{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,30]],"date-time":"2026-04-30T11:48:22Z","timestamp":1777549702897,"version":"3.51.4"},"reference-count":52,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2021,8,13]],"date-time":"2021-08-13T00:00:00Z","timestamp":1628812800000},"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>Salmonella enterica serovar Schwarzengrund is one of the most frequently isolated Salmonella serotypes responsible for human and poultry infections in Taiwan, and it has raised public health concerns. To better facilitate the understanding of transmission patterns and the dynamics of epidemics, sharing molecular data on pathogen profiles is urgently needed. The objectives of the current study were to determine and establish baseline data of S. enterica serovar Schwarzengrund isolates from 23 epidemiologically unrelated sources from year 2000 to 2018 and examine their phenotypic and genotypic characteristics. Genomic DNA of the Salmonella isolates was extracted and subjected to whole-genome sequencing using an Illumina platform. Results showed that all selected isolates exhibited multidrug resistance, and six of those were resistant to ciprofloxacin phenotypically. Genotypically, these isolates carried genes resistant to aminoglycoside (100%), phenicol (91.3%), \u03b2-lactams (69.5%), folate pathway antagonist (100%), tetracycline (82.6%), and fluoroquinolone (4.3%). Moreover, these isolates harbor integrons with five different gene cassettes identified for the first time, which are associated with resistance to trimethoprim, streptomycin, tetracycline, sulfonamide, chloramphenicol, and gentamicin. Furthermore, prevalence of IncFIB plasmid was found among studied isolates, which may increase its ability to colonize the chicken cecum and cause extra-intestinal disease. Salmonella pathogenicity islands SPI-1 to SPI-5, SPI-13, and SPI-14, as well as C63PI locus, were also detected in all isolates. This study demonstrated that a considerable high antimicrobial resistance with high virulence levels of Salmonella were found from animal sources. Sharing data on these pathogen profiles can not only help increase the reproducibility and accessibility of genomic analysis but can also support surveillance and epidemiological investigations for salmonellosis in the region.<\/jats:p>","DOI":"10.3390\/pathogens10081024","type":"journal-article","created":{"date-parts":[[2021,8,13]],"date-time":"2021-08-13T09:22:38Z","timestamp":1628846558000},"page":"1024","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Prevalence of IncFIB Plasmids Found among Salmonella enterica Serovar Schwarzengrund Isolates from Animal Sources in Taiwan Using Whole-Genome Sequencing"],"prefix":"10.3390","volume":"10","author":[{"given":"I-Chen","family":"Li","sequence":"first","affiliation":[{"name":"Zoonoses Research Center, School of Veterinary Medicine, National Taiwan University, No. 1, Sec. 4, Roosevelt Road, Taipei City 106, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hsiu-Hui","family":"Wu","sequence":"additional","affiliation":[{"name":"Animal Technology Research Center, Agricultural Technology Research Institute, No. 52, Kedong 2nd Road, Zhunan Township, Miaoli County 350, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zeng-Weng","family":"Chen","sequence":"additional","affiliation":[{"name":"Animal Technology Research Center, Agricultural Technology Research Institute, No. 52, Kedong 2nd Road, Zhunan Township, Miaoli County 350, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chung-Hsi","family":"Chou","sequence":"additional","affiliation":[{"name":"Zoonoses Research Center, School of Veterinary Medicine, National Taiwan University, No. 1, Sec. 4, Roosevelt Road, Taipei City 106, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,8,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1073\/pnas.1814484116","article-title":"Analysis of research intensity on infectious disease by disease burden reveals which infectious diseases are neglected by researchers","volume":"116","author":"Furuse","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1260","DOI":"10.1016\/S0140-6736(17)32130-X","article-title":"Global, regional, and national disability-adjusted life-years (DALYs) for 333 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990\u20132016: A systematic analysis for the Global Burden of Disease Study 2016","volume":"390","author":"Hay","year":"2017","journal-title":"Lancet"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2209","DOI":"10.1128\/JCM.37.7.2209-2214.1999","article-title":"Molecular subtyping of Clostridium perfringens by pulsed-field gel electrophoresis to facilitate food-borne-disease outbreak investigations","volume":"37","author":"Maslanka","year":"1999","journal-title":"J. Clin. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3201\/eid1901.120393","article-title":"Listeriosis outbreaks and associated food vehicles, United States, 1998\u20132008","volume":"19","author":"Cartwright","year":"2013","journal-title":"Emerg. Infect. Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"654","DOI":"10.4315\/0362-028X.JFP-16-364","article-title":"Utility of Combining Whole Genome Sequencing with Traditional Investigational Methods To Solve Foodborne Outbreaks of Salmonella Infections Associated with Chicken: A New Tool for Tackling This Challenging Food Vehicle","volume":"80","author":"Crowe","year":"2017","journal-title":"J. Food Prot."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"258","DOI":"10.3389\/fmicb.2016.00258","article-title":"Whole Genome Sequencing for Public Health Surveillance of Shiga Toxin-Producing Escherichia coli Other than Serogroup O157","volume":"7","author":"Chattaway","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1038\/nrg3226","article-title":"Transforming clinical microbiology with bacterial genome sequencing","volume":"13","author":"Didelot","year":"2012","journal-title":"Nat. Rev. Genet."},{"key":"ref_8","first-page":"38","article-title":"Pulsed-Field Gel Electrophoresis (PFGE): Principles and Applications in Molecular Epidemiology: A Review","volume":"2","author":"Nsofor","year":"2016","journal-title":"Int. J. Curr. Res."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"380","DOI":"10.1093\/cid\/ciw242","article-title":"Implementation of Nationwide Real-time Whole-genome Sequencing to Enhance Listeriosis Outbreak Detection and Investigation","volume":"63","author":"Jackson","year":"2016","journal-title":"Clin. Infect. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e00594-00517","DOI":"10.1128\/genomeA.00594-17","article-title":"100K Pathogen Genome Project","volume":"5","author":"Weimer","year":"2017","journal-title":"Genome Announc."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1001\/jama.2018.21669","article-title":"Next-Generation Sequencing of Infectious Pathogens","volume":"321","author":"Gwinn","year":"2019","journal-title":"JAMA"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"D19","DOI":"10.1093\/nar\/gkq1019","article-title":"The sequence read archive","volume":"39","author":"Leinonen","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"S149","DOI":"10.1086\/381581","article-title":"Invasive Salmonella infections in the United States, FoodNet, 1996\u20131999: Incidence, serotype distribution, and outcome","volume":"38","author":"Vugia","year":"2004","journal-title":"Clin. Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"359","DOI":"10.3382\/ps.2009-00001","article-title":"Contamination of Salmonella Schwarzengrund cells in chicken meat from traditional marketplaces in Taiwan and comparison of their antibiograms with those of the human isolates","volume":"89","author":"Chen","year":"2010","journal-title":"Poult. Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1292\/jvms.20-0096","article-title":"Increased Salmonella Schwarzengrund prevalence and antimicrobial susceptibility of Salmonella enterica isolated from broiler chickens in Kagoshima Prefecture in Japan between 2013 and 2016","volume":"82","author":"Duc","year":"2020","journal-title":"J. Vet. Med. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"726","DOI":"10.3201\/eid1305.061489","article-title":"International spread of multidrug-resistant Salmonella Schwarzengrund in food products","volume":"13","author":"Aarestrup","year":"2007","journal-title":"Emerg. Infect. Dis."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Emond-Rheault, J.-G., Hamel, J., Jeukens, J., Freschi, L., Kukavica-Ibrulj, I., Boyle, B., Tamber, S., Malo, D., Franz, E., and Burnett, E. (2020). The Salmonella enterica Plasmidome as a Reservoir of Antibiotic Resistance. Microorganisms, 8.","DOI":"10.3390\/microorganisms8071016"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"242","DOI":"10.3389\/fpubh.2019.00242","article-title":"Using Genomics to Track Global Antimicrobial Resistance","volume":"7","author":"Hendriksen","year":"2019","journal-title":"Front. Public Health"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e01687-18","DOI":"10.1128\/MRA.01687-18","article-title":"Draft Genome Sequences of 27 Salmonella enterica Serovar Schwarzengrund Isolates from Clinical Sources","volume":"8","author":"Khajanchi","year":"2019","journal-title":"Microbiol. Resour. Announc."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2582","DOI":"10.1128\/JCM.00535-13","article-title":"Minimum Core Genome Sequence Typing of Bacterial Pathogens: A Unified Approach for Clinical and Public Health Microbiology","volume":"51","author":"Chen","year":"2013","journal-title":"J. Clin. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1186\/1471-2164-15-737","article-title":"Characterization of the core and accessory genomes of Pseudomonas aeruginosa using bioinformatic tools Spine and AGEnt","volume":"15","author":"Ozer","year":"2014","journal-title":"BMC Genom."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1128\/CMR.00059-12","article-title":"Antimicrobial resistance and virulence: A successful or deleterious association in the bacterial world?","volume":"26","author":"Beceiro","year":"2013","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2182","DOI":"10.1128\/IAI.01277-10","article-title":"Discovery of Salmonella virulence factors translocated via outer membrane vesicles to murine macrophages","volume":"79","author":"Yoon","year":"2011","journal-title":"Infect. Immun."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"S106","DOI":"10.1093\/clinids\/24.Supplement_1.S106","article-title":"Multidrug-resistant Salmonella typhi: A worldwide epidemic","volume":"24","author":"Rowe","year":"1997","journal-title":"Clin. Infect. Dis."},{"key":"ref_25","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_26","doi-asserted-by":"crossref","first-page":"5117","DOI":"10.1038\/s41598-019-41528-z","article-title":"Analysis of fluoroquinolones in dusts from intensive livestock farming and the co-occurrence of fluoroquinolone-resistant Escherichia coli","volume":"9","author":"Schulz","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1565","DOI":"10.1021\/bi5000564","article-title":"Mechanism of Quinolone Action and Resistance","volume":"53","author":"Aldred","year":"2014","journal-title":"Biochemistry"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"718084","DOI":"10.1155\/2014\/718084","article-title":"High Resolution Melting Analysis for Rapid Mutation Screening in Gyrase and Topoisomerase IV Genes in Quinolone-Resistant Salmonella enterica","volume":"2014","author":"Ngoi","year":"2014","journal-title":"BioMed Res. Int."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"e01985-19","DOI":"10.1128\/AEM.01985-19","article-title":"Implications of Mobile Genetic Elements for Salmonella enterica Single-Nucleotide Polymorphism Subtyping and Source Tracking Investigations","volume":"85","author":"Li","year":"2019","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Mutai, W.C., Waiyaki, P.G., Kariuki, S., and Muigai, A.W.T. (2019). Plasmid profiling and incompatibility grouping of multidrug resistant Salmonella enterica serovar Typhi isolates in Nairobi, Kenya. BMC Res. Notes, 12.","DOI":"10.1186\/s13104-019-4468-9"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Johnson, T.J., Thorsness, J.L., Anderson, C.P., Lynne, A.M., Foley, S.L., Han, J., Fricke, W.F., McDermott, P.F., White, D.G., and Khatri, M. (2010). Horizontal gene transfer of a ColV plasmid has resulted in a dominant avian clonal type of Salmonella enterica serovar Kentucky. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0015524"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1016\/j.ijmm.2013.02.001","article-title":"Plasmids and the spread of resistance","volume":"303","author":"Carattoli","year":"2013","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.plasmid.2016.11.005","article-title":"A novel group of IncQ1 plasmids conferring multidrug resistance","volume":"89","author":"Oliva","year":"2017","journal-title":"Plasmid"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Oladeinde, A., Cook, K., Orlek, A., Zock, G., Herrington, K., Cox, N., Plumblee Lawrence, J., and Hall, C. (2018). Hotspot mutations and ColE1 plasmids contribute to the fitness of Salmonella Heidelberg in poultry litter. PLoS ONE, 13.","DOI":"10.1101\/312322"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.actatropica.2007.05.018","article-title":"Class 1 integrons and resistance gene cassettes among multidrug resistant Salmonella serovars isolated from slaughter animals and foods of animal origin in Ethiopia","volume":"103","author":"Molla","year":"2007","journal-title":"Acta Trop."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"4539","DOI":"10.1093\/nar\/gkw319","article-title":"Identification and analysis of integrons and cassette arrays in bacterial genomes","volume":"44","author":"Cury","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"388","DOI":"10.3201\/eid1503.081131","article-title":"Integron-mediated multidrug resistance in a global collection of nontyphoidal Salmonella enterica isolates","volume":"15","author":"Krauland","year":"2009","journal-title":"Emerg. Infect. Dis."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Hayward, M.R., AbuOun, M., La Ragione, R.M., Tch\u00f3rzewska, M.A., Cooley, W.A., Everest, D.J., Petrovska, L., Jansen, V.A., and Woodward, M.J. (2014). SPI-23 of S. Derby: Role in adherence and invasion of porcine tissues. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0107857"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"270","DOI":"10.3389\/fcimb.2019.00270","article-title":"Salmonella Pathogenicity Island 1 (SPI-1) and Its Complex Regulatory Network","volume":"9","author":"Lou","year":"2019","journal-title":"Front. Cell Infect. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1046\/j.1365-2958.2002.02820.x","article-title":"Salmonella effectors within a single pathogenicity island are differentially expressed and translocated by separate type III secretion systems","volume":"43","author":"Knodler","year":"2002","journal-title":"Mol. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Jiang, L., Feng, L., Yang, B., Zhang, W., Wang, P., Jiang, X., and Wang, L. (2017). Signal transduction pathway mediated by the novel regulator LoiA for low oxygen tension induced Salmonella Typhimurium invasion. PLoS Pathog., 13.","DOI":"10.1371\/journal.ppat.1006429"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1835","DOI":"10.1099\/00221287-144-7-1835","article-title":"Magnesium transport in Salmonella typhimurium: Regulation of mgtA and mgtCB during invasion of epithelial and macrophage cells","volume":"144","author":"Smith","year":"1998","journal-title":"Microbiology"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1111\/j.1365-2958.2005.04666.x","article-title":"Salmonella enterica serotype Typhimurium MisL is an intestinal colonization factor that binds fibronectin","volume":"57","author":"Dorsey","year":"2005","journal-title":"Mol. Microbiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"994","DOI":"10.1111\/j.1365-2958.2004.04323.x","article-title":"Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium","volume":"54","author":"Morgan","year":"2004","journal-title":"Mol. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1367","DOI":"10.1099\/mic.0.000319","article-title":"SPI-9 of Salmonella enterica serovar Typhi is constituted by an operon positively regulated by RpoS and contributes to adherence to epithelial cells in culture","volume":"162","author":"Hidalgo","year":"2016","journal-title":"Microbiology"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"29131","DOI":"10.1074\/jbc.M604640200","article-title":"Proteomic Analysis of Salmonella enterica Serovar Typhimurium Isolated from RAW 264.7 Macrophages","volume":"281","author":"Shi","year":"2006","journal-title":"J. Biol. Chem."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1186\/1297-9716-42-34","article-title":"Animal contact as a source of human non-typhoidal salmonellosis","volume":"42","author":"Hoelzer","year":"2011","journal-title":"Vet. Res."},{"key":"ref_48","unstructured":"Grimont, P.A., and Weill, F.X. (2007). Antigenic Formulae of the Salmonella serovars, WHO Collaborating Centre for Reference and Research on Salmonella Institut Pasteur. [9th ed.]."},{"key":"ref_49","unstructured":"CLSI (2016). Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"e102","DOI":"10.1002\/cpbi.102","article-title":"Using SPAdes De Novo Assembler","volume":"70","author":"Prjibelski","year":"2020","journal-title":"Curr. Protoc. Bioinform"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2443","DOI":"10.1093\/bioinformatics\/btv171","article-title":"MeDuSa: A multi-draft based scaffolder","volume":"31","author":"Bosi","year":"2015","journal-title":"Bioinformatics"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/8\/1024\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:45:26Z","timestamp":1760165126000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/8\/1024"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,8,13]]},"references-count":52,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2021,8]]}},"alternative-id":["pathogens10081024"],"URL":"https:\/\/doi.org\/10.3390\/pathogens10081024","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,8,13]]}}}