{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,12]],"date-time":"2026-10-12T19:11:59Z","timestamp":1791832319970,"version":"4.3.4"},"reference-count":33,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2019,9,23]],"date-time":"2019-09-23T00:00:00Z","timestamp":1569196800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biomolecules"],"abstract":"<jats:p>The prevalence of Staphylococcus aureus in 2160 bulk ready-to-eat foods from the Sichuan province of China during 2013\u20132016 was investigated. The antibiotic resistance and the associated genes, as well as biofilm formation capacity of the S. aureus isolates were measured. Furthermore, the relationship between the antibiotic resistance and the resistant genes was discussed. It was found that 54 S. aureus isolates were recovered, and their prevalence in meat products, dairy, fruit and vegetables, and desserts were 31 (2.6%), six (3.0%), nine (2.2%) and eight (2.3%), respectively. Most strains (52\/54) were resistant to at least one of the antibiotics, and 21 isolates were identified as multidrug-resistant (MDR) S. aureus. Three isolates were found to be methicillin-resistant S. aureus. Penicillin, erythromycin, clindamycin, tetracycline and inducible clindamycin resistance were determined as the predominant antibiotics, and the isolates with the phenotypic resistance on these five antibiotics were all determined positive for the resistant gene associated. In total, 33 of 54 S. aureus isolates showed biofilm formation capacity, including two strong biofilm producers, one moderate and 30 weak ones. Two S. aureus isolates with strong biofilm formation abilities showed multi-drug resistance, and one moderate biofilm producer was resistant to two categories of antibiotics.<\/jats:p>","DOI":"10.3390\/biom9100524","type":"journal-article","created":{"date-parts":[[2019,9,23]],"date-time":"2019-09-23T11:02:00Z","timestamp":1569236520000},"page":"524","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":38,"title":["The Prevalence, Antibiotic Resistance and Biofilm Formation of Staphylococcus aureus in Bulk Ready-To-Eat Foods"],"prefix":"10.3390","volume":"9","author":[{"given":"Qi","family":"Lin","sequence":"first","affiliation":[{"name":"College of Biomass Science and Engineering, and Healthy Food Evaluation Research Center, Sichuan University, Chengdu 610065, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Honghu","family":"Sun","sequence":"additional","affiliation":[{"name":"Chengdu Institute for Food and Drug Control, Chengdu 610045, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kai","family":"Yao","sequence":"additional","affiliation":[{"name":"College of Biomass Science and Engineering, and Healthy Food Evaluation Research Center, Sichuan University, Chengdu 610065, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiong","family":"Cai","sequence":"additional","affiliation":[{"name":"Chengdu Institute for Food and Drug Control, Chengdu 610045, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yao","family":"Ren","sequence":"additional","affiliation":[{"name":"College of Biomass Science and Engineering, and Healthy Food Evaluation Research Center, Sichuan University, Chengdu 610065, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1687-9016","authenticated-orcid":false,"given":"Yuanlong","family":"Chi","sequence":"additional","affiliation":[{"name":"College of Biomass Science and Engineering, and Healthy Food Evaluation Research Center, Sichuan University, Chengdu 610065, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,9,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.foodcont.2018.03.027","article-title":"Microbial contamination in bulk ready-to-eat meat products of China in 2016","volume":"91","author":"Yang","year":"2018","journal-title":"Food Control."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Abdolshahi, A., Naybandi-Atashi, S., Heydari-Majd, M., Salehi, B., Kobarfard, F., Ayatollahi, S.A., Ata, A., Tabanelli, G., Sharifi-Rad, M., and Montanari, C. (2018). Antibacterial activity of some Lamiaceae species against Staphylococcus aureus in yoghurt-based drink (Doogh). Cell. Mol. Biol., 64.","DOI":"10.14715\/cmb\/2018.64.8.11"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1751","DOI":"10.3390\/toxins2071751","article-title":"Food poisoning and Staphylococcus aureus enterotoxins","volume":"2","author":"Argudin","year":"2010","journal-title":"Toxins"},{"key":"ref_4","first-page":"570","article-title":"Genotypic Characterization of Methicillin-resistant Staphylococcus aureus Isolated from Pigs and Retail Foods in China","volume":"30","author":"Wang","year":"2017","journal-title":"Biomed. Environ. Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/j.fm.2013.01.005","article-title":"Microbiological examination of ready-to-eat foods and ready-to-bake frozen pastries from university canteens","volume":"34","author":"Kotzekidou","year":"2013","journal-title":"Food Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1089\/fpd.2014.1850","article-title":"Staphylococcus aureus ST6-t701 isolates from food-poisoning outbreaks (2006\u20132013) in Xi\u2019an, China","volume":"12","author":"Li","year":"2015","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"85","DOI":"10.4014\/jmb.1210.10022","article-title":"A Foodborne Outbreak of Staphylococcus aureus Associated with Fried Chicken in Republic of Korea","volume":"23","author":"Hyeon","year":"2013","journal-title":"J. Microbiol. Biotechnol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"6637","DOI":"10.1128\/AEM.01165-12","article-title":"Characterization of Staphylococcus aureus strains associated with food poisoning in Shenzhen, China","volume":"78","author":"Yan","year":"2012","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1006\/mcpr.2001.0363","article-title":"Multiplex PCR for the detection of tetracycline resistant genes","volume":"15","author":"Ng","year":"2001","journal-title":"Mol. Cell. Probes"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"350","DOI":"10.3855\/jidc.8316","article-title":"Prevalence of inducible clindamycin resistance in methicillin-resistant Staphylococcus aureus: The first study in Jordan","volume":"11","author":"Jarajreh","year":"2017","journal-title":"J. Infect. Dev. Ctries"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1016\/j.jiph.2016.08.007","article-title":"Antibiotic resistance","volume":"10","author":"Frieri","year":"2017","journal-title":"J. Infect. Public Health"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.ddtec.2014.02.003","article-title":"Biofilms as a mechanism of bacterial resistance","volume":"11","year":"2014","journal-title":"Drug Discov. Today Technol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3407","DOI":"10.1128\/AAC.47.11.3407-3414.2003","article-title":"Lysostaphin Disrupts Staphylococcus aureus and Staphylococcus epidermidis Biofilms on Artificial Surfaces","volume":"47","author":"Wu","year":"2003","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"737","DOI":"10.5301\/ijao.5000027","article-title":"Antibiotic-induced biofilm formation","volume":"34","author":"Kaplan","year":"2011","journal-title":"Int. J. Artif. Organs"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.foodcont.2012.06.002","article-title":"Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in retail raw chicken in China","volume":"29","author":"Wang","year":"2013","journal-title":"Food Control."},{"key":"ref_16","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_17","doi-asserted-by":"crossref","first-page":"3437","DOI":"10.1128\/AAC.00317-09","article-title":"Inoculum effect with cefazolin among clinical isolates of methicillin-susceptible Staphylococcus aureus: Frequency and possible cause of cefazolin treatment failure","volume":"53","author":"Nannini","year":"2009","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1128\/AAC.44.2.231-238.2000","article-title":"Correlation between the Resistance Genotype Determined by Multiplex PCR Assays and the Antibiotic Susceptibility Patterns of Staphylococcus aureus and Staphylococcus epidermidis","volume":"44","author":"Martineau","year":"2000","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.1128\/AAC.43.5.1062","article-title":"Distribution of Genes Encoding Resistance to Macrolides, Lincosamides, and Streptogramins among Staphylococci","volume":"43","author":"Lina","year":"1999","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.ijfoodmicro.2010.02.005","article-title":"Differences in attachment of Salmonella enterica serovars to cabbage and lettuce leaves","volume":"139","author":"Patel","year":"2010","journal-title":"Int. J. Food Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.fm.2012.03.012","article-title":"Influence of serotype on the growth kinetics and the ability to form biofilms of Salmonella isolates from poultry","volume":"31","author":"Capita","year":"2012","journal-title":"Food Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1450","DOI":"10.4315\/0362-028X.JFP-18-035","article-title":"Prevalence and Antimicrobial Susceptibility of Bacterial Pathogens in Ready-to-Eat Foods Retailed in Osaka Prefecture, Japan","volume":"81","author":"Harada","year":"2018","journal-title":"J. Food Prot."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1456","DOI":"10.1111\/j.1365-2672.2011.05168.x","article-title":"Prevalence and classification of toxigenic Staphylococcus aureus isolated from refrigerated ready-to-eat foods (sushi, kimbab and California rolls) in Korea","volume":"111","author":"Kim","year":"2011","journal-title":"J. Appl. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1038","DOI":"10.1016\/j.trac.2010.06.004","article-title":"Fast screening methods to detect antibiotic residues in food samples","volume":"29","author":"Maquieira","year":"2010","journal-title":"TrAC Trends in Anal. Chem."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Cheatham, S., Thapaliya, D., Taha, M., Milliken, K., Dalman, M.R., Kadariya, J., Grenier, D., and Smith, T.C. (2019). Prevalence of Staphylococcus aureus and methicillin-resistant S. aureus on environmental surfaces in Ohio nursing homes. Am. J. Infect. Control.","DOI":"10.1016\/j.ajic.2019.05.021"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/j.foodcont.2018.08.030","article-title":"Prevalence and characterization of Staphylococcus aureus and Staphylococcus argenteus in chicken from retail markets in China","volume":"96","author":"Li","year":"2019","journal-title":"Food Control."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Xing, X., Li, G., Zhang, W., Wang, X., Xia, X., Yang, B., and Meng, J. (2014). Prevalence, Antimicrobial Susceptibility, and Enterotoxin Gene Detection of Staphylococcus aureus Isolates in Ready-to-Eat Foods in Shaanxi, People\u2019s Republic of China. J. Food Prot., 77.","DOI":"10.4315\/0362-028X.JFP-13-301"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.jgar.2018.10.005","article-title":"Prevalence, multidrug resistance and molecular typing of methicillin-resistant Staphylococcus aureus (MRSA) in retail meat from Punjab, India","volume":"16","author":"Zehra","year":"2019","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1007\/s12088-012-0296-5","article-title":"Acquired resistance to macrolide-lincosamide-streptogramin antibiotics in lactic Acid bacteria of food origin","volume":"52","author":"Thumu","year":"2012","journal-title":"Indian J. Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2613","DOI":"10.1128\/JCM.43.6.2613-2615.2005","article-title":"Selection of strains for quality assessment of the disk induction method for detection of inducible clindamycin resistance in Staphylococci: A CLSI collaborative study","volume":"43","author":"Zelazny","year":"2005","journal-title":"J. Clin. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/j.fm.2016.04.001","article-title":"Staphylococcus aureus isolated from handmade sweets: Biofilm formation, enterotoxigenicity and antimicrobial resistance","volume":"58","author":"Kroning","year":"2016","journal-title":"Food Microbiol."},{"key":"ref_32","first-page":"400","article-title":"Association between biofilm production, adhesion genes and drugs resistance in different SCCmec types of methicillin resistant Staphylococcus aureus strains isolated from several major hospitals of Iran","volume":"21","author":"Bimanand","year":"2018","journal-title":"Iran J. Basic Med. Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"8607","DOI":"10.3168\/jds.2016-11310","article-title":"Investigation of the antibiotic resistance and biofilm-forming ability of Staphylococcus aureus from subclinical bovine mastitis cases","volume":"99","author":"Aslantas","year":"2016","journal-title":"J. Dairy Sci."}],"container-title":["Biomolecules"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2218-273X\/9\/10\/524\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:23:25Z","timestamp":1760189005000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2218-273X\/9\/10\/524"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,9,23]]},"references-count":33,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2019,10]]}},"alternative-id":["biom9100524"],"URL":"https:\/\/doi.org\/10.3390\/biom9100524","relation":{},"ISSN":["2218-273X"],"issn-type":[{"value":"2218-273X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,9,23]]}}}