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Haeghebaert et al., 2002), there were 1267 FBD outbreaks, involving 17,378 persons, and causing 1383 hospitalizations, and 10 deaths.
Clostridium perfringens is the second most common causative agent of FBD in the US, after Salmonella. Bacillus cereus is a Gram-positive, facultatively aerobic, spore-forming rod (McKillip, 2000). Staphylococcus aureus is a facultative anaerobic Gram-positive coccus; it is non-motile and catalase and coagulase positive. Staphylococcus aureus strains can be classified into biotypes according to their human or animal origin. Staphylococcus aureus is an important pathogen due to a combination of toxin-mediated virulence, invasiveness, and antibiotic resistance. Genes encoding SEs have different genetic supports, most of which are mobile genetic elements (Table 4). The SEs belong to a family of the so-called pyrogenic toxins originating from staphylococcus and streptococcus species. In all cases of staphylococcal food poisoning, the foodstuff or one of the ingredients, was contaminated with an SE-producing S. The foods that are most often involved in staphylococcal food poisoning differ widely from one country to another. In any case, the main sources of contamination are humans (handlers contaminate food via manual contact or via the respiratory tract by coughing and sneezing), and contamination occurs after heat treatment of the food.
In most countries (including the USA and France, whose statistical data are given here as an example, Table 1), bacteria are the leading cause of FBD and appear to be the causative agents of more than two thirds of the recorded FBD outbreaks. Miscellaneous bacteria (including Gram positive and Gram negative ones) produce toxins that cause food-borne poisoning, resulting in symptoms ranging from gastrointestinal disorders to paralysis and death.
It is an anaerobic, Gram-positive, spore-forming rod (Brynestad and Granum, 2002) and is widely distributed in the environment (frequent in the intestines of humans and many domestic and feral animals).
Cells are spherical single or paired cocci, or form grape-like clusters (staphylo means grape in greek). Devriese (1984) developed a biotype schema, including six different biotypes (human, non-b-hemolytic human, avian, bovine, ovine, and nonspecific), based on biochemical characteristics.
This bacterium is a significant cause of nosocomial infections, as well as community-acquired diseases. Pyrogenic toxins include SEs, TSST, exfoliatins A and B and streptococcus pyrogenic toxins.
The enterotoxin activity is uniquely characterized by the SE ability to cause emetic responses when administered orally to monkeys, whereas other superantigens are not emetic (Dinges et al., 2000). Effect of vitamin E supplementation on vitamin K status in adults with normal coagulation status -- Booth et al.
To date, around 250 different food-borne diseases have been described, and bacteria are the causative agents of two thirds of food-borne disease outbreaks. Bacteria causing food-borne infections have a pathogenesis centered on their ability to penetrate, survive and multiply in host cells. We give here some examples of Gram-positive bacteria, other than Staphylococcus aureus, involved in food-borne poisoning. The spores are heat resistant and can survive in foods that are incorrectly or minimally processed. The staphylococcal cell wall is resistant to lysozyme and sensitive to lysostaphin, which specifically cleaves the pentaglycin bridges of Staphylococcus spp. The spectrum of staphylococcal infections ranges from pimples and furuncles to toxic shock syndrome and sepsis, most of which depend on numerous virulence factors.
In the first SEs identified, the peptide sequence was available before the nucleo tide sequence.
Seb is chromosomally located in some clinical isolates (Shafer and Iandolo, 1978), whereas it has been found in a 750-kb plasmid in other S. SE production has been studied in strains grown in laboratory media and in diverse foodstuffs. A simplified system for biotyping Staphylococcus aureus strains isolated from different animal species. Prevalence and expression of enterotoxins in Bacillus cereus and other Bacillus spp., a literature review. Among the predominant bacteria involved in these diseases, Staphylococcus aureus is a leading cause of gastroenteritis resulting from the consumption of contaminated food. The pathogenesis of bacteria causing food-borne poisoning depends on their capacity to produce toxins after ingestion (in the digestive tract) or before (toxins preformed in foodstuff).
Clostridium perfringens causes perfringens food poisoning, the symptoms of which are intense abdominal cramps and diarrhea.
Food-borne botulism is a severe type of food poisoning caused by the ingestion of foods containing the potent neurotoxin formed during growth of the organism. On the other hand, some infections, such as staphylococcal food poisoning, rely on one single type of virulence factor: the SEs. This was the case for SEA (Huang et al., 1987), SEB (Huang and Bergdoll, 1970) and SEC (Schmidt and Spero, 1983). They have phylogenetic relationships as well (for a review, see Balaban and Rasooly, 2000). Nevertheless, estimations vary considerably from one food to another and from one report to another.
Toxin genes and other characteristics of Staphylococcus aureus isolates from milk of cows with mastitis. Penicillinase plasmid-linked genetic determinants for enterotoxins B and C1 production in Staphylococcus aureus. Nucleotide sequence of the staphylococcal enterotoxin C1 and relatedness to other pyrogenic toxins. Phage-associated differences in staphylococcal enterotoxin A gene (sea) expression correlate with sea allele class. Production of enterotoxins and toxic shock syndrome toxin by Staphylococcus aureus isolated from bovine mastitis in Brazil. Regulation of exoprotein expression in Staphylococcus aureus by a locus (sar) distinct from agr. Staphylococcus aureus bacteriophages mediating the simultaneous lysogenic conversion of d-lysin, staphylokinase and enterotoxin A: molecular mechanism of triple conversion. Estimation of human dose of staphylococcal enterotoxin A from a large outbreak of staphylococcal food poisoning involving chocolate milk.
Characterization of putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens.
Lack of complete correlation between emetic and T-cell-stimulatory activities of staphylococcal enterotoxins. Nucleotide sequence of the staphylococcal enterotoxin C3 gene: sequence comparison of all three type C staphylococcal enterotoxins. Investigation of the role of the disulphide bond in the activity and structure of staphylococcal enterotoxin C1. Application of pulse-field gel electrophoresis to the epidemiological characterization of Staphylococcus intermedius implicated in a food-related outbreak.
Differences between Danish bovine and human Staphylococcus aureus isolates in possession of superantigens.

Characterization of novel type C staphylococcal enterotoxins: biological and evolutionary implications. Identification and characterization of staphylococcal enterotoxin types G and I from Staphylococcus aureus. Combined effects of water activity, pH, and suboptimal temperature on growth and enterotoxin production.
Detection of seg, seh, and sei genes in Staphylococcus aureus isolates and determination of the enterotoxin productivities of S. Amino acid requirement for growth and enterotoxin production by Staphylococcus aureus in chemically defined media. Effect of a commercial starter culture on growth of Staphylococcus aureus and thermonuclease and enterotoxins (C1 and C2) production in broth cultures. Alkaline pH decreases expression of the accessory gene regulator (agr) in Staphylococcus aureus.
Glucose and nonmaintained pH decrease expression of the accessory gene regulator (agr) in Staphylococcus aureus. Effect of intestinal Lactobacillus starter cultures on the behaviour of Staphylococcus aureus in fermented sausage. Temperature limits of growth, TNase, and enterotoxin production of Staphylococcus aureus strains isolated from foods.
Isolation and characterization of a plasmid involved with enterotoxin B production in Staphylococcus aureus.
Detection of staphylococcal enterotoxins by enzyme-linked immunosorbent assays and radioimmunoassays: comparison of monoclonal and polyclonal antibody systems.
Staphylococcal enterotoxin A gene (sea) expression is not affected by the accessory gene regulator (agr).
Behaviour and enterotoxin production by Staphylococcus aureus during the manufacture and ripening of raw goats’ milk lactic cheeses.
The enterotoxin D plasmid of Staphylococcus aureus encodes a second enterotoxin determinant (sej).
Staphylococcal food poisoning is due to the absorption of staphylococcal enterotoxins preformed in the food. Among FBDs, food-borne infections are caused by many different disease-causing pathogens that can contaminate foods, while food-borne poisoning is caused by poisonous chemicals, or other harmful substances that are present in food. Symptoms appear 8 to 22 h after consumption of contaminated foods and are over within 24 h (1 or 2 weeks in the elderly). The symptoms of staphylococcal food poisoning are abdominal cramps, nausea, vomiting, sometimes followed by diarrhea (never diarrhea alone).
The abundance of literature on SEs varies considerably among the types, according to the chronology of their identification and their importance in staphylococcal food poisoning. Although there is considerable data on the structure-function relationships of SE superantigen activity, emetic activity has not been precisely localized. Conditions of expression of agr are so well documented because it regulates most of the virulence factors in S. Here are some examples of variations concerning strains isolated from cows with mastitis and milk products.
Here, we briefly review the latest data on staphy-lococcal enterotoxins and some papers exemplifying the interactions between S.
In many countries, national health care organizations record FBD outbreaks, defined as the occurrence of two or more cases of a similar illness resulting from the ingestion of a common food.
The incidence of the disease is low, but the disease is of considerable concern because of its high mortality rate if not treated immediately and properly. The onset of symptoms is rapid (from 30 min to 8 h) and usually spontaneous remission is observed after 24 h.
To date, 14 different SE types have been identified, which share structure and sequence similarities (Table 2). Vomiting (emetic) type of illness is caused by a low molecular weight, heat-stable peptide. The SEs are short proteins secreted in the medium and soluble in water and saline solutions. Thus, SEA to E and SEH have been clearly demonstrated as being capable of more or less potent emetic activity.
Staphylococcus aureus is considered an exigent bacterium in terms of nutritional requirements. Various examples of staphylococcal food poisoning are described in the literature (Bergdoll, 1989).
Thus, the origins of staphylococcal food poisoning differ widely among countries; this may be due to differences in the consumption and food habits in each of the countries.
In Denmark, another study performed on strains isolated from cows with mastitis found that only 1 of 414 S. Deaths in pig-bel syndrome are caused by infection and necrosis of the intestines and from resulting septicemia. More recently, increasing data resulting from partial or complete genome sequence analyses have allowed the identification of several new SE types. Valine is necessary for growth and arginine and cystine are necessary for both growth and SE production in five strains of S. In one case, cheese was involved in an outbreak because it had been made from milk contaminated after pasteurization and before inoculation with lactic starter culture. In France, for example, the consumption of raw milk cheeses is much higher than in Anglo-Saxon countries.
Botulinum toxin causes paralysis by blocking motor nerve terminals at the myoneural junction. Symptoms of the emetic type are similar to those caused by staphylococcal food-borne poisoning. These new SEs were first identified on the basis of sequence and structural similarities with existing SEs.
In this particular case, the starter culture did not grow properly, resulting in a fermentation accident that allowed the S.
This may explain the relative importance of milk products involved in staphylococcal food poisoning in France. Most of them possess a cystine loop required for proper conformation and which is probably involved in the emetic activity (discussed below). They are highly stable, resist most proteolytic enzymes, such as pepsin or trypsin, and thus keep their activity in the digestive tract after ingestion. Although pyrogenic toxins are involved in distinct pathologies, they have common biological activities: they are pyrogenic, and they cause immunosuppression and nonspecific T-cell proliferation. Glucose has been shown to have an inhibitory effect on SE production, especially for SEB and SEC (Bergdoll, 1989).
In 1985, chocolate milk was the origin of a staphylococcal food poisoning in the Kentucky, USA. In these latter studies, the authors investigated the strains for SEA to E (SEA to D for Cardoso et al.), but not for newly described SEs.
As agr expression is tightly linked to quorum sensing (Novick, 2000), the production of agr-dependent SEs in foodstuffs is dependent on the ability of S. This inhibitory effect has been attributed to a drop in pH, as a consequence of glucose metabolism.

This chocolate milk was contaminated and stored at too high a temperature for 4 to 5 h, before pasteurization. Nevertheless, it remains a major cause of FBD because it can contaminate food products during preparation and processing.
There is thus a great increase in the percentage of enterotoxigenic strains when the newly described SEs are taken into account. Staphylococcus aureus is indeed found in the nostrils, and on the skin and hair of warm-blooded animals.
Staphylococcal enterotoxin B can be destroyed by pepsin digestion at pH 2 but it is pepsin resistant at higher pHs, which are normal conditions in the stomach after food ingestion (Bergdoll, 1983).
These, and many other examples, illustrate the importance of the elimination of any contamination sources during the processing and refrigeration of food and food ingredients whenever possible.
Along with the SEA, SEC, and SED often found in these studies, SEG, SEI, and SEJ seem to be the predominant SEs in strains isolated from cattle with bovine mastitis (Akineden et al., 2001). Staphylococcus aureus can indeed be easily eliminated from foodstuffs by heat treatment (in pasteurized foods) or by competition with other flora (in fermented foods), whereas SEs resist most of the treatments used during food processing. Staphylococcal enterotoxins are highly heat resistant as well; they are thought to be more heat resistant in foodstuffs than in a laboratory culture medium (Bergdoll, 1983), but can be inactivated by heat treatments used in the sterilization of canned foods when they are present at low concentrations (Bergdoll, 1983). The products can be refrigerated before, as well as after, heat treatment (pasteurization). Great efforts have been applied to the development of detection methods for SEs, based on immunological and activity assays.
Nevertheless, a high correlation exists between these activities since, in most cases, genetic mutations resulting in a loss of superantigen activity result also in a loss of emetic activity (Harris et al., 1993). In the case of canned foods that have been correctly processed, bacteria and SEs are usually destroyed.
Although immunological assays are quicker and cheaper, the relevance of the immunological approach is still under discussion.
Superantigen activity results from direct interaction of SEs with T-cell antigen receptors (TCR) and the major histocompatibility complex (MHC) of antigen-presenting cells (APC). Nevertheless, some cases of staphylococcal food poisoning involving canned mushrooms that were correctly processed were reported in the USA (Bennet, 1992).
Heat treatment in an acidic medium usually leads to a loss of immunological activity and a concomitant loss of biological activity. A normal antigen is presented to TCR in the form of peptides bound to MHC class I or II, after processing in APC (Figure 1A).
For example, acetic acid has a greater inhibitory effect than lactic acid on SE production. Nevertheless, data based on PCR-based detection of SE genes (including the newly described genes) has to be examined with precaution.
This, plus their ecological niche, can easily explain their incidence in foodstuffs that require manipulation during processing, including fermented food products, such as cheeses. Nevertheless, SEA and SED were found to be undetectable (loss of serological recognition) but still active (in kittens in an in vivo assay) after heat treatment (Bennet, 1992). High concentrations of sodium chloride increase the inhibitory effect of acidic pH, with no SE production at salt concentrations above 12%, independent of the pH (Notermans and Heuvelman, 1983). Sandwich enzyme-linked immunosorbent assays (ELISA) have been developed for SEA to SEE (Thompson et al., 1986), and are commercially available. Thus considerable research effort is still required for better understanding of the interactions between S. Heat inactivation of SEA, SEB, and SEC has been shown to vary according to the food matrix and to the pH (Schwabe et al., 1990). T-cell antigen receptors are glycosylated heterodimers composed either of a and b, or of d and g chains.
On the other hand, alkaline pH also decreases the production of SEB, SEC, and SED via decreased expression of agr (Regassa and Betley, 1992). Most of the studies on SEA to SEE demonstrate a good correlation between the occurrence of the sea to see genes and the production of the corresponding SEs. It is thus quite difficult to foresee the impact of heat treatment on SE activity, since it depends on SE type, SE concentration and the food matrix. This recognition of the antigen is a primary step in the cellular immune response and is a key to the high specificity of the immune response.
Research is also needed for the identification of new SEs and of new enterotoxigenic staphylococci. Furthermore, in some cases, heat inactivation is spontaneously reversible by an alkaline pH (Schwabe et al., 1990) or by urea treatment (Bennet, 1992). Only a few T-cells can recognize a specific antigen presented in the MHC of an APC (McCormick et al., 2001). Recently, ELISA for SEH (Su and Wong, 1996), and for SEG and SEI have been described (Omoe et al., 2002). Much effort is being applied towards the development of new, and more sensitive methods for SE detection in foodstuffs. Taken together, these data show that SEs resist conditions (heat treatment, low pH) that easily destroy the bacteria that produced them. Superantigen toxins interact with many T-cells by the recognition of specific Vb chains of the TCR. Genigeorgis (1989) demonstrated that the higher the concentration of competing microorganisms in milk, the lower the rate of S.
One strain producing SEH has already been involved in some staphylococcal food poisoning (Su and Wong, 1996), and most seh-harboring strains produce significant amounts of SEH.
Taken together, these studies should lead to better control and a subsequent reduction of staphylococcal food poisoning outbreaks.
They are able to cross-link the TCR and the MHC class II of APC, thus causing activation (Figure 1B). It seems that an interaction between SE and MHC is first required for binding to the Vb chain of the APC.
This cross-link results in the nonspecific activation and proliferation of T-cells and a massive secretion of interleukins that may be involved in the mechanism of SE toxicity. The effect of lactic acid starter is mainly due to lactic acid production, lowered pH, oxygen peroxide production, competition for nutrients and is sometimes due to the synthesis of antimicrobial substances, such as bacteriocins. This demonstrates the importance of quantitative assessment of SE production in foods in order to have a clear idea of the relationship between the recently described SEs and food poisoning. Through this interaction, SEs activate T-cells at orders of magnitude above antigen-specific activation. Thus, recent PCR-based studies demonstrate that newly described SE genes are widely distributed among S. The domains of SE involved in these interactions are well characterized through genetic and crystallographic studies.
SEB-producing strains are considered as potential microbiological weapons of warfare and terrorism (Greenfield et al., 2002).

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