA, and ECDC (2015). The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-Borne Outbreaks in 2014. EFSA J., 13, 4329.","DOI":"10.2903\/j.efsa.2015.4329"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1087","DOI":"10.1093\/cid\/ciw475","article-title":"World Health Organization Ranking of Antimicrobials According to Their Importance in Human Medicine: A Critical Step for Developing Risk Management Strategies to Control Antimicrobial Resistance from Food Animal Production","volume":"Volume 63","author":"Collignon","year":"2016","journal-title":"Proceedings of the Clinical Infectious Diseases"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1111\/1462-2920.12351","article-title":"A unique megaplasmid contributes to stress tolerance and pathogenicity of an emergent Salmonella enterica serovar Infantis strain","volume":"16","author":"Aviv","year":"2014","journal-title":"Environ. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Carfora, V., Alba, P., Leekitcharoenphon, P., Ballar\u00f2, D., Cordaro, G., Di Matteo, P., Donati, V., Ianzano, A., Iurescia, M., and Stravino, F. (2018). Colistin resistance mediated by mcr-1 in ESBL-producing, multidrug resistant Salmonella infantis in broiler chicken industry, Italy (2016\u20132017). Front. Microbiol., 9.","DOI":"10.3389\/fmicb.2018.02395"},{"key":"ref_19","first-page":"e05596","article-title":"Salmonella control in poultry flocks and its public health impact","volume":"17","author":"Koutsoumanis","year":"2019","journal-title":"EFSA J."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Musa, L., Casagrande Proietti, P., Branciari, R., Menchetti, L., Bellucci, S., Ranucci, D., Marenzoni, M.L., and Franciosini, M.P. (2020). Antimicrobial Susceptibility of Escherichia coli and ESBL-Producing Escherichia coli Diffusion in Conventional, Organic and Antibiotic-Free Meat Chickens at Slaughter. Animals, 10.","DOI":"10.3390\/ani10071215"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Newton, K., Gosling, B., Rabie, A., and Davies, R. (2020). Field investigations of multidrug resistant Salmonella Infantis epidemic strain incursions into broiler flocks in England and Wales. Avian Pathol., 1\u201328.","DOI":"10.1080\/03079457.2020.1809634"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1080\/10408410591005110","article-title":"Use of antimicrobial agents in veterinary medicine and implications for human health","volume":"31","author":"Wassenaar","year":"2005","journal-title":"Crit. Rev. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"538","DOI":"10.3389\/fmicb.2018.00538","article-title":"Retrospective analysis of bacterial cultures sampled in German chicken-fattening farms during the years 2011-2012 revealed additional VIM-1 carbapenemase-producing Escherichia coli and a serologically rough Salmonella enterica serovar infantis","volume":"9","author":"Roschanski","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1177","DOI":"10.1007\/s11274-006-9159-8","article-title":"Antibiotic resistance and molecular characterization of poultry isolates of Salmonella by RAPD-PCR","volume":"22","author":"Thakur","year":"2006","journal-title":"World J. Microbiol. Biotechnol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1387","DOI":"10.1016\/j.scitotenv.2017.09.012","article-title":"Towards the understanding of antibiotic occurrence and transport in groundwater: Findings from the Baix Fluvi\u00e0 alluvial aquifer (NE Catalonia, Spain)","volume":"612","author":"Petrovic","year":"2018","journal-title":"Sci. Total Environ."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1016\/j.mib.2010.08.005","article-title":"Antibiotic resistance in the environment: A link to the clinic?","volume":"13","author":"Wright","year":"2010","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_27","first-page":"7956","article-title":"Carbapenemase-producing bacteria in food-producing animals, wildlife and environment: A challenge for human health","volume":"8","author":"Bonardi","year":"2019","journal-title":"Ital. J. Food Saf."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"910","DOI":"10.3389\/fmicb.2020.00910","article-title":"Fourth Generation Cephalosporin Resistance Among Salmonella enterica Serovar Enteritidis Isolates in Shanghai, China Conferred by blaCTX\u2013M\u201355 Harboring Plasmids","volume":"11","author":"Fu","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_29","unstructured":"European Medicine Agency (2020, October 19). Available online: https:\/\/www.ema.europa.eu\/en\/documents\/press-release\/categorisation-antibiotics-used-animals-promotes-responsible-use-protect-public-animal-health_en.pdf."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1016\/j.drup.2012.03.005","article-title":"Evolution of antibiotic resistance at non-lethal drug concentrations","volume":"15","author":"Andersson","year":"2012","journal-title":"Drug Resist. Updates"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/j.ijantimicag.2016.06.025","article-title":"Extended-spectrum \u03b2-lactamase-producing Salmonella enterica serovar Infantis from humans in Italy","volume":"48","author":"Dionisi","year":"2016","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_32","unstructured":"ISO (2020, September 17). ISO 6579-1:2017\/Amd 1:2020\u2014Microbiology of the Food Chain\u2014Horizontal Method for the Detection, Enumeration and Serotyping of Salmonella\u2014Part 1: Detection of Salmonella spp.\u2014Amendment 1: Broader Range of Incubation Temperatures, Amendment to the Status of Annex D, and Correction of the Composition of MSRV and SC. Available online: https:\/\/www.iso.org\/standard\/76671.html."},{"key":"ref_33","unstructured":"Grimont, P.A.D., and Weill, F.-X. (2007). Antigenic Formulae of the Salmonella Serovars, WHO Collaborating Center for Reference and Research on Salmonella, Institut Pasteur. [9th ed.]. Available online: http:\/\/www.scacm.org\/free\/Antigenic%20Formulae%20of%20the%20Salmonella%20Serovars%202007%209th%20edition.pdf."},{"key":"ref_34","unstructured":"Clinical and Laboratory Standards Institute (CLSI) (2020). Performance Standards for Antimicrobial Susceptibility Testing, CLSI. [30th ed.]. CLSI Supplement M100."},{"key":"ref_35","unstructured":"(2020, October 02). European Committee on Antimicrobial Susceptibility Testing. Available online: https:\/\/www.eucast.org\/fileadmin\/src\/media\/PDFs\/EUCAST_files\/Breakpoint_tables\/v_10.0_Breakpoint_Tables.pdf."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1111\/j.1469-0691.2011.03570.x","article-title":"Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance","volume":"18","author":"Magiorakos","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1093\/jac\/dki412","article-title":"Multiplex PCR for rapid detection of genes encoding CTX-M extended-spectrum \u03b2-lactamases [4]","volume":"57","author":"Woodford","year":"2006","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1235","DOI":"10.1089\/fpd.2009.0294","article-title":"Genetic and phenotypic characterization of the blaCMY gene from escherichia coli and salmonella enterica isolated from food-producing animals, humans, the environment, and retail meat","volume":"6","author":"Heider","year":"2009","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1089\/fpd.2006.3.59","article-title":"Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet","volume":"3","author":"Ribot","year":"2006","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"792","DOI":"10.1080\/1828051X.2020.1799724","article-title":"Comparison of nonlinear growth models and factors affecting body weight at different ages in Toy Poodles","volume":"19","author":"Menchetti","year":"2020","journal-title":"Ital. J. Anim. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1503","DOI":"10.1016\/0895-4356(95)00048-8","article-title":"Importance of events per independent variable in proportional hazards regression analysis II. Accuracy and precision of regression estimates","volume":"48","author":"Peduzzi","year":"1995","journal-title":"J. Clin. Epidemiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1167","DOI":"10.1016\/j.theriogenology.2010.01.003","article-title":"Method agreement analysis: A review of correct methodology","volume":"73","author":"Watson","year":"2010","journal-title":"Theriogenology"}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/9\/11\/814\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:33:50Z","timestamp":1760178830000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/9\/11\/814"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,11,16]]},"references-count":42,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2020,11]]}},"alternative-id":["antibiotics9110814"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics9110814","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,11,16]]}}}