Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2023 Dec 15;11(12):2993.
doi: 10.3390/microorganisms11122993.

Enterotoxigenic and Antimicrobic Susceptibility Profile of Staphylococcus aureus Isolates from Fresh Cheese in Croatia

Ivana Ljevaković-Musladin  1 , Lidija Kozačinski  2 , Marija Krilanović  3 , Marina Vodnica Martucci  3 , Mato Lakić  1 , Luca Grispoldi  4 , Beniamino T Cenci-Goga  4
Affiliations

Enterotoxigenic and Antimicrobic Susceptibility Profile of Staphylococcus aureus Isolates from Fresh Cheese in Croatia

Ivana Ljevaković-Musladin et al. Microorganisms. .

Abstract

Certain Staphylococcus aureus strains harbour staphylococcal enterotoxin genes and hence can produce enterotoxin during their growth in food. Therefore, food can be a source of staphylococcal food poisoning, one of the most common food-borne diseases worldwide. Epidemiological data show that S. aureus is often present in raw milk cheeses, and consequently, cheeses are often the source of staphylococcal food poisoning outbreaks. The aim of this study was to determine the phenotypic characteristics of S. aureus isolates from fresh cheese, including antibiotic susceptibility; the presence of classical sea-see enterotoxin genes through molecular methods; and the isolate's ability to produce SEA-SEE enterotoxins in vitro through reversed passive latex agglutination. A total of 180 coagulase-positive staphylococci were isolated from 18 out of 30 cheese samples, and 175 were confirmed as S. aureus through latex agglutination and API STAPH tests. All isolates possessed phenotypic characteristics typical for S. aureus, with certain variations in the egg yolk reaction (18.3% of the isolates showed a weak reaction and 28% no reaction at all) and haemolysis pattern (36.6% of the isolates produced double-haemolysis and 4.6% were non-haemolytic). Antibiotic resistance was observed in 1.1% of the isolates and to mupirocin only. Real-time PCR detected the sec gene in 34 (19.4%) isolates, but most isolates (80.6%) were not enterotoxigenic. For all 34 (19.4%) strains that carried the sec gene, the RPLA method detected the production of the SEC enterotoxin in vitro. For those enterotoxigenic strains, the possibility of enterotoxin production in fresh cheese could not be ruled out.

Keywords: Staphylococcus aureus; antimicrobic susceptibility; cheese; enterotoxigenicity; staphylococcal enterotoxins.

PubMed Disclaimer

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Cluster dendrogram for 175 S. aureus isolates.
Figure 2
Figure 2
Cluster dendrogram for 34 SEC-positive S. aureus isolates.
See this image and copyright information in PMC

References

    1. Nia Y., Mutel I., Assere A., Lombard B., Auvray F., Hennekinne J.-A. Review Over a 3-Year Period of European Union Proficiency Tests for Detection of Staphylococcal Enterotoxins in Food Matrices. Toxins. 2016;8:107. doi: 10.3390/toxins8040107. - DOI - PMC - PubMed
    1. Rajkovic A., Jovanovic J., Monteiro S., Decleer M., Andjelkovic M., Foubert A., Beloglazova N., Tsilla V., Sas B., Madder A., et al. Detection of toxins involved in foodborne diseases caused by Gram-positive bacteria. Compr. Rev. Food Sci. Food Saf. 2020;19:1605–1657. doi: 10.1111/1541-4337.12571. - DOI - PubMed
    1. De Buyser M.-L., Dufour B., Maire M., Lafarge V. Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. Int. J. Food Microbiol. 2001;67:1–17. doi: 10.1016/S0168-1605(01)00443-3. - DOI - PubMed
    1. Delmas G., Gallay A., Espié E., Haeghebaert S., Pihier N., Weill F.X., De Valk H., Vaillant V., Desenclos J.C. Les toxi-infections alimentaires collectives en France entre 1996 et 2005. Bull. Epidemiol. Hebd. 2006;51–52:418–422.
    1. Gajewska J., Zakrzewski A., Chajęcka-Wierzchowska W., Zadernowska A. Meta-analysis of the global occurrence of S. aureus in raw cattle milk and artisanal cheeses. Food Control. 2023;147:109603. doi: 10.1016/j.foodcont.2023.109603. - DOI

LinkOut - more resources