{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,2]],"date-time":"2026-07-02T00:10:54Z","timestamp":1782951054043,"version":"3.54.5"},"reference-count":48,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2016,2,5]],"date-time":"2016-02-05T00:00:00Z","timestamp":1454630400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Staphylococcus aureus is one of the leading causes of food poisoning. Its pathogenicity results from the possession of virulence genes that produce different toxins which result in self-limiting to severe illness often requiring hospitalization. In this study of 200 sushi and sashimi samples, S. aureus contamination was confirmed in 26% of the food samples. The S. aureus isolates were further characterized for virulence genes and antibiotic susceptibility. A high incidence of virulence genes was identified in 96.2% of the isolates and 20 different virulence gene profiles were confirmed. DNA amplification showed that 30.8% (16\/52) of the S. aureus carried at least one SE gene which causes staphylococcal food poisoning. The most common enterotoxin gene was seg (11.5%) and the egc cluster was detected in 5.8% of the isolates. A combination of hla and hld was the most prevalent coexistence virulence genes and accounted for 59.6% of all isolates. Antibiotic resistance studies showed tetracycline resistance to be the most common at 28.8% while multi-drug resistance was found to be low at 3.8%. In conclusion, the high rate of S. aureus in the sampled sushi and sashimi indicates the need for food safety guidelines.<\/jats:p>","DOI":"10.3390\/ijerph13020199","type":"journal-article","created":{"date-parts":[[2016,2,5]],"date-time":"2016-02-05T10:06:16Z","timestamp":1454666776000},"page":"199","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":54,"title":["Virulence Factors and Antibiotic Susceptibility of Staphylococcus aureus Isolates in Ready-to-Eat Foods: Detection of S. aureus Contamination and a High Prevalence of Virulence Genes"],"prefix":"10.3390","volume":"13","author":[{"given":"Suat","family":"Puah","sequence":"first","affiliation":[{"name":"Department of Biomedical Science, Faculty of Medicine, University of Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kek","family":"Chua","sequence":"additional","affiliation":[{"name":"Department of Biomedical Science, Faculty of Medicine, University of Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin","family":"Tan","sequence":"additional","affiliation":[{"name":"Department of Biomedical Science, Faculty of Medicine, University of Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2016,2,5]]},"reference":[{"key":"ref_1","unstructured":"FDA Food Code 2009: Chapter 1\u2014Purpose & Definitions, Available online: http:\/\/www.fda.gov\/Food\/GuidanceRegulation\/RetailFoodProtection\/FoodCode\/ucm186464.htm."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"311","DOI":"10.4315\/0362-028X-57.4.311","article-title":"Anisakid parasites, Staphylococcus aureus and Bacillus cereus in sushi and sashimi from Seattle area restaurants","volume":"57","author":"Adams","year":"1994","journal-title":"J. Food Prot."},{"key":"ref_3","unstructured":"Food and Environmental Hygiene Department HKSAR Risk Assessment Studies Report No. 2. Microbiological Hazards Evaluation. Sushi and Sashimi in Hong Kong, Available online: http:\/\/www.cfs.gov.hk\/english\/programme\/programme_haccp\/files\/ss_ras2_eng.pdf."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"860","DOI":"10.4315\/0362-028X-71.4.860","article-title":"Microbiological quality of sushi from sushi bars and retailers","volume":"71","author":"Atanassova","year":"2008","journal-title":"J. Food Prot."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/j.ijfoodmicro.2012.03.022","article-title":"Occurrence and characteristics of methicillin-resistant and -susceptible Staphylococcus aureus and methicillin-resistant coagulase-negative staphylococci from Japanese retail ready-to-eat raw fish","volume":"156","author":"Hammad","year":"2012","journal-title":"Int. J. Food Microbiol."},{"key":"ref_6","first-page":"1701","article-title":"Hygienic-sanitary evaluation of sushi and sashimi sold in Messina and Catania, Italy","volume":"3","author":"Muscolino","year":"2014","journal-title":"Ital. J. Food Saf."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1111\/j.1574-6976.2011.00311.x","article-title":"Staphylococcus aureus and its food poisoning toxins: Characterization and outbreak investigation","volume":"36","author":"Hennekinne","year":"2012","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Kadariya, J., Smith, T.C., and Thapaliya, D. (2014). Staphylococcus aureus and staphylococcal food-borne disease: An ongoing challenge in public health. Biomed. Res. Int., 2014.","DOI":"10.1155\/2014\/827965"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"607","DOI":"10.3201\/eid0505.990502","article-title":"Food-related illness and death in the United States","volume":"5","author":"Mead","year":"1999","journal-title":"Emerg. Infect. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2930","DOI":"10.1128\/AEM.07487-11","article-title":"Genotypes, exotoxin gene content, and antimicrobial resistance of Staphylococcus aureus strains recovered from foods and food handlers","volume":"78","author":"Argudin","year":"2012","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/j.micinf.2004.10.009","article-title":"Enterotoxins and toxic shock syndrome toxin in Staphylococcus aureus recovered from human nasal carriers and manually handled foods: Epidemiological and genetic findings","volume":"7","author":"Fueyo","year":"2005","journal-title":"Microbes Infect."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/S0928-8244(03)00225-6","article-title":"Understanding the mechanism of action of the exfoliative toxins of Staphylococcus aureus","volume":"39","author":"Ladhani","year":"2003","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1128","DOI":"10.1086\/313461","article-title":"Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia","volume":"29","author":"Lina","year":"1999","journal-title":"Clin. Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"12","DOI":"10.3389\/fcimb.2012.00012","article-title":"Staphylococcus aureus hemolysins, bi-component leukocidins, and cytolytic peptides: A redundant arsenal of membrane-damaging virulence factors?","volume":"2","author":"Vandenesch","year":"2012","journal-title":"Front. Cell Infect. Microbiol."},{"key":"ref_15","unstructured":"Sambrook, J., and Russell, D.W. (2001). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory. [3rd ed.]."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"3869","DOI":"10.1128\/JCM.42.8.3869-3872.2004","article-title":"Modified multiplex PCR method for detection of pyrogenic exotoxin genes in staphylococcal isolates","volume":"42","author":"Lovseth","year":"2004","journal-title":"J. Clin. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1654","DOI":"10.1128\/jcm.30.7.1654-1660.1992","article-title":"Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene","volume":"30","author":"Brakstad","year":"1992","journal-title":"J. Clin. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1032","DOI":"10.1128\/JCM.38.3.1032-1035.2000","article-title":"Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance","volume":"38","author":"Mehrotra","year":"2000","journal-title":"J. Clin. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"479","DOI":"10.4315\/0362-028X-63.4.479","article-title":"The detection of enterotoxins and toxic shock syndrome toxin genes in Staphylococcus aureus by polymerase chain reaction","volume":"63","author":"Maclauchlin","year":"2000","journal-title":"J. Food Prot."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"3411","DOI":"10.1128\/JCM.37.10.3411-3414.1999","article-title":"Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates","volume":"37","author":"Monday","year":"1999","journal-title":"J. Clin. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1089\/fpd.2006.3.274","article-title":"Prevalence of enterotoxin and toxic shock syndrome toxin genes in Staphylococcus aureus isolated from milk of cows with mastitis","volume":"3","author":"Srinivasan","year":"2006","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/j.mcp.2005.03.002","article-title":"Development of a multiplex PCR assay for the identification of Staphylococcus aureus enterotoxigenic strains isolated from milk and dairy products","volume":"19","author":"Cremonesi","year":"2005","journal-title":"Mol. Cell Probes"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1128\/IAI.70.2.631-641.2002","article-title":"Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease","volume":"70","author":"Jarraud","year":"2002","journal-title":"Infect. Immun."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.ijfoodmicro.2007.02.013","article-title":"Novel multiplex PCR for the detection of the Staphylococcus aureus superantigen and its application to raw meat isolates in Korea","volume":"117","author":"Hwang","year":"2007","journal-title":"Int. J. Food Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"4999","DOI":"10.1128\/IAI.00045-08","article-title":"Identification and characterization of two novel staphylococcal enterotoxins, types S and T","volume":"76","author":"Ono","year":"2008","journal-title":"Infect. Immun."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1251","DOI":"10.1099\/jmm.0.2008\/002824-0","article-title":"Molecular epidemiology and antimicrobial susceptibilities of 273 exfoliative toxin-encoding-gene-positive Staphylococcus aureus isolates from patients with impetigo in Japan","volume":"57","author":"Nakaminami","year":"2008","journal-title":"J. Med. Microbiol."},{"key":"ref_27","unstructured":"Clinical and Laboratory Standards Institute (CLSI) (2013). Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Second Informational Supplement; CLSI Document M100-S22, Clinical and Laboratory Standards Institute."},{"key":"ref_28","first-page":"318","article-title":"Halotolerant and halophilic bacteria isolated during the ripening of salted products","volume":"61","author":"Herrero","year":"2003","journal-title":"J. Food Prot."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/j.ijfoodmicro.2012.05.021","article-title":"Incidence and characterization of Staphylococcus aureus in fishery products marketed in Galicia (Northwest Spain)","volume":"157","year":"2012","journal-title":"Int. J. Food Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.foodcont.2014.06.025","article-title":"Evaluation of ready to eat sashimi in northern Portugal restaurants","volume":"47","author":"Santos","year":"2015","journal-title":"Food Control"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ijfoodmicro.2014.11.020","article-title":"Genetic diversity and virulence potential of Staphylococcus aureus isolates from raw and processed food commodities in Shanghai","volume":"195","author":"Song","year":"2015","journal-title":"Int. J. Food Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"10254","DOI":"10.3390\/ijerph120910254","article-title":"Detection of antibiotic resistant Staphylococcus aureus from milk: A public health implication","volume":"12","author":"Akindolire","year":"2015","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1879","DOI":"10.4315\/0362-028X.JFP-15-150","article-title":"Molecular characterization and antimicrobial resistance profile of methicillin-resistant Staphylococcus aureus in retail chicken","volume":"78","author":"Sallam","year":"2015","journal-title":"J. Food Prot."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2177","DOI":"10.3390\/toxins2082177","article-title":"Staphylococcal enterotoxins","volume":"2","author":"Pinchuk","year":"2010","journal-title":"Toxins (Basel)"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"4061","DOI":"10.1128\/IAI.72.7.4061-4071.2004","article-title":"egc-Encoded superantigens from Staphylococcus aureus are neutralized by human sera much less efficiently than are classical staphylococcal enterotoxins or toxic shock syndrome toxin","volume":"72","author":"Holtfreter","year":"2004","journal-title":"Infect. Immun."},{"key":"ref_36","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_37","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1089\/fpd.2014.1850","article-title":"Staphylococcus aureus ST6-t701 isolates from food-poisoining outbreaks (2006\u20132013) in Xi\u2019an, China","volume":"12","author":"Li","year":"2015","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.ijfoodmicro.2014.12.002","article-title":"Prevalence and characterization of methicillin susceptible Staphylococcus aureus ST398 isolates from retail foods","volume":"196","author":"Li","year":"2015","journal-title":"Int. J. Food Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1278","DOI":"10.1128\/JCM.43.3.1278-1284.2005","article-title":"Cytotoxin and pyrogenic toxin superantigen gene profiles of Staphylococcus aureus associated with subclinical mastitis in daily cows and relationships with macrorestriction genomic profiles","volume":"43","author":"Fueyo","year":"2005","journal-title":"J. Clin. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"864","DOI":"10.1111\/j.1365-2672.2006.02957.x","article-title":"Molecular analysis of Staphylococcus aureus isolates associated with staphylococcal food poisoning in South Korea","volume":"101","author":"Cha","year":"2006","journal-title":"J. Appl. Microbiol."},{"key":"ref_41","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_42","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1089\/fpd.2007.0088","article-title":"Prevalence and antimicrobial resistance of foodborne pathogens isolated from food products in China","volume":"4","author":"Chao","year":"2007","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1089\/fpd.2010.0679","article-title":"Characterization of toxin genes and antimicrobial susceptibility of Staphylococcus aureus isolates from Louisiana retail meats","volume":"8","author":"Pu","year":"2011","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_44","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_45","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.ijfoodmicro.2011.10.030","article-title":"Characterization of Staphylococcus aureus isolated from powdered infant formula milk and infant rice cereal in China","volume":"153","author":"Wang","year":"2012","journal-title":"Int. J. Food Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1128\/CMR.00002-11","article-title":"Food animals and antimicrobials: Impacts on human health","volume":"24","author":"Marshall","year":"2011","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1774","DOI":"10.4315\/0362-028X-67.8.1774","article-title":"Antibacterial activities of naturally occurring compounds against antibiotic-resistant Bacillus cereus vegetative cells and spores, Escherichia coli, and Staphylococcus aureus","volume":"67","author":"Friedman","year":"2004","journal-title":"J. Food Prot."},{"key":"ref_48","unstructured":"Food and Drug Administration (FDA) Chapter 12: Pathogen Growth and Toxin Formation (Other Than Clostridium Botulinum) as a Result of Time\/Temperature Abuse, Available online: http:\/\/www.fda.gov\/downloads\/Food\/GuidanceRegulation\/UCM251970.pdf."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/13\/2\/199\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T19:18:54Z","timestamp":1760210334000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/13\/2\/199"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,2,5]]},"references-count":48,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2016,2]]}},"alternative-id":["ijerph13020199"],"URL":"https:\/\/doi.org\/10.3390\/ijerph13020199","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,2,5]]}}}