Occurrence and Patterns of Enterotoxin Genes, Types and Antimicrobial Resistance Patterns in in Food and Food Contact Surfaces in Singapore

Overview

Journal Microorganisms

Specialty Microbiology

Date 2023 Jul 29

PMID 37512957

Authors

Ker Li Lim

Wei Ching Khor

Kar Hui Ong

Lois Timothy

Kyaw Thu Aung

Affiliations

Soon will be listed here.

Abstract

contamination of food and food contact surfaces is a public health concern given its virulent and antimicrobial-resistant properties worldwide. In this study, a total of 181 MSSA isolates were analyzed for SE genes, antimicrobial resistance patterns, and types. Overall, 24.9% of isolates were positive for SE gene detection, with being the most prevalent classical SE (18.8%). The most predominant sample sources for SE gene contamination were hand swabs for (6/48), meat dishes for (3/14) and seafood dishes for (2/24). Antimicrobial resistance was also observed at relatively high frequencies for the clinically important antibiotics penicillin G and ampicillin (both 54.7%), followed by tetracycline (14.9%) and azithromycin (8.8%). In addition, characterization of types revealed type t5078 to be the most predominant (40.3%), with significant associations between types t127 and t5521 and the gene. This study offers insights into the enterotoxin gene and antimicrobial resistance profiles of in cooked or ready-to-eat food to inform future surveillance and epidemiological studies.

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References

Akpaka P, Roberts R, Monecke S . Molecular characterization of antimicrobial resistance genes against Staphylococcus aureus isolates from Trinidad and Tobago. J Infect Public Health. 2016; 10(3):316-323. DOI: 10.1016/j.jiph.2016.05.010. View

Johler S, Macori G, Bellio A, Acutis P, Gallina S, Decastelli L . Short communication: Characterization of Staphylococcus aureus isolated along the raw milk cheese production process in artisan dairies in Italy. J Dairy Sci. 2018; 101(4):2915-2920. DOI: 10.3168/jds.2017-13815. View

Pinchuk I, Beswick E, Reyes V . Staphylococcal enterotoxins. Toxins (Basel). 2011; 2(8):2177-97. PMC: 3153290. DOI: 10.3390/toxins2082177. View

Strommenger B, Kettlitz C, Weniger T, Harmsen D, Friedrich A, Witte W . Assignment of Staphylococcus isolates to groups by spa typing, SmaI macrorestriction analysis, and multilocus sequence typing. J Clin Microbiol. 2006; 44(7):2533-40. PMC: 1489514. DOI: 10.1128/JCM.00420-06. View

Olsen J, Christensen H, Aarestrup F . Diversity and evolution of blaZ from Staphylococcus aureus and coagulase-negative staphylococci. J Antimicrob Chemother. 2006; 57(3):450-60. DOI: 10.1093/jac/dki492. View

Asao T, Kumeda Y, Kawai T, Shibata T, Oda H, Haruki K . An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: estimation of enterotoxin A in the incriminated milk and powdered skim milk. Epidemiol Infect. 2003; 130(1):33-40. PMC: 2869936. DOI: 10.1017/s0950268802007951. View

Shimamura Y, Kidokoro S, Murata M . Survey and properties of Staphylococcus aureus isolated from Japanese-style desserts. Biosci Biotechnol Biochem. 2006; 70(7):1571-7. DOI: 10.1271/bbb.50617. View

Chajecka-Wierzchowska W, Zadernowska A, Nalepa B, Sierpinska M, Laniewska-Trokenheim L . Retail ready-to-eat food as a potential vehicle for Staphylococcus spp. harboring antibiotic resistance genes. J Food Prot. 2014; 77(6):993-8. DOI: 10.4315/0362-028X.JFP-13-466. View

Berger T, Eisenkraft A, Bar-Haim E, Kassirer M, Aran A, Fogel I . Toxins as biological weapons for terror-characteristics, challenges and medical countermeasures: a mini-review. Disaster Mil Med. 2017; 2:7. PMC: 5330008. DOI: 10.1186/s40696-016-0017-4. View

10.

Strommenger B, Kettlitz C, Werner G, Witte W . Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus. J Clin Microbiol. 2003; 41(9):4089-94. PMC: 193808. DOI: 10.1128/JCM.41.9.4089-4094.2003. View

11.

Johler S, Giannini P, Jermini M, Hummerjohann J, Baumgartner A, Stephan R . Further evidence for staphylococcal food poisoning outbreaks caused by egc-encoded enterotoxins. Toxins (Basel). 2015; 7(3):997-1004. PMC: 4379538. DOI: 10.3390/toxins7030997. View

12.

Mashouf R, Hosseini S, Mousavi S, Arabestani M . Prevalence of Enterotoxin Genes and Antibacterial Susceptibility Pattern of Staphylococcus aureus Strains Isolated from Animal Originated Foods in West of Iran. Oman Med J. 2015; 30(4):283-90. PMC: 4561649. DOI: 10.5001/omj.2015.56. View

13.

Gill D . Bacterial toxins: a table of lethal amounts. Microbiol Rev. 1982; 46(1):86-94. PMC: 373212. DOI: 10.1128/mr.46.1.86-94.1982. View

14.

Sanlibaba P . Prevalence, antibiotic resistance, and enterotoxin production of Staphylococcus aureus isolated from retail raw beef, sheep, and lamb meat in Turkey. Int J Food Microbiol. 2021; 361:109461. DOI: 10.1016/j.ijfoodmicro.2021.109461. View

15.

Peacock S, de Silva G, Justice A, Cowland A, Moore C, Winearls C . Comparison of multilocus sequence typing and pulsed-field gel electrophoresis as tools for typing Staphylococcus aureus isolates in a microepidemiological setting. J Clin Microbiol. 2002; 40(10):3764-70. PMC: 130877. DOI: 10.1128/JCM.40.10.3764-3770.2002. View

16.

Normanno G, Firinu A, Virgilio S, Mula G, DAmbrosio A, Poggiu A . Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. Int J Food Microbiol. 2004; 98(1):73-9. DOI: 10.1016/j.ijfoodmicro.2004.05.008. View

17.

Oliveira D, Tomasz A, de Lencastre H . The evolution of pandemic clones of methicillin-resistant Staphylococcus aureus: identification of two ancestral genetic backgrounds and the associated mec elements. Microb Drug Resist. 2002; 7(4):349-61. DOI: 10.1089/10766290152773365. View

18.

Cremonesi P, Luzzana M, Brasca M, Morandi S, Lodi R, Vimercati C . Development of a multiplex PCR assay for the identification of Staphylococcus aureus enterotoxigenic strains isolated from milk and dairy products. Mol Cell Probes. 2005; 19(5):299-305. DOI: 10.1016/j.mcp.2005.03.002. View

19.

Da Costa T, de Oliveira C, Chambers H, Chatterjee S . PBP4: A New Perspective on β-Lactam Resistance. Microorganisms. 2018; 6(3). PMC: 6164785. DOI: 10.3390/microorganisms6030057. View

20.

Ho J, ODonoghue M, Boost M . Occupational exposure to raw meat: a newly-recognized risk factor for Staphylococcus aureus nasal colonization amongst food handlers. Int J Hyg Environ Health. 2013; 217(2-3):347-53. DOI: 10.1016/j.ijheh.2013.07.009. View