PRESENCE OF STAPHYLOCOCCUS AUREUS ENTEROTOXIN GENES IN MILK AND DAIRY PRODUCTS - A REVIEW

Milijana Sindjic

doi:10.5937/ffr0-55906

Milijana Sindjic Faculty of Veterinary Medicine, University of Belgrade

DOI: https://doi.org/10.5937/ffr0-55906

Sažetak

Staphylococcus aureus is a highly adaptable microorganism that is commonly found in a variety of settings, including the skin and mucous membranes of humans and animals, as well as in the air, soil, and water. It is widely known for possessing a variety of virulence factors that enable it to cause and spread diseases. The presence of the genes for TSST-1 and enterotoxin A in milk and milk products will receive the most emphasis in this review. S. aureus isolated from milk can carry individual or combinations of genes coding for classical enterotoxins. The expression of many virulence-related genes S. aureus is regulated by the agr (accessory gene regulator) system, a two-component signaling system that down-regulates surface proteins and up-regulates secretory proteins, including various enterotoxins such as SEB, SEC, SED, and TSST-1. Staphylococcal food poisoning (SFP) is commonly linked to the growth of staphylococci in protein-rich foods, for example, meat, milk, and dairy products. The growth of S. aureus and the production of enterotoxins are heavily influenced by the characteristics of the food, including salt content, pH, nutrient availability, oxygen levels, and temperature. In the dairy industry, strict control methods and ongoing monitoring are necessary to guarantee food safety. Long-term storage of milk above 8°C greatly raises the danger of S. aureus growth and the possibility of enterotoxin development.

Reference

Abril, G. A., Villa, G. T., Barros-Velázquez, J., Cañas, B., Sánchez-Pérez A., Calo-Mata, P., & Carrera, M. (2020). Staphylococcus aureus exotoxins and their detection in the dairy industry and mastitis. Toxins, 12(9), 537. https:// doi.org/ 10.3390/toxins12090537

Ahmad-Mansour, N., Loubet, P., Pouget, C., Dunyach-Remy, C., Sotto, A., Lavigne, J. P., & Molle, V. (2021). Staphylococcus aureus toxins: an update on their pathogenic properties and potential treatments. Toxins, 13(10), 677. https://doi.org/10.3390/toxins13100677

Babić, M., Pajić, M., Nikolić, A., Teodorović, V., Mirilović, M., Milojević, L., & Velebit, B. (2018). Expression of toxic shock syndrome toxin-1 gene of Staphylococcus aureus in milk: Proof of concept. Mljekarstvo, 68(1), 12-20. https://doi.org/10.15567/mljekarstvo.2018.0102

Babić, M., Pajić, M., Radinović, M., Boboš, S., Bulajić, S., Nikolić, A. & Velebit, B. (2019). Effects of temperature abuse on the growth and staphylococcal enterotoxin A gene (sea) expression of Staphylococcus aureus in milk. Foodborne Pathogens and Disease, 16(4), 282-289. https://doi.org/10.1089/fpd.2018.2544.

Balaban, N., & Rasooly, A. (2000). Staphylococcal enterotoxins. International Journal of Food Microbiology, 61(1), 1-10. https//doi.org/10.1016/s0168-1605(00)00377-9

Baniardalan, S., Mohammadzadeh, A., Pajohi-Alamoti, M., Mahmoodi, P., & Sadeghinasab, A. (2017). Detection of toxic shock toxin (tst) gene in Staphylococcus aureus isolated from bovine milk samples. Bulgarian Journal of Veterinary Medicine, 20(3), 236-243. https://doi.org/ 10.15547/bjvm.1007

Belay, N., & Rasooly, A. (2002). Staphylococcus aureus growth and enterotoxin A production in an anaerobic environment. Journal of Food Protection, 65(1), 199-204. https://doi.org/10.4315/0362-028x-65.1.199

Bergdoll, M. S., & Lee Wong, A. C. (2006). Staphylococcal intoxications. Foodborne Infections and Intoxications, 3, 523-562. https://doi.org/ 10.1016/B978-012588365-8/50018-9

Bianchi, D. M., Gallina, S., Bellio, A., Chiesa, F., Civera, T., & Decastelli, L. (2014). Enterotoxin gene profiles of Staphylococcus aureus isolated from milk and dairy products in Italy. Letters in Applied Microbiology, 58(2), 190-196. https://doi.org/10.1111/lam.12182

Božić, D. (2024). Staphylococcus aureus virulence factors and their role in biofilm-associated infections. Archives of Pharmacy, 74 (Notebook 4), 523-539. https://doi.org/10.5937/arhfarm74-51881

Chambers, H. F., & DeLeo, F. R. (2009). Waves of resistance: Staphylococcus aureus in the antibiotic era. Nature Reviews Microbiology, 7(9), 629-641. https://doi.org/ 10.1038/nrmicro2200

Cotter, P. D., Hill, C., & Ross, R. P. (2005) Bacteriocins: developing innate immunity for food. Nature Reviews Microbiology, 3(10), 777–788. https://doi.org/ 10.1038/nrmicro1273

Cretenet, M., Nouaille, S., Thouin, J., Rault, L., Stenz, L., François, P., Hennekinne, J. A., Piot, M., Maillard, B. M., Fauquant, J., Loubière, P., Le Loir, Y., & Even, S. (2011). Staphylococcus aureus virulence and metabolism are dramatically affected by Lactococcus lactis in cheese matrix. Environmental Microbiology Reports, 3(3), 340-351. https://doi.org/ 10.1111/j.1758-2229.2010.00230.x

Deurenberg, R. H., Nieuwenhuis, R. F., Driessen, C., London, N., Stassen, F. R., Tiel Van, F. H., Stobberingh, E.E., & Vink, C. (2005). The prevalence of the Staphylococcus aureus tst gene among community-and hospital-acquired strains and isolates from Wegener's Granulomatosis patients. FEMS Microbiology Letters, 245(1), 185-189. https://doi.org/ 10.1016/j.femsle.2005.03.002

Etter, D., Ukowitz, C., Eicher, C., Tasara, T., & Johler, S. (2022). Mild NaCl stress influences staphylococcal enterotoxin C transcription in a time-dependent manner and reduces protein expression. Frontiers in Microbiology, 13, 820067. https://doi.org/10.3389/fmicb.2022.820067

Even, S., Charlier, C., Nouaille, S., Ben Zakour, N. L., Cretenet, M., Cousin, F. J., Gautier, M., Cocaign-Bousquet, M., Loubière, P. & Le Loir, Y. (2009). Staphylococcus aureus virulence expression is impaired by Lactococcus lactis in mixed cultures. Applied and Environmental Microbiology, 75(13), 4459-4472. https://doi.org/ 10.1128/AEM.02388-08

Farahmand, A. S., Ahmadi, M., Dastmalchi, S. H., & Anassori, E. (2013). Identification of toxic shock syndrome Toxin-1 (TSST-1) gene in Staphylococcus aureus isolated from bovine mastitis milk. Archives of Razi Institute, 68(1), 17–22. https//doi.org/ 10.7508/ari.2013.01.003

Fagundes, H., Barchesi, L., Nader Filho, A., Ferreira, L. M., & Oliveira, C. A. F. (2010). Occurrence of Staphylococcus aureus in raw milk produced in dairy farms in São Paulo state, Brazil. Brazilian Journal of Microbiology, 41, 376-380.

Farrell, G. M., & Upton, M. E. (1978). The effect of low temperature on the growth and survival of Staphylococcus aureus and Salmonella typhimurium when inoculated on to bacon. International Journal of Food Science & Technology, 13(1), 15-23. https://doi.org/10.1111/j.1365-2621.1978.tb00771.x

Foster, T. J. (2005). Immune evasion by staphylococci. Nature Reviews Microbiology, 3(12), 948-958. https//doi.org/ 10.1038/nrmicro1289

Fooladi, A. I., Tavakoli, H. R., & Naderi, A. (2010). Detection of enterotoxigenic Staphylococcus aureus isolates in domestic dairy products. Iranian Journal of Microbiology, 2(3), 137.

Fueyo, J. M., Mendoza, M. C., Rodicio, M. R., Muniz, J., Alvarez, M. A., & Martín, M. C. (2005). Cytotoxin and pyrogenic toxin superantigen gene profiles of Staphylococcus aureus associated with subclinical mastitis in dairy cows and relationships with macrorestriction genomic profiles. Journal of Clinical Microbiology, 43(3), 1278-1284. https//doi.org/ 10.1128/JCM.43.3.1278-1284.2005

Grispoldi, L., Karama, M., Armani, A., Hadjicharalambous, C., & Cenci-Goga, B. T. (2021). Staphylococcus aureus enterotoxin in food of animal origin and staphylococcal food poisoning risk assessment from farm to table. Italian Journal of Animal Science, 20(1), 677-690. https://doi.org/10.1080/1828051X.2020.1871428

Hassani, S., Doust, R. H., & Mobarez, A. M. (2014). Enterotoxin A gene barrier Staphylococcus aureus within traditionally dairy products of Tehran. International Journal of Enteric Pathogens, 2(4), 20904-20906. https://doi.org/ 10.17795/ijep20906

Homsombat, T., Boonyayatra, S., Awaiwanont, N., & Pichpol, D. (2021). Effect of temperature on the expression of classical enterotoxin genes among staphylococci associated with bovine mastitis. Pathogens, 10(8), 975. https://doi.org/10.3390/pathogens10080975

Huntzinger, E., Boisset, S., Saveanu, C., Benito, Y., Geissmann, T., Namane, A., Lina, G., Etienne, J., Ehresmann, B., Ehresmann, C., Jacquier, A., Vandenesch, F., & Romby, P. (2005). Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. The EMBO Journal, 24(4), 824-835. https://doi.org/ 10.1038/sj.emboj.7600572

Hudson, J. A., Olsen, L., & Cook, R. (2011). Minimum growth temperatures of foodborne pathogens and recommended chiller temperatures. MPI Technical Paper No. 2016/04. Ministry for Primary Industries, New Zealand Government. Wellington, New Zealand: Crown Copyright Ministry for Primary Industries https://www.mpi.govt.nz/dmsdocument/44050/direct

Ito, A., Sato, Y., Kudo, S., Sato, S., Nakajima, H., & Toba, T. (2003). The screening of hydrogen peroxide-producing lactic acid bacteria and their application to inactivating psychrotrophic food-borne pathogens. Current Microbiology, 47(3), 231–236. https://doi.org./ 10.1007/s00284-002-3993-1

Jenul, C., & Horswill, A. R. (2019). Regulation of Staphylococcus aureus virulence. Microbiology Spectrum, 7(2), 1110-1128. https/doi.org/ 10.1128/microbiolspec.GPP3-0031-2018

Kadariya, J., Smith, T. C., & Thapaliya, D. (2014). Staphylococcus aureus and staphylococcal food‐borne disease: an ongoing challenge in public health. BioMed Research International, 2014(1), 827965. https//doi.org/ 10.1155/2014/827965

Li, S. J., Hu, D. L., Maina, E. K., Shinagawa, K., Omoe, K., & Nakane, A. (2011). Superantigenic activity of toxic shock syndrome toxin‐1 is resistant to heating and digestive enzymes. Journal of Applied Microbiology, 110(3), 729-736. https//doi.org/ 10.1111/j.1365-2672.2010.04927.x

Malachowa, N., & DeLeo, F. R. (2010). Mobile genetic elements of Staphylococcus aureus. Cellular and Molecular Life Sciences, 67, 3057-3071. https//doi.org/ 10.1007/s00018-010-0389-4

Medveďova , A., Valík, Ľ., & Studeničová, A. (2009). The effect of temperature and water activity on the growth of Staphylococcus aureus. Czech Journal of Food Sciences, 27(Special Issue 2), S2-28-S2-35. https//doi.org/ 10.17221/204/2009-CJFS

Morar, A., Ban-Cucerzan, A., Herman, V., Tîrziu, E., Sallam, K. I., Abd-Elghany, S. M., & Imre, K. (2021). Multidrug resistant coagulase-positive Staphylococcus aureus and their enterotoxins detection in traditional cheeses marketed in Banat Region, Romania. Antibiotics, 10(12), 1458. https//doi.org/ 10.3390/antibiotics10121458

Mossel, D.A.A., Corry, J.E.L., Struijk, C.B., & Baird, R.M., (1995). Essentials of the microbiology of foods. A textbook for advanced studies. Chichester, England: John Wiley and Sons.

Mossel, D. A. A., & Netten, P. V. (1990). Staphylococcus aureus and related Staphylococci in foods: ecology, proliferation, toxinogenesis, control and monitoring. Journal of Applied Bacteriology, 19, S123–S145.

Oliveira, L. D., Soares e Barros, L. S., Silva, V. C., & Cirqueira, M. G. (2011). Study of Staphylococcus aureus in raw and pasteurized milk consumed in the Reconcavo area of the State of Bahia, Brazil. Journal of Food Processing & Technology, 2(6), 128–132. https//doi.org/10.4172/2157-7110.1000128

Omoe, K., Ishikawa, M., Shimoda, Y., Hu, D. L., Ueda, S., & Shinagawa, K. (2002). Detection of seg, seh, and sei genes in Staphylococcus aureus isolates and determination of the enterotoxin productivities of S. aureus isolates harboring seg, seh, or sei genes. Journal of Clinical Microbiology, 40(3), 857-862. https//doi.org/10.1128/JCM.40.3.857-862.2002

Ote, I., Taminiau, B., Duprez, J. N., Dizier, I., & Mainil, J. G. (2011). Genotypic characterization by polymerase chain reaction of Staphylococcus aureus isolates associated with bovine mastitis. Veterinary Microbiology, 153(3-4), 285-292. https//doi.org/ 10.1016/j.vetmic.2011.05.042.

Pinchuk, I. V., Beswick, E. J., & Reyes, V. E. (2010). Staphylococcal enterotoxins. Toxins, 2(8), 2177-2197. https//doi.org/ 10.3390/toxins2082177

Pitt, W., Harden, T., & Hull, R. R. (2000). Investigation of the antimicrobial activity of raw milk against several foodborne pathogens. Milk Science International - Milchwissenschaft, 55(5), 249-252.

Ross, R. P., Morgan, S., & Hill, C. (2002). Preservation and fermentation: past, present and future. International Journal of Food Microbiology, 79(1-2), 3-16. https://doi.org./10.1016/s0168-1605(02)00174-5

Qi, Y., & Miller, K. J. (2000). Effect of low water activity on staphylococcal enterotoxin A and B biosynthesis. Journal of Food Protection, 63(4), 473-478. https://doi.org/ 10.4315/0362-028x-63.4.473

Schelin, J., Wallin-Carlquist, N., Thorup Cohn, M., Lindqvist, R., & Barker, G. C. (2011). The formation of Staphylococcus aureus enterotoxin in food environments and advances in risk assessment. Virulence, 2(6), 580-592. https//doi.org/10.4161/viru.2.6.18122

Smith, J. L., Buchanan, R. L., & Palumbo, S. A. (1983). Effect of food environment on staphylococcal enterotoxin synthesis: a review. Journal of Food Protection, 46(6), 545-555. https//doi.org/ 10.4315/0362-028X-46.6.545

Tsutsuura, S., & Murata, M. (2012). Temperature dependence of staphylococcal enterotoxin A production by Staphylococcus aureus. Bioscience, Biotechnology, and Biochemistry, 77(1), 30-37. https://doi.org/ 10.1271/bbb.120391

Vitale, M., Scatassa, M. L., Cardamone, C., Oliveri, G., Piraino, C., Alduina, R., & Napoli, C. (2015). Staphylococcal food poisoning case and molecular analysis of toxin genes in Staphylococcus aureus strains isolated from food in Sicily, Italy. Foodborne Pathogens and Disease, 12(1), 21-23. https//doi.org/ 10.1089/fpd.2014.1760

Wallin-Carlquist, N., Cao, R., Márta, D., da Silva, A. S. A., Schelin, J., & Rådström, P. (2010). Acetic acid increases the phage-encoded enterotoxin A expression in Staphylococcus aureus. BMC Microbiology, 10, 1-10. https//doi.org/10.1186/1471-2180-10-147

Zeaki, N., Budi Susilo, Y., Pregiel, A., Rådström, P., & Schelin, J. (2015). Prophage-encoded staphylococcal enterotoxin A: Regulation of production in Staphylococcus aureus strains representing different sea regions. Toxins, 7(12), 5359-5376. https://doi.org/10.3390/toxins7124889

Zhang, J., Wang, J., Jin, J., Li, X., Zhang, H., Shi, X., & Zhao, C. (2022). Prevalence, antibiotic resistance, and enterotoxin genes of Staphylococcus aureus isolated from milk and dairy products worldwide: A systematic review and meta-analysis. Food Research International, 162, 111969. https//doi.org/ 10.1016/j.foodres.2022.111969