Staphylococcal food poisoning outbreaks occurred in Sicily (Italy) from 2009 to 2016


Submitted: 17 August 2023
Accepted: 11 December 2023
Published: 13 March 2024
Abstract Views: 1193
PDF: 14
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Authors

Notification of foodborne outbreaks has been mandatory in Europe since 2005, and surveillance is carried out along the entire food chain. Here we report the results obtained from laboratory investigations about four cases of foodborne outbreaks that occurred in Sicily between 2009 and 2016, deemed to be related to staphylococcal enterotoxins (SEs) and coagulase-positive Staphylococci (CPS) by the Local Public Health Authority. Primosale cheese samples were processed by culture methods for enumeration of CPS and immunoenzymatic assays for detection and differentiation of the SEs possibly contained in food samples. In all cases, the mistrusted foods were found to be contaminated by CPS at bacterial loads between 5 and 8 log CFU/g and contained SE type C (SEC). The reported data confirm the risk of staphylococcal food poisoning associated with the consumption of raw milk cheese. SEC is the most commonly occurring SE in goat milk and dairy products and the most represented enterotoxin in Sicilian dairy products. Our results highlighted the need for improving the current monitoring efficiency and implementing the available laboratory methods to collect more faithful epidemiological data on the current prevalence of staphylococcal toxins in the food chain, including SEs currently not detectable by validated analytical methods.


Abdel-Hameid Ahmed A, Saad Maharik NM, Valero A, Kamal S, 2019. Incidence of enterotoxigenic Staphylococcus aureus in milk and Egyptian artisanal dairy products. Food Control 104:20-7.

Argudín MÁ, Mendoza MC, Rodicio MR, 2010. Food poisoning and Staphylococcus aureus enterotoxins. Toxins 2:1751-73.

Basanisi MG, Nobili G, La Bella G, Russo R, Spano G, Normanno G, La Salandra G, 2016. Molecular characterization of Staphylococcus aureus isolated from sheep and goat cheeses in southern Italy. Small Ruminant Res 135:17-9.

Bianchi DM, Ingravalle F, Adriano D, Gallina S, Gramaglia M, Zuccon F, Astegiano S, Bellio A, Macori G, Ru G, Decastelli L, 2014. Reproducibility study for the detection of staphylococcal enterotoxins in dairy products between official Italian national laboratories. J Food Prot 77:999-1004.

Chen Q, Xie S, 2019. Genotypes, enterotoxin gene profiles, and antimicrobial resistance of staphylococcus aureus associated with foodborne outbreaks in Hangzhou, China. Toxins 11:307.

D’Amico DJ, Donnelly CW, 2011. Characterization of Staphylococcus aureus strains isolated from raw milk utilized in small-scale artisan cheese production. J Food Prot 74:1353-8.

De Buyser M, Groult J, Brisabois A, Assere A, Lombard B, 2009a. Detection of genes encoding Staphylococcal enterotoxins multiplex PCR for Seg to Sej and Sep. Method of the CRL for coagulase positive Staphylococci, including Staphylococcus aureus, Version 1. CRL CPS; AFSSA, Maisons-Alfort, France.

De Buyser M, Groult J, Brisabois A, Assere A, Lombard B, 2009b. Detection of genes encoding staphylococcal enterotoxins multiplex PCR for Sea to See and Ser. Method of the CRL for coagulase positive Staphylococci, including Staphylococcus aureus, version 1. CRL CPS; AFSSA, Maisons-Alfort, France.

Etter D, Schelin J, Schuppler M, Johler S, 2020. Staphylococcal Enterotoxin C - an update on SEC variants, their structure and properties, and their role in foodborne intoxications. Toxins 12:584.

European Food Safety Authority, European Centre for Disease Prevention and Control, 2021. The European Union One Health 2019 zoonoses report. EFSA J 19:e06406.

Genigeorgis C, 1989. Present state of knowledge on staphylococcal intoxication. Int J Food Microbiol 9:327-60.

Giammanco GM, Pepe A, Aleo A, D’Agostino V, Milone S, Mammina C, 2011. Microbiological quality of Pecorino Siciliano ‘primosale’ cheese on retail sale in the street markets of Palermo, Italy. New Microbiol 34:179-85.

Hennekinne JA, De Buyser ML, Dragacci S, 2012. Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiol Rev 36:815-36.

Hennekinne JA, Ostyn A, Guillier F, Gohier M, Messio S, Dragacci S, Krys S, Lombard B, 2007. Interlaboratory validation of the Vidas SET2 kit for detection of staphylococcal enterotoxins in milk products. J AOAC Int 90:756-64.

Hennekinne JA, Ostyn A, Guillier F, Herbin S, Prufer AL, Dragacci S, 2010. How should staphylococcal food poisoning outbreaks be characterized? Toxins 2:2106-16.

ISO, 2001. Microbiology of food and animal feeding stuffs - horizontal method for the enumeration of beta-glucuronidase-positive Escherichia coli - part 2: colony-count technique at 44 degrees C using 5-bromo-4-chloro-3-indolyl beta-D-glucuronide. ISO Norm 16649:2:2001. International Standardization Organization ed., Geneva, Switzerland.

ISO, 2002. Microbiology of food and animal feeding stuffs - horizontal method for the detection of Salmonella spp. ISO Norm 6579:2002. International Standardization Organization ed., Geneva, Switzerland.

ISO, 2004. Microbiology of food and animal feeding stuffs - horizontal method for the enumeration of coagulase-positive Staphylococci (Staphylococcus aureus and other species) - technique using rabbit plasma fibrinogen agar medium. ISO Norm 6888-2:2004. International Standardization Organization ed., Geneva, Switzerland.

ISO, 2006. Microbiology of food and animal feeding stuffs - horizontal method for the enumeration of coliforms - colony-count technique. ISO Norm 4832:2006. International Standardization Organization ed., Geneva, Switzerland.

ISO, 2017a. Microbiology of the food chain - horizontal method for the immunoenzymatic detection of staphylococcal enterotoxins in foodstuffs. ISO Norm 19020:2017. International Standardization Organization ed., Geneva, Switzerland.

ISO, 2017b. Microbiology of the food chain - horizontal method for the detection and enumeration of Listeria monocytogenes and of Listeria spp. - part 1: detection method. ISO Norm 11290-1:2017b. International Standardization Organization ed., Geneva, Switzerland.

Johler S, Macori G, Bellio A, Acutis PL, Gallina S, Decastelli L, 2018. Short communication: characterization of Staphylococcus aureus isolated along the raw milk cheese production process in artisan dairies in Italy. J Dairy Sci 101:2915-20.

Kadariya J, Smith TC, Thapaliya D, 2014. Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. Biomed Res Int 2014:827965.

Kérouanton A, Hennekinne JA, Letertre C, Petit L, Chesneau O, Brisabois A, De Buyser ML, 2007. Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int J Food Microbiol, 115:369-75.

Normanno G, La Salandra G, Dambrosio A, Quaglia NC, Corrente M, Parisi A, Santagada G, Firinu A, Crisetti E, Celano V, 2007. Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. Int J Food Microbiol 115:290-6.

Nunes MM, Caldas ED, 2017. Preliminary quantitative microbial risk assessment for Staphylococcus enterotoxins in fresh Minas cheese, a popular food in Brazil. Food Control 73:524-31.

Schelin J, Wallin-Carlquist N, Thorup Cohn M, Lindqvist R, Barker GC, 2011. The formation of Staphylococcus aureus enterotoxin in food environments and advances in risk assessment. Virulence 2:580-92.

Vitale M, Scatassa ML, 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 12:21-3.

Weiler N, Leotta GA, Zárate MN, Manfredi E, Alvarez ME, Rivas M, 2011. Foodborne outbreak associated with consumption of ultrapasteurized milk in the Republic of Paraguay. Rev Argent Microbiol 43:33-6. [Article in Spanish].

1.
Cardamone C, Castello A, Oliveri G, Costa A, Sciortino S, Nia Y, Hennekinne JA, Romano A, Zuccon F, Decastelli L. Staphylococcal food poisoning outbreaks occurred in Sicily (Italy) from 2009 to 2016. Ital J Food Safety [Internet]. 2024 Mar. 13 [cited 2024 May 18];13(2). Available from: https://www.pagepressjournals.org/ijfs/article/view/11667

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