Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France

Cheese is a complex and dynamic microbial ecosystem characterized by the presence of a large variety of bacteria, yeasts, and molds. Some microorganisms, including species of lactobacilli or lactococci, are known to contribute to the organoleptic quality of cheeses, whereas the presence of other microorganisms may lead to spoilage or constitute a health risk. Staphylococcus aureus is recognized worldwide as an important food-borne pathogen, owing to the production of enterotoxins in food matrices. In order to study enterotoxin gene expression during cheese manufacture, we developed an efficient procedure to recover total RNA from cheese and applied a robust strategy to study gene expression by reverse transcription-quantitative PCR (RT-qPCR). This method yielded pure preparations of undegraded RNA suitable for RT-qPCR. To normalize RT-qPCR data, expression of 10 potential reference genes was investigated during S. aureus growth in milk and in cheese. The three most stably expressed reference genes during cheese manufacture were ftsZ, pta, and gyrB, and these were used as internal controls for RT-qPCR of the genes sea and sed, encoding staphylococcal enterotoxins A and D, respectively. Expression of these staphylococcal enterotoxin genes was monitored during the first 72 h of the cheese-making process, and mRNA data were correlated with enterotoxin production.

Tool for Quantification of Staphylococcal Enterotoxin Gene Expression in Cheese

Selection and characterization of DNA aptamers against Staphylococcus aureus enterotoxin C1.

Bacterial toxins are food safety hazards causing about 10% of all reported foodborne outbreaks in Europe. Pertinent to Gram-positive pathogens, the most relevant toxins are emetic toxin and diarrheal enterotoxins of Bacillus cereus, neurotoxins of Clostridium botulinum, enterotoxin of Clostridium perfringens, and a family of enterotoxins produced by Staphylococcus aureus and some other staphylococci. These toxins are the most important virulence factors of respective foodborne pathogens and a primary cause of the related foodborne diseases. They are proteins or peptides that differ from each other in their size, structure, toxicity, toxicological end points, solubility, and stability, types of food matrix to which they are mostly related to. These differences influence the characteristics of required detection methods. Therefore, detection of these toxins in food samples, or detection of toxin production capacity in the bacterial isolate, remains one of the cornerstones of microbial food analysis and an essential tool in understanding the relevant properties of these toxins. Advanced research has led into new insights of the incidence of toxins, mechanisms of their production, their physicochemical properties, and their toxicological mode of action and dose-response profile. This review focuses on biological, immunological, mass spectrometry, and molecular assays as the most commonly used detection and quantification methods for toxins of B. cereus, C. botulinum, C. perfringens, and S. aureus. Gathered and analyzed information provides a comprehensive blueprint of the existing knowledge on the principles of these assays, their application in food safety, limits of detection and quantification, matrices in which they are applicable, and type of information they provide to the user.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/1541-4337.12571

Detection of toxins involved in foodborne diseases caused by Gram-positive bacteria.

In complex environments such as cheeses, the lack of relevant information on the physiology and virulence expression of pathogenic bacteria and the impact of endogenous microbiota has hindered progress in risk assessment and control. Here, we investigated the behaviour of Staphylococcus aureus, a major foodborne pathogen, in a cheese matrix, either alone or in the presence of Lactococcus lactis, as a dominant species of cheese ecosystems. The dynamics of S. aureus was explored in situ by coupling a microbiological and, for the first time, a transcriptomic approach. Lactococcus lactis affected the carbohydrate and nitrogen metabolisms and the stress response of S. aureus by acidifying, proteolysing and decreasing the redox potential of the cheese matrix. Enterotoxin expression was positively or negatively modulated by both L. lactis and the cheese matrix itself, depending on the enterotoxin type. Among the main enterotoxins involved in staphylococcal food poisoning, sea expression was slightly favoured in the presence of L. lactis, whereas a strong repression of sec4 was observed in cheese matrix, even in the absence of L. lactis, and correlated with a reduced saeRS expression. Remarkably, the agr system was downregulated by the presence of L. lactis, in part because of the decrease in pH. This study highlights the intimate link between environment, metabolism and virulence, as illustrated by the influence of the cheese matrix context, including the presence of L. lactis, on two major virulence regulators, the agr system and saeRS.

https://hal-normandie-univ.archives-ouvertes.fr/hal-02291148/document

Staphylococcus aureus virulence and metabolism are dramatically affected by Lactococcus lactis in cheese matrix

Aim: Immunological tools used to detect staphylococcal enterotoxins (SEs) in foods are numerous. The aim of this study was to evaluate, on naturally contaminated milk product samples, the performance of the Vidas SET2, in comparison to the Transia plate SET.



Methods and Results:  The Vidas SET2 was compared with the Transia plate SET on supernatants of Staphylococcus aureus isolates and on naturally contaminated milk products. It is noteworthy that when using IgG rabbit treatment, both kits can be considered as equivalent to detect enterotoxins in naturally contaminated milk products.



Conclusions:  This study demonstrated that the Vidas SET2 performance is similar to that of Transia plate SET kit, when a rabbit IgG treatment step is used before detection step. This additional treatment significantly decreased, from 42% to 8%, the rate of positive deviations observed using the Transia plate SET detection kit.



Significance and Impact of the Study:  The Vidas SET2 was clearly found as more specific, when no preliminary rabbit IgG treatment was used, and which results in a better workflow when a large number of samples have to be analysed within a few days. Considering the results obtained, the Vidas SET2 detection kit can be used to assess the safety of milk products for SEs.

Intralaboratory validation according to the EN ISO 16 140 Standard of the Vidas SET2 detection kit for use in official controls of staphylococcal enterotoxins in milk products.

Aim: To determine the performance of the Ridascreen® SET Total kit, after sample extraction and concentration by dialysis, with regard to its use in official controls for staphylococcal enterotoxins under European Regulation (EC) No. 2073/2005 modified. This study was conducted on naturally contaminated cheese samples and compared with the results of the previously validated Vidas® SET2 kit.



Methods and Results:  The effectiveness of the Ridascreen® SET Total kit on naturally contaminated cheeses was compared to that of the Vidas® SET2 kit by applying the EN ISO 16140 standard. Sensitivity and specificity were also compared using spiked buffer solutions and cheese samples with SEA to SEE toxins.



Conclusions:  This study showed that the Ridascreen® SET Total kit is as effective as the Vidas® SET2 kit.



Significance and Impact of the Study:  The Ridascreen® SET Total kit was found to specifically detect SEA to SEE in cheeses. The Ridascreen® SET Total can therefore be used to check the staphylococcal enterotoxin content and ensure consumer protection.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1472-765X.2011.03025.x

Intra-laboratory validation of the Ridascreen® SET Total kit for detecting staphylococcal enterotoxins SEA to SEE in cheese.

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Intralaboratory validation according to the EN ISO 16 140 Standard of the Vidas SET2 detection kit for use in official controls of staphylococcal enterotoxins in milk products.

Intra-laboratory validation of the Ridascreen® SET Total kit for detecting staphylococcal enterotoxins SEA to SEE in cheese.