COAGULASE POSITIVE STAPHYLOCOCCI ENUMERATION AND ENTEROTOXINS DETECTION IN MILK AND DAIRY PRODUCTS FROM CENTRAL ITALY

Main Article Content

L. IANNETTI
O. VISCIANO
C. MARFOGLIA
G. IANNITTO
G. PARISCIANI
M. SERICOLA
D. PETRONE
M.S. MANGIERI
F. POIMILIO
M. SCHIRONE

Keywords

Coagulase positive staphylococci, milk, dairy products, process-hygiene criteria, staphylococcal enterotoxins

Abstract

This study aims at enumerating coagulase positive staphylococci (CPS) in 404 samples of milk and dairy products collected in own-checks or during the official controls from different dairy industries located in Central Italy. These microorganisms were enumerated using ISO 6888-2:1999/Amd. 1:2003 and only when they exceeded 105CFU/g, the presence of any of the seven more common staphylococcal enterotoxins (SEA, SEB, SEC1, SEC2, SEC3, SED and SEE) was also investigated. Own-checks samples resulted always below the detection limit, whereas among those collected by the competent authorities in the framework of official controls, provola (100%) and mozzarella (22.9%) samples were positive to CPS, with mean values of 1.8x102 and 2.8x105 CFU/g respectively. Such values exceeded the maximum limits set by Commission Regulation (EC) No. 2073/2005, resulting in a request of hygiene improvements in the first case; in the second case, the presence of staphylococcal enterotoxins in 8 (2.7%) mozzarella samples out of 298 investigated cheese products was also observed, resulting in their withdrawn from the market. Therefore, this study aims at highlighting that monitoring of CPS incidence in dairy products and subsequent testing of cheeses for enterotoxins when appropriate represent an important tool for public health in order to avoid the occurrence of foodborne outbreaks.
Abstract 182 | pdf Downloads 178

References

Armani M., Macori G., Gallina S., Tavella A., Giusti M., Paolazzi G., Trentini L., Rabini M., Decastelli L. and Lombardo D. 2016. Coagulase positive staphylococci and food poisoning toxins –A case study of an outbreak investigation occurred in a sheperd hut. 17th International Congress on Infectious Diseases. Int. J. Infect. Dis. 45S:464.

Cremonesi P., Perez G., Pisoni G., Moroni P., Morandi S., Luzzana M., Brasca M. and Castiglioni B. 2007. Detection of enterotoxigenic Staphylococcus aureus isolates in raw milk cheese. Lett. Appl. Microbiol. 45(6):586-591.

Delbes C., Alomar J., Chougui N., Martin J.F. and Montel M.C. 2006. Staphylococcus aureus growth and enterotoxin production during the manufacture of uncooked, semihard cheese from cows’ raw milk. J. Food Prot. 69(9):2161-2167.

EC 2002. Regulation (EC) No 178/2002 of the European Parliament and of the Council of 28 January 2002 laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety. Off. J. Eur. Union L31:1-44.

EC 2005. Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Off. J. Eur. Union L338:1-26.

EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control). 2017. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J. 15(12):5077:1-228.

EU 2012. Regulation (EU) No 1151/2012 of the European Parliament and of the Council of 21/11/2012 on quality schemes for agricultural products and foodstuffs. Off. J. Eur. Union L343:1-29.

Johler S., Macori G., Bellio A., Acutis P.L., Gallina S. and 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(4):2915-2920.

Jorgensen H.J., Mork T., Hogasen H.R. and Rorvik L.M. 2005. Enterotoxigenic Staphylococcus aureus in bulk milk in Norway. J. Appl. Microbiol. 99(1):158-166.

Martins I.M., Kabuki D.Y., Miya N.T.N. and Pereira J.L. 2014. Occurrence and characterization of enterotoxigenic potential Staphylococcus isolated from dairy products. J. Food Safety 34(3):185-192.

Mehli L., Hoel S., Thomassen G.M.B., Jakobsen A.N. and Karlsen H. 2017. The prevalence, genetic diversity and antibiotic resistance of Staphylococcus aureus in milk, whey, and cheese from artisan farm dairies. Int. Dairy J. 65:20-27.

MIPAAF (Ministero delle Politiche Agricole, Alimentari, Forestali e del Turismo). Decreto 8 settembre 1999, n. 350. Regolamento recante norme per l’individuazione dei prodotti tradizionali di cui all'articolo 8, comma 1, del decreto legislativo 30 aprile 1998, n.173.

Neder V.E., Canavesio V.R. and Calvinho L.F. 2011. Presence of enterotoxigenic Staphylococcus aureus in bulk tank milk from Argentine dairy farms. Rev. Argent. Microbiol. 43:104-106.

Rajic-Savic N., Katic V., Velebit B. and Colovic S. 2015. Characteristics of enterotoxigenic coagulase positive staphylococci isolated from bovine milk in cases of subclinical mastitis. Procedia Food Sci. 5:250-253.

Rola J.G., Czubkowska A., Korpysa-Dzirba W. and Osek J. 2016. Occurrence of Staphylococcus aureus on farms with small scale production of raw milk cheeses in Poland. Toxins 8(62):1-9.

Rosengren Å., Fabricius A., Guss B., Sylvén S., Lindqvist R. 2010. Occurrence of foodborne pathogens and characterization of Staphylococcus aureus in cheese produced on farm-dairies. Int. J. Food Microbiol. 144:263-269.

Ruiz P., Barragán I., Seseña S. and Palop M.L. 2016. Is staphylococci population from milk of healthy goats safe? Int. J. Food Microbiol. 238:146-152.

Sánchez-Gamboa C., Hicks-Pérez L., Gutiérrez-Méndez N., Heredia N., García S. and Nevárez-Moorillón G.V. 2018. Microbiological changes during ripening of Chihuahua cheese manufactured with raw milk and its seasonal variations. Foods 7(153):1-12.

Schelin J., Wallin-Carlquist N., Thorup Cohn M., Lindqvist R., Barker G.C. and Rådström P. 2011. The formation of Staphylococcus aureus enterotoxin in food environments and advances in risk assessment. Virulence 2(6):580-592.

Schirone M., Tofalo R., Perpetuini G., Manetta A.C., Di Gianvito P., Tittarelli F., Battistelli N., Corsetti A., Suzzi G. and Martino G. 2018. Influence of iodine feeding on microbiological and physico-chemical characteristics and biogenic amines content in a raw ewes’ milk cheese. Foods 7(108):1-11.

Schirone M., Tofalo R., Visciano P., Corsetti A. and Suzzi G. 2012. Biogenic amines in Italian Pecorino cheese. Front. Microbiol. 3(171):1-9.

Soltan Dallal M.M., Reza Khoramizadeh M., Agha Amiri S., Saboor Yaraghi A.A. and Nezhad Fard R.M. 2016. Coagulase gene polymorphism of Staphylococcus aureus isolates. A study on dairy food products and other foods in Tehran, Iran. Food Sci. Human Wellness 5:186-190.

Verraes C., Claeys W., Cardoen S., Daube G., De Zutter L., Imberechts H., Dierick k. and Herman L. 2014. A review of the microbiological hazards of raw milk from animal species other than cows. Int. Dairy J. 39:121-130.

Viçosa G.N., Moraes P.M., Yamazi A.K. and Nero L.A. 2009. Enumeration of coagulase and thermonuclease-positive Staphylococcus spp. in raw milk and fresh soft cheese: an evaluation of Baird-Parker agar, Rabbit Plasma Fibrinogen agar and the Petrifilm TM Staph Express count system. Food Microbiol. 27:447-452.

Yoon Y., Lee S. and Choi K.H. 2016. Microbial benefits and risks of raw milk cheese. Food Control 63:201-215.

Wallin-Carlquist N., Márta D., Borch E. and Rådström P. 2010. Prolonged expression and production od Staphylococcus aureus enterotoxin A in processed pork meat. Int. J. Food Microbiol. 141:S69-S74.