• coagulase-positive staphylococci;
  • staphylococcal enterotoxins;
  • staphylococcal food poisoning


  1. Top of page
  2. Abstract
  3. A worldwide review of outbreaks related to coagulase-positive staphylococci and their toxins: the story
  4. Characteristics and behaviour of S. aureus in the food environment
  5. Toxinogenic conditions and characteristics of SEs
  6. SFPOs: symptomatology; reporting system including EU control; monitoring schemes; occurrence and analytical methods used
  7. Concluding remarks
  8. References
  9. Supporting Information

Staphylococcal food poisoning (SFP) is one of the most common food-borne diseases and results from the ingestion of staphylococcal enterotoxins (SEs) preformed in food by enterotoxigenic strains of Staphylococcus aureus. To date, more than 20 SEs have been described: SEA to SElV. All of them have superantigenic activity whereas half of them have been proved to be emetic, representing a potential hazard for consumers. This review, divided into four parts, will focus on the following: (1) the worldwide story of SFP outbreaks, (2) the characteristics and behaviour of S. aureus in food environment, (3) the toxinogenic conditions and characteristics of SEs, and (4) SFP outbreaks including symptomatology, occurrence in the European Union and currently available methods used to characterize staphylococcal outbreaks.

A worldwide review of outbreaks related to coagulase-positive staphylococci and their toxins: the story

  1. Top of page
  2. Abstract
  3. A worldwide review of outbreaks related to coagulase-positive staphylococci and their toxins: the story
  4. Characteristics and behaviour of S. aureus in the food environment
  5. Toxinogenic conditions and characteristics of SEs
  6. SFPOs: symptomatology; reporting system including EU control; monitoring schemes; occurrence and analytical methods used
  7. Concluding remarks
  8. References
  9. Supporting Information

Staphylococcal food poisoning (SFP) is one of the most common food-borne diseases in the world following the ingestion of staphylococcal enterotoxins (SEs) that are produced by enterotoxigenic strains of coagulase-positive staphylococci (CPS), mainly Staphylococcus aureus (Jablonski & Bohach, 1997) and very occasionally by other staphylococci species such as Staphylococcus intermedius (Genigeorgis, 1989; Khambaty et al., 1994).

When outbreaks occurred during large social events, chaotic situations resulted requiring the rapid implementation of medical care for a high number of cases (Bonnetain et al., 2003; Do Carmo et al., 2004).

Here are some examples of SFP outbreaks (SFPOs).

The first description of food-borne disease involving staphylococci was investigated in Michigan (USA) in 1884 by Vaughan and Sternberg. This food poisoning event was because of consumption of a cheese contaminated by staphylococci. The authors stated: ‘It seems not improbable that the poisonous principle is a ptomaine developed in the cheese as a result of the vital activity of the above-mentioned Micrococcus or some other microorganisms which had preceded it, and had perhaps been killed by its own poisonous products’.

Ten years later, Denys (1894) concluded that the illness of a family who had consumed meat from a cow that had died of vitullary fever was owing to the presence of pyogenic staphylococci.

In 1907, Owen recovered staphylococci from dried beef involved in an outbreak showing characteristics of SFP symptomatology (Dack et al., 1930).

Proof of the involvement of staphylococci in food poisoning was first brought by Barber in 1914. He demonstrated with certainty that staphylococci were able to cause poisoning by his consumption of unrefrigerated milk from a cow suffering from mastitis, an inflammation owing to staphylococci. However, the correlation between staphylococci-containing food and symptomatology was not recognized until other examples of food poisoning occurred later in the twentieth century. It was Baerthlein, when reporting on a huge outbreak involving 2000 soldiers of the German army during WWI, who established in 1922 the possible role of bacteria. ‘I am going to report the case of an extended demonstration of poisoned sausages (approximately 2000 cases) held in the spring 1918 during the military campaign of Verdun, which would probably have catastrophic military consequences. Early in June 1918, sudden and massive demonstrations that have the appearance of an acute and in some cases severe gastroenteritis, similar to cholera, affected the troops around Verdun; entire companies were disabled except just a few people, and within two days about 2000 men had been affected. The symptoms were so severe that some troops (more than 200) had to be transferred to field hospitals. The suspicion of food poisoning has been mentioned because, according to reports of the sick, the disease occurred 2 or 3 hours (some of the symptoms appeared after 6 to 8 hours) after eating a dish of sausages. Only troops who did not eat the meal were spared, such as soldiers who had returned to headquarters to receive orders, soldiers who for other reasons had not eaten sausages, and soldiers who were on leave and/or following a different diet. However, it was surprising that among the troops that were not present at the front, such as butchers, who ate the same sausage two days earlier, we did not observe any cases of disease’.

In 1930, Dack et al. found that a sponge cake was responsible for the intoxication of 11 individuals; he highlighted that the disease was probably linked to a toxin called ‘enterotoxin’ produced by yellow haemolytic Staphylococcus. Broth culture filtrates of this strain were administrated intravenously to a rabbit and orally to three human volunteers. The rabbit died, after first developing water diarrhoea, and the three volunteers developed nausea, chilliness and vomiting after 3 h. In the same year, Jordan showed that various strains of staphylococci exhibited cultural properties of generating a substance which was purified from broth and, when taken orally, produced gastrointestinal disturbance.

A few years later, in 1934, Jordan and Burrows observed nine outbreaks related to the presence of staphylococci in food remnants, whereas Dolman (1934) explained that ‘the food poisoning substance is probably produced by only a few strains of staphylococci, and that it is a special metabolite whose formation and excretion are favored in the laboratory by such environmental conditions as a semi-fluid medium and atmosphere containing a high percentage of carbon dioxide, conditions which promote, respectively, abundant growth and increased cellular permeability with partial buffering’.

One of the first well-documented SFP outbreaks was described by Denison in 1936. This outbreak occurred among high school students after they had eaten tainted cream puffs. He depicted the typical symptoms of 122 cases as follows: ‘Within 2–4 hours after eating there was first noticed a feeling of nausea. Severe abdominal cramps developed and were quickly followed by vomiting which was severe and continued at 5–20 minute intervals for 1–8 hours […] A diarrhea of 1–7 liquid stools usually began with the vomiting and continued for several hours after its onset […] During the acute stage the temperature was normal or subnormal, the pulse noticeably increased, there were cold sweats, prostration was severe and the patients were very definitely in a state of shock. Headache was mild and of a short duration. Muscular cramping […] was present in the majority. Dehydration was marked in some. While the acute symptoms usually lasted only 1–8 hours, complete recovery […] was delayed for 1–2 days’.

Staphylococcal food poisoning symptomatology has been extensively studied especially by the US Army: in a naturally occurring outbreak among US Army personnel, involving 400 of 600 men, DeLay (1944) reported that about 25% of cases were classified as severe or shock cases. Numerous SFP outbreaks have been described since the end of WWII. For example, Brink & Van Metter (1960) from the Institute for Cooperative Research of the University of Pennsylvania wrote a long report on an outbreak of SE food poisoning which happened in 1960: ‘On a Saturday afternoon in the middle of summer, an epidemic of staphylococcal enterotoxin food poisoning occurred at a picnic held two miles from Gabriel, a small Midwestern town. (The name of the town and other names in this report are fictitious, in accordance with commitments to Task Surprise respondents.) About 1700 persons attended the picnic, which is an annual affair sponsored by the Johnson Co., of Croydon, some 60 miles away. Early in the morning, approximately seven hours before the picnic began, an unventilated, unrefrigerated truck containing a large supply of ham sandwiches was parked at the picnic grounds. The truck was exposed to the heat of direct sunlight, while the average ambient temperature for the day was close to 100 degrees Fahrenheit. In this environment, the staphylococcal organisms which elaborate the toxin multiplied rapidly. During the epidemic that followed, approximately 1100 persons became ill ’. A selection of 24 outbreaks involving SEs is presented in Table 1.

Table 1. Excerpt of food poisonings presented in the literature
YearLocationIncriminated foodNumber of casesReferences
1968School children, TexasChicken salad1300Anonymous (1968)
1971UK armySausages rools, ham sandwiches100Morris et al. (1972)
1975Flight from Japan to DenmarkHam197Eisenberg et al. (1975)
1976Flight from Rio to NYCChocolate eclairs80Anonymous (1976)
1980CanadaCheese curd62Todd et al. (1981)
1982North Carolina and PennsylvaniaHam and cheese sandwich; stuffed chicken121Anonymous (1983a)
1983Caribbean cruise shipDessert cream pastry215Anonymous (1983b)
1984ScotlandSheep's milk cheese27Bone et al. (1989)
1985France, UK, Italy, LuxembourgDried lasagna50Woolaway et al. (1986)
1985School children, Kentucky2% chocolate milk> 1000Evenson et al. (1988)
1986Country Club, New MexicoTurkey, poultry, gravy67Anonymous (1986)
1989Various US statesCanned mushrooms102Anonymous (1989)
1990ThailandEclairs485Thaikruea et al. (1995)
1992Elementary school, TexasChicken salad1364Anonymous (1992)
1997Retirement party, FloridaPrecooked ham18Anonymous (1997)
1998Minas Gerais, BrazilChicken, roasted beef, rice and beans4000Do Carmo et al. (2004)
2000Osaka, JapanLow-fat milk13 420Asao et al. (2003)
2006Ile de France area, FranceCoco nut pearls (Chinese dessert)17Hennekinne et al. (2009)
2007Scouts’ camp, BelgiumHamburger15Fitz-James et al. (2008)
2007Elementary school, AustriaMilk, cacao milk, vanilla milk166Schmid et al. (2009)
2008Weeding dinner, Ile de France area, FranceCarribean meals47

De Buyser & Hennekinne,

pers. commun.

2008French districtPasta salad100

De Buyser & Hennekinne,

pers. commun.

2009Nagoya university festival, JapanCrepes75Kitamoto et al. (2009)
2009Various districts, FranceRaw milk cheese23Ostyn et al. (2010)

The main point highlighted by these reports is that any food that provides a convenient medium for CPS growth may be involved in a SFP outbreak (SFPO). The foods most frequently involved differ widely from one country to another, probably due to differing food habits (Le Loir et al., 2003). For instance, in the UK or the United States, meat or meat-based products are the food vehicles mostly involved in SFP (Genigeorgis, 1989), although poultry, salads and cream-filled bakery items are other good examples of foods that have been involved (Minor & Marth, 1972). In France, various food types have been associated with SFPOs but as the consumption of unpasteurized milk cheeses is much more common than in Anglo-Saxon countries, milk-based products are more frequently involved than in other countries (De Buyser et al., 2001).

To conclude this section, as SFP is a short-term disease and usually results in full recovery, doctors do not take it very seriously, especially when the outbreak affects only a few people. Although such outbreaks should be reported to the sanitary authorities, this situation leads to under-reporting (De Buyser et al., 2001). However, many researchers consider that SFP is one of the most common food-borne diseases worldwide (Balaban & Rasooly, 2000).

Characteristics and behaviour of S. aureus in the food environment

  1. Top of page
  2. Abstract
  3. A worldwide review of outbreaks related to coagulase-positive staphylococci and their toxins: the story
  4. Characteristics and behaviour of S. aureus in the food environment
  5. Toxinogenic conditions and characteristics of SEs
  6. SFPOs: symptomatology; reporting system including EU control; monitoring schemes; occurrence and analytical methods used
  7. Concluding remarks
  8. References
  9. Supporting Information

Staphylococcus is a spherical, nonsporulating, nonmotile bacterium (coccus) that, when observed under the microscope, occurs in pairs, short chains or grape-like clusters. These facultative aero-anaerobic bacteria are Gram- and catalase positive. Staphylococci are ubiquitous in the environment and can be found in the air, dust, sewage, water, environmental surfaces, humans and animals.

To date, more than 50 species and subspecies of staphylococci have been described according to their potential to produce coagulase. Their classification thus distinguishes between coagulase-producing strains, designated as coagulase-positive staphylococci (CPS) and noncoagulase-producing strains, called coagulase-negative staphylococci (CNS). Among CNS, some species are known to play an important role in the fermentation of meat and milk-based products and are therefore considered as food grade. The enterotoxigenic potential of CNS has always been a subject of controversy. Several investigations failed to detect enterotoxin production or enterotoxin-like gene in CNS (Rosec et al., 1997; Becker et al., 2001). However, some studies found that certain CNS strains were able to produce enterotoxins which could lead to food poisoning (Vernozy-Rozand et al., 1996; Zell et al., 2008). More recently, another study demonstrated that, among 129 CNS strains isolated from fermented foodstuffs, only one carried SE genes (Even et al., 2010). However, as only CPS strains have been evidenced in food poisoning incidents, this review will focus on these species.

Among the seven described species belonging to the CPS group (Table 2), S. aureus ssp. aureus is the main causative agent described in SFPOs. Among other CPS, Becker et al. (2001) highlighted the enterotoxigenic potential of S. intermedius. The enterotoxigenic potential (particularly for SEC) of this species has been shown in strains isolated from dogs (Hirooka et al., 1988). The presence in the environment of strains producing toxins raises a possible health hazard, especially when carried by animals such as dogs that come in close contact with humans. Staphylococcus intermedius was involved in one outbreak caused by blended margarine and butter involving over 265 cases in October 1991 in the United States (Khambaty et al., 1994; Bennett, 1996).

Table 2. Genus Staphylococcus: coagulase-positive species
SpeciesMain sourcesReferences
  1. a

    Staphylococcus intermedius, S. pseudintermedius and S. delphini are very close species also called the S. intermedius group. Staphylococcus pseudintermedius is now considered as the main species isolated from dogs.

S. aureus ssp. aureusHumans, animalsRosenbach (1884)
S. aureus ssp. anaerobiusSheepDe la Fuente et al. (1985)
S. intermediusaDog, horse, mink, pigeonHajek (1976)
S. pseudintermediusaDog, catDevriese et al. (2005)
S. delphiniaDolphinVaraldo et al. (1988)
S. schleiferi ssp. coagulansDog (external ear)Igimi et al. (1990)
S. lutraeOtterFoster et al. (1997)


Staphylococcus aureus belongs to the normal flora found on the skin and mucous membranes of mammals and birds. This bacterium can be disseminated in the environment of its hosts and survives for long periods in these areas. Several biotypes isolated from different hosts (human, poultry, cattle and sheep/goat) have been described within S. aureus species demonstrating the close adaptation of the bacterium to its host. They were identified according to four biochemical tests (staphylokinase, ß-haemolysin production, coagulation of bovine plasma and growth type on crystal violet agar) following the simplified biotyping scheme described by Devriese (1984). However, many strains cannot be assigned to these host-specific biotypes and belong to nonhost-specific (NHS) biotypes, i.e., those associated with several hosts. Later, a poultry-like biotype associated with meat products and meat workers was tentatively designated as a ‘slaughterhouse’ biotype by Isigidi et al. (1990). Indeed, introduction of an additional biochemical test, protein A production, and phage typing allowed researchers to differentiate the poultry biotype from this new biotype. However, as the protein A test is no longer commercially available, and as phage typing cannot be routinely used, these two biotypes cannot be easily distinguished. Several pitfalls were encountered when applying the biotyping method: discordant results owing to the variety of test parameters, lack of standardized reagents, problematic interpretation for ‘haemolysin’, ‘bovine plasma coagulation’ and ‘crystal violet’ tests when applied to some strains and, as previously mentioned, lack of commercially available tests to distinguish between the described biotypes. Despite these drawbacks, S. aureus biotyping has been useful in tracing or estimating the origin of this organism in various food products (Devriese et al., 1985; De Buyser et al., 1987; Rosec et al., 1997), in the food industry (Isigidi et al., 1990) and also for epidemiological investigations of food-poisoning outbreaks (Hennekinne et al., 2003; Kerouanton et al., 2007). In a recent study, Alves et al. (2009) performed pulsed-field gel electrophoresis (PFGE) typing of S. aureus strains isolated from small (n = 88) and large ruminants (n = 65). The authors carried out a molecular analysis and confirmed that ovine and caprine strains which could not be distinguished from one another were nonetheless different from bovine strains. To suggest the source of contamination (animal or human origins), molecular-based methods have been used by various authors to study the food poisoning outbreaks (Chiou et al., 2000; Shimizu et al., 2000; Wei & Chiou, 2002; Kerouanton et al., 2007; Ostyn et al., 2010). Among these methods, PFGE and the Staphylococcus protein A gene (spa) typing have been used alone or in association providing additional information to highlight the origin of the S. aureus contamination.

Means of contamination

The prerequisite of SFP is that food or one of its ingredients is contaminated with an enterotoxigenic strain of Staphylococcus spp. Moreover, to induce SFP, conditions for staphylococci growth and enterotoxin production are needed.

Five conditions are required to induce SFPOs: (1) a source containing enterotoxin-producing staphylococci: raw materials, healthy or infected carrier, (2) transfer of staphylococci from source to food, e.g., unclean food preparation tools because of poor hygiene practices, (3) food composition with favourable physicochemical characteristics for S. aureus growth and toxinogenesis, (4) favourable temperature and sufficient time for bacterial growth and toxin production, and (5) ingestion of food containing sufficient amounts of toxin to provoke symptoms. Most SFPOs arise because of poor hygiene practices during processing (Asao et al., 2003), cooking or distributing the food product (Pereira et al., 1996). Moreover, after contamination, inadequate cooling of foods can induce Staphylococcus growth and/or stimulate toxin production, resulting in food poisoning (Barber, 1914; Anonymous, 1997).

Staphylococci are commonly found in a wide variety of mammals and birds, and transfer of S. aureus to food has two main sources: human carriage during food processing and dairy animals in case of mastitis. Human strains are mainly involved in SFPOs. However, animals are also known to be a potential source of primary contamination. For example, in the case of staphylococcal mastitis of ruminants such as cows, goats or ewes, S. aureus can be carried over from the udder into the milk. In a study conducted on 178 S. aureus strains associated with 31 SFPOs isolated, Kerouanton et al. (2007) demonstrated for the first time that animal strains were responsible for two outbreaks.

Numerous examples of SFPO are described in the literature of the last few decades (Table 1). Among these examples, the case which happened in 1997 in Florida (USA) during the course of a retirement party where precooked ham was served (Anonymous, 1997) provides an interesting demonstration of the five conditions needed to cause SFPO: on 27 September 1997, a community hospital in North-eastern Florida (USA) notified the Health Department about several persons who were treated in the emergency room because of gastrointestinal illnesses suspected of being associated with a common meal ingested on 26 September 1997.

On September 25, a food preparer had purchased a 16-pound precooked packaged ham, baked it at home at 204 °C for 1.5 h, and transported it to her workplace, a large institutional kitchen; finally, she sliced the ham while it was hot with the help of a commercial slicer. The food preparer declared that she had no cuts, sores or infected wounds on her hands. She reported that she routinely cleaned the slicer in place rather than dismantling it and cleaning it according to recommended procedures and that she did not use an approved sanitizer. All 16 pounds of sliced ham were placed in a 14-inch by 12-inch by 3-inch plastic container that was covered with foil and stored in a walk-in cooler for 6 h and then transported back to the preparer's home and refrigerated overnight. The ham was served cold at the party the next day. The leftover food was collected and submitted for laboratory analysis. Of the approximately 125 persons who attended the party, 98 completed and returned questionnaires. Of these, 31 persons attended the event but ate nothing, and none of them became ill; they were excluded from further analysis. A total of 18 (19%) persons had illnesses meeting the case definition, including 17 party attendees and one person who ate food brought home from the party. Eighteen persons reported nausea (94%), vomiting (89%), diarrhoea (72%), weakness (67%), sweating (61%), chills (44%), fatigue (39%), myalgia (28%), headache (11%) and fever (11%). Onset of illness occurred at a mean of 3.4 h after eating (range: 1–7 h); symptoms lasted a median of 24 h (range: 2–72 h). Seven persons sought medical treatment, and two of those were hospitalized overnight. Illness was strongly associated with the eaten ham (risk ratio = 26.8). Of the 18 ill persons, 17 (94%) had eaten ham. The ill person who had not attended the party had eaten only leftover ham. None of the other foods served at the party were significantly associated with illness. One sample of leftover cooked ham and one sample of leftover rice pilaf were analysed by reversed passive latex agglutination (RPLA) to identify SE and were positive for SEA.

Potential for methicillin-resistant Staphylococcus aureus (MRSA) contamination and transmission

Food is also an important factor for the transfer of antimicrobial resistance. Such transfer can occur by means of residues of antibiotics in food, through the transfer of resistant food-borne pathogens or through the ingestion of resistant strains of the original food microflora and resistance transfer to pathogenic microorganisms (Khan et al., 2000; Pesavento et al., 2007). Most animals may be colonized with S. aureus, but only recently MRSA strains were isolated from several food production animals, including pigs, cattle, chicken and other animals (Huijsdens et al., 2006; de Neeling et al., 2007). Pigs in particular, and also pig farmers and their families, were found colonized with MRSA, and in the Netherlands, contact with pigs is now recognized as a risk factor for MRSA carriage (Van Duijkeren et al., 2007). An association between the emergence of MRSA strains in pigs and the use of antibiotics in pig farming has been suggested (de Neeling et al., 2007; Wulf & Voss, 2008). During slaughtering of MRSA-positive animals, contamination of carcasses and the environment with MRSA may occur, and consequently, meat from these animals may become contaminated. MRSA strains have been detected in different foods, including bovine milk and cheese (Normanno et al., 2007), meat products (Van Loo et al., 2007; de Boer et al., 2008) and raw chicken meat (Kitai et al., 2005; Kwon et al., 2006). These studies highlighted low isolation frequencies for MRSA in foods. Kitai et al. (2005) isolated two MRSA strains (0.5%) from 444 raw chicken meat products sampled in supermarkets in Japan. A study in Korea, including 930 slaughterhouse and retail meat samples, showed the presence of MRSA in two chicken meat samples (0.2%) but not in any pork or beef samples (Kwon et al., 2006). In an Italian survey of 1634 foodstuff samples, six (0.4%) MRSA strains were isolated from bovine milk and cheese (Normanno et al., 2007) whereas Van Loo et al. (2007) found two (2.5%) MRSA strains in 79 samples of raw pork and beef.

Regarding the involvement of MRSA in SFP, Jones et al. (2002) reported for the first time an outbreak of gastrointestinal illness caused by community-acquired MRSA. In this outbreak, various S. aureus strains were isolated from food remnants, affected people and food handlers. Among these strains, one produced staphylococcal enterotoxin C and was identified as being MRSA. This isolate was resistant to penicillin and oxacillin but sensitive to all other antibiotics tested. To our knowledge, only few data are available on the occurrence of MRSA in SFP. In a study carried out in France on foods incriminated in SFPOs, Kerouanton et al. (2007) highlighted two MRSA strains of the 33 tested. They concluded that with reference to human clinical isolates, the SFPO strains were more susceptible to antibiotics (except for two that were resistant to methicillin).

Factors influencing the growth of CPS

Microorganisms in foods are affected by a multiplicity of parameters described as intrinsic and extrinsic factors and processing effects. Some of these parameters will be discussed later. However, it should be stressed that, in complex media such as foods, these factors interact with a great extent. Many of the data presented here were derived from laboratory experiments in which all other conditions beside the factor to be tested were ideal. Table 3 summarizes some of the factors affecting growth and SE production by S. aureus.

Table 3. Factors affecting growth and enterotoxin production by Staphylococcus aureus (Tatini, 1973)
 Organism growthStaphylococcal enterotoxin production
  1. a

    Aerobic (anaerobic 0.90 [RIGHTWARDS ARROW]0.99).

  2. b

    Aerobic (anaerobic 0.92 [RIGHTWARDS ARROW] 0.99).

Water activity (aW)0.980.83 [RIGHTWARDS ARROW]0.99a0.980.85 [RIGHTWARDS ARROW]0.99b
NaCl (%)00–2000–10
Redox potential (Eh)> +200 mV< −200 mV to > +200 mV> +200 mV< −100 mV to > +200 mV
AtmosphereAerobicAnaerobic–aerobicAerobic (5–20% dissolved O2)Anaerobic–aerobic
Water activity (aw)

With regard to staphylococci, water activity (aw) is of great importance because these bacteria are able to grow over a much wider aw range than other food-associated pathogens. As can be seen from Table 3, the bacteria can grow at a minimum aw of 0.83–0.86 (equivalent to about 20% NaCl; Troller & Stinson, 1975) provided that all other conditions are optimal. The optimum aw is > 0.99 (Smith et al., 1983). The aw conditions for SE production are somewhat different than those for growth, depending on the type of toxin. SEA and SED production occurs under nearly all aw conditions allowing growth of S. aureus as long as all other conditions are optimal. Production of SEB is very sensitive to reductions in aw and hardly any is produced at aw 0.93 despite extensive growth. The effect of aw on SEC production follows the same pattern as SEB production (Ewald & Notermans, 1988; Qi & Miller, 2000). Thota et al. (1973) found SEE production in media containing 10% NaCl (according to Troller, 1971; this concentration corresponds to aw 0.92). Important factors affecting growth and SE production are also the humectant used to lower the aw, the pH, the atmospheric composition and also the incubation temperature (Table 3). Thus, conditions for growth and SE production in laboratory media and in food, respectively, may differ to some extent. Studies on the osmoadaptive strategies of S. aureus have revealed that when the cells are grown in a low aw medium, they respond by accumulating certain low molecular weight compounds termed compatible solutes. Glycine betaine, carnitine and proline have been shown to be principal compatible solutes accumulated within osmotically stressed S. aureus cells, and their accumulation results from sodium-dependent transport systems (Gutierrez et al., 1995; Qi & Miller, 2000). There is strong evidence that compatible solutes stimulate not only growth but also toxin synthesis. For example, SEB production was significantly stimulated at low aw when proline was available in the broth (Qi & Miller, 2000).


Most staphylococcal strains grow at pH values between 4 and 10, with the optimum being 6–7 (Table 3). When the other cultural parameters became nonoptimal, the pH range tolerated is reduced. For example, the lowest pH that permitted growth and SE production by aerobically cultured S. aureus strains was 4.0, while the lowest pH values that supported growth and SE production in anaerobic cultures were 4.6 and 5.3 (Smith et al., 1983). Other important parameters influencing the response of S. aureus to pH are the size of inoculum, the type of growth medium, the NaCl concentration (aw), the temperature and the atmosphere (Genigeorgis, 1989). The majority of S. aureus strains tested produced detectable amounts of SE aerobically at a pH of 5.1. However, in anaerobic conditions, most strains failed to produce detectable SE below pH 5.7 (Tatini, 1973; Bergdoll, 1989; Smith et al., 1983).

Redox potential

Optimum redox potential and ranges for growth and SE formation are given in Table 3. Staphylococcus aureus is a facultative anaerobic bacterium that grows best in the presence of oxygen. Under anaerobic conditions, however, growth is much slower, and even after several days, cell numbers do not reach those attained under aerobic conditions. Thus, aerated cultures produced approximately 10-fold more SEB than cultures incubated in an atmosphere of 95% N2 + 5% CO2. Similarly, greatly increased SEA, SEB and SEC production was observed in shaken as compared to static cultures. The level of dissolved oxygen plays a very important role (Bergdoll, 1989; Genigeorgis, 1989). Under strict anaerobic conditions, the growth of S. aureus was slower than when cultivated aerobically. In broth incubated at 37 °C, the anaerobic generation time was 80 min, compared with 35 min for aerobic culture. With slower anaerobic growth, relatively less SEA was produced than under aerobic conditions, but in both cases, toxin was detected after 120 min of incubation (Belay & Rasooly, 2002). It has already been mentioned that minimum aw and minimum pH for growth as well as for SE formation are influenced by the atmosphere.


Staphylococcus aureus grows between 7 and 48 °C, temperature being optimal at around 37 °C (Table 3). The effect of temperature depends on the strain tested and on the type of the growth medium. In an extensive study (Schmitt et al., 1990) using 77 strains isolated from different foods, the optimum growth temperature generally did not vary much within the range of 35–40 °C. The minimum growth temperatures were irregularly distributed between 7 and 13 °C and the maximum between 40 and 48 °C. The minimum temperatures for SE production varied quite irregularly over a broad range between 15 and 38 °C and the maximum temperatures from 35 to 45 °C. For the lower temperature limit for SE production, production of low amounts of toxin has been observed after 3–4 days. Moreover, SE formation at 10 °C was reported by Tatini (1973) (Table 3) without indicating the detailed experimental conditions.

One of the most effective measures for inactivating S. aureus in food is heating. The bacterium is killed in milk if proper heat treatment is applied. Staphylococcus aureus was completely inactivated in milk after application of the following temperature/time conditions: 57.2 °C/80 min, 60.0 °C/24 min, 62.8 °C/6.8 min, 65.6 °C/1.9 min and 71.7 °C/0.14 min (Bergdoll, 1989). In the case of heat inactivation in other dairy products, however, one should keep in mind that staphylococci probably become more heat resistant as the aw is lowered until at an aw between 0.70 and 0.80, and the resistance begins to decline (Troller, 1986).

Nutritional factors and bacterial antagonism

Growth of S. aureus and SE production is also influenced by nutritional factors. Some data are given in Table 4.

Table 4. Effect of nutritional factors on staphylococcal enterotoxin (SE) production by Staphylococcus aureus
FactorMediumEnhancementNo effectRepressionReferences
Magnesium (0.4–1.5 mM)Amino acid-salt-vitaminsSEB  Keller et al. (1978)
Phosphate (15–45 mM) SEB  
Potassium (30 mM)SEB   
Ammonium SEB  
Trace elements SEB  



BHI (or yeast extract) + N-Z Amine NAK





 Morita et al. (1979)
Hydrolyzed caseinCasein-based mediumSEB  Bergdoll (1989)
YeastNot definedSEA, SED  Halpin-Dohnalek & Marth (1989)
Glucose (≥ 0.30%)Casein hydrolysate medium, suppl. (pH controlled)  SEBMorse et al. (1969)
Glucose, glycerolAmino acid medium (pH controlled)  SEA, SEB, SECJarvis et al. (1975)
Lactose, maltose, sucrose, glucose, glucose + fructose (all 1% and 5%)Casein hydrolysate medium SEC Woodburn et al. (1978)
Proline, histidine, alanine, serine,Salts-vitamin-amino acid medium (amino acids individually added, 10 mM)SEB (weak)   
Aspartate, glycine, threonine, glutamateSalts-vitamin-amino acid medium (amino acids individually added, 10 mM)  SEBSmith et al. (1983)
PyruvateCasein hydrolysate medium  SEBSmith et al. (1983)

Staphylococcus aureus does not grow well in the presence of a competitive flora. Its inhibition is mainly because of acidic products, lowering of the pH, production of H2O2 or other inhibitory substances like antibiotics, volatile compounds or nutritional competition (Haines & Harmon, 1973; Genigeorgis, 1989). Important factors affecting the degree of inhibition are the ratio of the numbers of competitors to the number of S. aureus as well as the temperature (Smith et al., 1983; Genigeorgis, 1989).

Starter cultures used in the production of fermented milk products such as cheese, yoghurt, buttermilk and others can effectively prevent the growth of S. aureus and SE formation. In the case of a failure of these cultures, however, the pathogen will not be inhibited and the product may be hazardous.

Toxinogenic conditions and characteristics of SEs

  1. Top of page
  2. Abstract
  3. A worldwide review of outbreaks related to coagulase-positive staphylococci and their toxins: the story
  4. Characteristics and behaviour of S. aureus in the food environment
  5. Toxinogenic conditions and characteristics of SEs
  6. SFPOs: symptomatology; reporting system including EU control; monitoring schemes; occurrence and analytical methods used
  7. Concluding remarks
  8. References
  9. Supporting Information

Nomenclature and structure

Since the first characterization of SEA and SEB in 1959 to 1960 by Casman and Bergdoll, 22 different SEs have been described (Table 5); they are designated SEA to SElV2, in the chronological order of their discovery except for SEF which was later renamed TSST1 (Bergdoll et al., 1959; Casman, 1960; Thomas et al., 2007; Ono et al., 2008): enterotoxins A (SEA), B (SEB), C1 (SEC1), C2 (SEC2), C3 (SEC3), D (SED), E (SEE), G (SEG), H (SEH), I (SEI), J (SElJ) (Balaban & Rasooly, 2000), K (SElK) (Orwin et al., 2001), L (SElL), M (SElM), N (SElN), O (SElO) (Jarraud et al., 2001), P (SElP) (Omoe et al., 2005), Q (SElQ) (Orwin et al., 2002), R (SER) (Omoe et al., 2003), S (SES), T (SET) (Ono et al., 2008), U (SElU) (Letertre et al., 2003), and U2 and V (Thomas et al., 2006).

Table 5. Staphylococcal enterotoxin characteristics
Toxin typeGeneral characteristicsMode of activityReferences
Molecular weight (Da)Genetic basis of SESuperantigenic actionaEmetic actionb
  1. a

    +, positive reaction.

  2. b

    +, positive reaction; (+), weak reaction; −, negative reaction; nk, not known.

  3. c

    For SElL, emetic activity was not demonstrated in Macaca nemestrina monkey.

  4. d

    For SElP, emetic activity was demonstrated in Suncus murinus but not in primate model.

SEA27 100Prophage++

Betley & Mekalanos (1985)

Borst & Betley (1994)

SEB28 336Chromosome, plasmid, pathogenicity island++

Jones & Khan (1986)

Shafer & Iandolo (1978)

Shalita et al. (1977)

Altboum et al. (1985)

SEC1-2-3≈ 27 500Plasmid++

Bohach & Schlievert (1987)

Hovde et al. (1990)

Altboum et al. (1985)

Fitzgerald et al. (2001)

SED26 360Plasmid++

Chang & Bergdoll (1979)

Bayles & Iandolo (1989)

SEE26 425Prophage++Couch et al. (1988)
SEG27 043enterotoxin gene cluster (egc), chromosome++

Munson et al. (1998)

Jarraud et al. (2001)

SEH25 210Transposon++

Su & Wong (1996)

Ren et al. (1994)

Noto & Archer (2006)

SEI24 928egc, chromosome+(+)

Munson et al. (1998)

Jarraud et al. (2001)

SElJ28 565Plasmids+nkZhang et al. (1998)
SEK25 539Pathogenicity island+nkOrwin et al. (2001)
SElL25 219Pathogenicity island+cOrwin et al. (2003)
SElM24 842egc, chromosome+nkJarraud et al. (2001)
SElN26 067egc, chromosome+nkJarraud et al. (2001)
SElO26 777egc, chromosome+nkJarraud et al. (2001)
SElP26 608Prophage+nkd

Kuroda et al. (2001)

Omoe et al. (2005)

SElQ25 076Pathogenicity island+

Jarraud et al. (2002)

Diep et al. (2006)

SER27 049Plasmids++Omoe et al. (2003)
SES26 217Plasmid++Ono et al. (2008)
SET22 614Plasmid+(+)Ono et al. (2008)
SElU27 192egc, chromosome+nkLetertre et al. (2003)
SElU226 672egc, chromosome+nkThomas et al. (2006)
SElV24 997egc, chromosome+nkThomas et al. (2006)

These toxins, (enterotoxin and enterotoxin like) are globular single-chain proteins with molecular weights ranging from 22 to 29 kDa. Moreover, their crystal structures, established for SEA, SEB, SEC, SED, SEH, SElI and SElK, reveal significant homology in their secondary and tertiary conformations (Mitchell et al., 2000). However, SEs, SEls and TSST-1 can be divided into four phylogenetic groups based on their primary amino acid sequences (Thomas et al., 2007).


Staphylococcal enterotoxins are resistant to environmental conditions (freezing, drying, heat treatment and low pH) that easily destroy the enterotoxin-producing strain. They are also resistant to proteolytic enzymes retaining their activity in the digestive tract after ingestion (Bergdoll, 1989). Thermal resistance is dependent on the relative purity of the SE preparation. Crude SEA in buffer was reduced from 21 μg mL−1 to < 1 μg mL−1 after heating at 100 °C for 130 min. Purified SEA (0.2 mg mL−1), however, was completely inactivated in buffer after heating at 80 °C for 3 min or 100 °C for 1 min. Generally, crude SEB seems to be considerably more heat resistant than purified SEA (Minor & Marth, 1972). The results of thermal inactivation of SEA and SED in milk and milk products are shown in Table 6 (Tatini, 1976). Generally, heat treatments commonly used in food processing are not effective for complete destruction of SE when present initially at levels expected to be found in food involved in food poisoning outbreaks (0.5–10 μg per 100 mL or 100 g) (Bergdoll, 1989). However, it should be borne in mind that thermal inactivation is often determined by loss of the serological reactivity of the SE. Biological activity may be lost before the serological activity. On the other hand, some outbreaks result from eating foods that have been heated after SE was produced (Bergdoll, 1989). Thermal stability of SE is influenced by the nature of the food, pH, presence of NaCl, etc., and also by the type of toxin. SEA, for instance, is relatively more stable to heat at pH 6.0 or higher than at pH 4.5–5.5. SED is relatively more stable at pH 4.5–5.5 than at pH 6.0 or higher (Tatini, 1976). If SE is not completely inactivated by heat, reactivation may occur under certain circumstances like cooking, storage or incubation (Tatini, 1976).

Table 6. Thermal inactivation of SEA and SED in milk and milk products at 72 °C for 15 s (Tatini, 1976)
Type of samplePercent serological activity remaininga
  1. NT, not tested.

  2. a

    Initial concentration: 1 μg mL−1.

Whole milk3630
Skim milk5630
Evaporated milk56NT
Reconstituted non-fat dry milk45NT

These proteins have been named according to their emetic activity (Lina et al., 2004) after oral administration in a primate model. Some were renamed SE-like toxins (SEl), because either no emetic properties were detected or they were not tested in primate models (Lina et al., 2004; Thomas et al., 2007). SEs belong to the broad family of pyrogenic toxin superantigens (Van den Bussche et al., 1993). Superantigens (SAgs), unlike conventional antigens, do not need to be processed by antigen-presenting cells (APC) before being presented to T cells. They can directly stimulate T cells by cross-linking major histocompatibility complex (MHC) class II molecules on APC with the variable portion of the T-cell antigen receptor β chain (TCR Vβ) or the T-cell antigen receptor α chain for SE (TCR Vα), thereby inducing polyclonal cell proliferation (Li et al., 1999; Pumphrey et al., 2007; Thomas et al., 2009). SAg-binding sites lie outside the peptide-binding groove and therefore do not depend on T-cell antigenic specificity but rather on the Vβ and/or Vα region of the TCR (Dellabona et al., 1990; Li et al., 1999; Pumphrey et al., 2007). This leads to activation of a large number of T cells followed by proliferation and massive release of chemokines and proinflammatory cytokines that may lead to potentially lethal toxic shock syndrome (Balaban & Rasooly, 2000). The SAgs can interact with epithelial cells leading to their transepithelial transport, cell activation and induction of inflammatory state. First, most SAgs have dose-dependent capacity to cross the intestinal wall and produce a local and systemic action on the immune system. This transport is favoured by the production of pro-inflammatory cytokine-like elements (McKay & Singh, 1997). A protein motif (i.e. KKKVTAQELD) highly conserved among SE and located in the amino acids 120–130 and 144–161, for TSST1 and SE respectively, has been identified and is involved in this transcytosis (Shupp et al., 2002). Stimulation of intestinal epithelial cells by SEA also induces an increase in the concentration of intracellular calcium via the release of cellular calcium reserves leading to their activation. This mechanism involves a nitric oxide synthase inducible by TNF-α (Hu et al., 2005). Finally, superantigenic stimulation of intestinal epithelial cells induces an inflammatory response. The activation of T84 cells (a human epithelial cell line) by SAgs induces the production of (1) monocyte chemoattractant protein 1 (MCP-1) and (2) regulated on activation normal T-cell expressed and secreted protein (RANTES). These chemokines promote the recruitment of immune mononuclear cells, which may explain the role of the SAgs in the pathogenesis of inflammatory gastrointestinal diseases (Jedrzkiewicz et al., 1999). In addition, both SEA and SEB bind to intestinal myofibroblasts with MHC class II molecules (Pinchuk et al., 2007). However, only SEA induces an immune response with the release of MCP-1, interleukins 8 and 6 (IL-8 and IL-6), granulocyte macrophage colony–stimulating factor (GM-CSF), and granulocyte colony–stimulating factor (G-CSF).

Although the superantigenic activity of SEs has been well characterized, as previously presented, the mechanisms leading to the emetic activity are less documented. Despite the considerable efforts to identify specific amino acids and domains within SEs which may be important for emesis, results are still limited and controversial. For example, SElL and SElQ are nonemetic, whereas SEI displays weak emetic activity (Ono et al., 2008). These toxins lack the disulphide loop characteristically found at the top of the N-terminal domain of other SEs. Nonetheless, the loop itself does not appear to be an absolute requirement for emesis, although it may stabilize a crucial conformation important for this activity (Hovde et al., 1994). Harris et al. (1993) examined the correlation between emetic and T-cell stimulatory activities of SEA and SEB where the amino acids had been substituted. In most cases, genetic mutations resulting in a loss of superantigen activity also resulted in loss of emetic activity. However, as there was not a perfect correlation between immunological and emetic activities in all the mutants, this study suggested that these two activities could be dissociated.

In contrast to other bacterial enterotoxins, specific cells and receptors in the digestive system have not been clearly linked to oral intoxication by a SE. Sugiyama & Hayama (1965) suggested that SEs stimulate the vagus nerve in the abdominal viscera, which transmits the signal to the emetic centre. Supporting this idea, receptors on vagal afferent neurons are essential for SEA-triggered emesis (Hu et al., 2007). In addition, SEs are able to penetrate the gut lining and activate local and systemic immune responses (Shupp et al., 2002). The diarrhoea sometimes associated with SE intoxication could be attributed to the inhibition of water and electrolyte reabsorption in the small intestine (Sullivan, 1969; Sheehan et al., 1970). In an attempt to link the two distinct activities of SEs, i.e., superantigenicity and emesis, it has been postulated that enterotoxin activity could facilitate transcytosis, enabling the toxin to enter the bloodstream and circulate through the body, thus allowing the interaction with APC and T cells that leads to superantigen activity (Hamad et al., 1997; Balaban & Rasooly, 2000). In this way, circulation of SEs following ingestion of SEs, as well as their spread from an S. aureus infection site, could have more profound effects upon the host than if the toxin remains localized (Larkin et al., 2009).

Genetic determinants and regulation of expression

Enterotoxin gene locations (Table 5) are numerous (Argudin et al., 2010). They can be carried by plasmids (seb, sed, sej, ser, ses, set) (Shalita et al., 1977; Bayles & Iandolo, 1989; Zhang et al., 1998; Omoe et al., 2003; Ono et al., 2008), phage (temperate for sea, defective for see) (Betley & Mekalanos, 1985; Couch et al., 1988; Coleman et al., 1989) or by genomic islands (seb, sec, seg, seh, sei, sek, sel, sem, sen, seo, sep and seq). Gene encoding for sec can be located on a plasmid or a pathogenicity island depending on the origin of the isolate (Fitzgerald et al., 2001). Jarraud et al. (2001) highlighted the existence of an operon, egc (enterotoxin gene cluster), encoding for several SEs such as SEG, SEI, SEM, SEN and SEO. The egc also contains two pseudogenes (φent1 and φent2). This locus probably plays the role of a nursery for se genes, as phenomena of duplication and recombination from a common ancestral gene could explain new forms of toxins. This was demonstrated by the identification of genes encoding for seu, seu2 and sev within egc (Letertre et al., 2003; Thomas et al., 2006). The location of se genes on mobile genetic elements can result in horizontal gene transfer between the strains of S. aureus. For example, the seb gene is located on the chromosome in some clinical isolates (Shafer & Iandolo, 1978), whereas it has a plasmidic location in other strains of S. aureus (Shalita et al., 1977).

A main regulatory system controlling the expression of virulence factors in S. aureus is the agr system (accessory gene regulator; Kornblum et al., 1990). This system works in combination with the sar system (Staphylococcal accessory regulator; Cheung et al., 1992; Novick et al., 2001). Most but not all of the expression of SEs is controlled by the agr system. For example, expressions of seb, sec and sed genes are agr-dependent, whereas expressions of sea and sej are agr-independent (Tremaine et al., 1993; Zhang et al., 1998). Vojtov et al. (2002) demonstrated that SEB is a negative global regulator of exoprotein gene expression acting through the agr system. The expression of agr system is closely linked to quorum sensing (Novick et al., 2001). In a recent study carried out on 28 enterotoxigenic strains of S. aureus isolated from food poisoning outbreaks or reference libraries to better understand se gene expression, Derzelle et al. (2009) demonstrated four different patterns of expression using quantitative reverse transcription PCR. The first pattern for sea, see, sej, sek, sep and seq indicated that the abundance of mRNAs was independent of the bacterial growth phases. In the second pattern, the transcript levels for seg, sei, sem, sen, seo and seu slightly decreased during bacterial growth. The third pattern indicated a huge and rapid induction of seb, sec and seh at the end of the exponential growth phase whereas the last highlighted a modest postexponential increase in sed, ser and sel expression.

To conclude this section, the currently known SEs form a group of serologically distinct, extracellular proteins that share important properties namely, (1) the ability to cause emesis in primate model; (2) superantigenicity through a noncomplete unspecific activation of T lymphocytes (as each SEs binds to a subset of Vβ chains) followed by cytokine release and systemic shock (Marrack & Kappler, 1990; Papageorgiou & Acharya, 2000); (3) resistance to heat and to digestion by pepsin; and (4) structural similarities (Dinges et al., 2000).

SFPOs: symptomatology; reporting system including EU control; monitoring schemes; occurrence and analytical methods used

  1. Top of page
  2. Abstract
  3. A worldwide review of outbreaks related to coagulase-positive staphylococci and their toxins: the story
  4. Characteristics and behaviour of S. aureus in the food environment
  5. Toxinogenic conditions and characteristics of SEs
  6. SFPOs: symptomatology; reporting system including EU control; monitoring schemes; occurrence and analytical methods used
  7. Concluding remarks
  8. References
  9. Supporting Information

Symptomatology and toxic dose

The incubation period and severity of symptoms observed depend on the amount of enterotoxins ingested and the susceptibility of each person. Initial symptoms, nausea followed by incoercible characteristic vomiting (in spurts), appear within 30 min–8 h (3 h on average) after ingesting the contaminated food. Other commonly described symptoms are abdominal pain, diarrhoea, dizziness, shivering and general weakness, sometimes associated with a moderate fever. In the most severe cases, headaches, prostration and low blood pressure have been reported. In the majority of cases, recovery occurs within 24–48 h without specific treatment, while diarrhoea and general weakness can last 24 h or longer. Death is rare (0.02‰ according to Mead et al., 1999), occurring in the most susceptible people to dehydration such as infants and the elderly (Do Carmo et al., 2004) and people affected by an underlying illness.

Regarding the toxin dose, most of the studies referred to SEA. Notermans et al. (1991) demonstrated the feasibility of a reference material containing about 0.5 μg of staphylococcal enterotoxin A (SEA), as it had been suggested that this dose can cause symptoms such as vomiting (Bergdoll, 1989). Mossel et al. (1995) cited an emetic dose 50 value of about 0.2 μg SE per kg of human body weight. They concluded that an adult would need to ingest about 10–20 μg of SE to suffer symptoms. Other authors (Martin et al., 2001) considered that < 1 μg of SE may cause food-poisoning symptoms in susceptible individuals. Evenson et al. (1988) estimated that the amount of SEA needed to cause vomiting and diarrhoea was 0.144 μg, the amount recovered from a half-pint (approximately 0.28 L) carton of a 2% chocolate milk. In SFP in Japan, the total intake of SEA in low-fat milk per capita was estimated mostly at approximately 20–100 ng (Asao et al., 2003; Ikeda et al., 2005). In an SFPO involving ‘coconut pearls’ (a Chinese dessert based on tapioca), Hennekinne et al. (2009) estimated the total intake of SEA per body at around 100 ng. Finally, Ostyn et al. (2010) investigated SFPOs owing to SEE and estimated that the total intake of SEE per body was 90 ng, a dose in accordance with those previously mentioned.

Reporting system, occurrence at European Union level

The reporting of food-borne outbreaks has been mandatory for the European Union Member States (EU MSs) since 2005. Moreover, since 2007, new harmonized specifications on the reporting of these outbreaks at Community level have come into force (Anonymous, 2007a). However, the food-borne outbreak investigation and reporting systems at national level are not harmonized within the EU. Therefore, differences in the number of reported outbreaks, the types of outbreaks and causative agents do not necessarily reflect different levels of food safety between EU MSs. The high number of reported outbreaks may reflect the increasing efficiency of the EU-MSs’ systems in investigating and identifying the outbreaks.

The European Food Safety Authority (EFSA) is responsible for examining the data on zoonoses, antimicrobial resistance and food-borne outbreaks submitted by Member States in accordance with Directive 2003/99/EC (Anonymous, 2003) and for preparing the Community Summary Report from the results. Data were produced in collaboration with the European Centre for Disease Control (ECDC), which provides the information on zoonosis cases in humans. The Zoonoses Collaboration Centre (ZCC – contracted by EFSA) in the National Food Institute of the Technical University of Denmark assisted EFSA and ECDC in this task (Fig. 1).


Figure 1. 3D structure of various staphylococcal enterotoxins. SEA: Staphylococcal enterotoxin A (Schad et al., 1995); SEB: Staphylococcal enterotoxin B (Papageorgiou et al., 1998); SEC2: Staphylococcal enterotoxin C2 (Swaminathan et al., 1995); SEC3: Staphylococcal enterotoxin C3 (Chi et al., 2002); SEG: Staphylococcal enterotoxin G (Fernandez et al., 2011); SEH: Staphylococcal enterotoxin H (green) with sulfate ions and water (Hâkansson et al., 2000); SEI: Staphylococcal enterotoxin I (Fernandez et al., 2006); SEK: Staphylococcal enterotoxin K (Gunther et al., 2007). All structures obtained from (Adapted by L. Bandounas).

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In 2005, the first year for reporting of food-borne outbreaks in the European Union, only seven Member States reported food-borne outbreaks (n = 36) caused by SEs.

European data from 2006 to 2008 are presented in Fig. 2.


Figure 2. Causative agents involved in European Union outbreaks 2006–2008 (data extracted from The Community Summary Reports 2006, 2007 and 2008).

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In 2006, EFSA (Anonymous, 2007c) reported that SEs were involved in 236 outbreaks of 5807 (4.1%) food poisoning outbreaks, corresponding to the fourth rank of causative agents after the ones associated with Salmonella spp. (59.3%), viruses (10.2%) and Campylobacter spp. (6.9%). Dairy products, red meat products and poultry were involved in 26 (11.0%), 19 (8.0%) and 16 (6.8%) of the 236 outbreaks respectively.

In 2007, EFSA (Anonymous, 2009) reported that bacterial toxins were involved in 458 of 5423 (8.1%) food poisoning outbreaks corresponding to the fourth rank of pathogenicity after those associated with Salmonella spp. (39.3%), viruses (11.8%) and Campylobacter spp. (8.1%). Among bacterial toxins, SEs were involved in 258 of the 458 notified outbreaks (56.3%). Thus, SEs were involved in 4.6% of all notified outbreaks in 2007.

Finally, in 2008, EFSA (Anonymous, 2010) reported that bacterial toxins were involved in 525 of 5332 (9.8%) food poisoning outbreaks, corresponding to the third rank of pathogenicity after those associated with Salmonella spp. (35.4%) and viruses (13.1%). Among bacterial toxins, SEs were involved in 291 of the 525 notified outbreaks (55.4%). Thus, SEs were involved in 5.5% of all notified food poisoning outbreaks in 2008.

Analytical methods for SE detection (Fig.3)

Diagnosis of SFP is generally confirmed either by the recovery of at least 105 S. aureus g−1 from food remnants or by the detection of SEs in food remnants. In some cases, confirmation of SFP is difficult because S. aureus is heat sensitive, whereas SEs are not. Thus, in heat-treated food matrices, S. aureus may be eliminated without inactivating SEs. In such cases, it is not possible to characterize a food poisoning outbreak by enumerating CPS in food remnants or detecting se genes in isolated strains.

While S. aureus is usually enumerated using microbiological techniques with dedicated media such as Baird Parker or rabbit plasma fibrinogen agar, three types of methods are used to detect bacterial toxins in food: bioassays, molecular biology and/or immunological techniques.


Bioassays are based on the capacity of an extract of the suspected food to induce symptoms such as vomiting, gastrointestinal symptoms in animals and/or superantigenic action in cell cultures. Historically, SEs have been detected based on their emetic activity in monkey-feeding and kitten-intraperitoneal tests (Surgalla et al., 1953; Bergdoll, 1989) and, more recently, using animal models such as house musk shrews Suncus murinus (Hu et al., 2003; Ono et al., 2008). Symptoms of SFP appear if the dose of SEA ingested by the animals is above 2.3 μg, a considerably higher amount than those involved in human food poisoning (Asao et al., 2003; Ostyn et al., 2010). Thus, this technique is not appropriate for characterizing SFPOs.

Molecular methods

Molecular biology methods often involve the polymerase chain reaction (PCR). These methods usually detect genes encoding enterotoxins in strains of S. aureus isolated from contaminated foods. However, these methods have two major limitations: first, staphylococcal strains must be isolated from food, and second, the results inform as to the presence or absence of genes encoding SEs, but do not provide any information on the expression of these genes in food. This method therefore cannot be the sole method for confirming S. aureus as causative agent in an outbreak. However, the PCR approach is a specific, highly sensitive and rapid method that can characterize the S. aureus strains involved in SFPOs, thereby providing highly valuable information. In outbreaks described by Ostyn et al. (2010), SEE has been found in the common source vehicle and the see gene was present in the tested S. aureus isolates. In such a case, se gene determination helps to confirm the role of an SE rarely encountered. Very recent efforts have been directed to determining directly which se genes are found in suspected foods. Following the huge SFP event which occurred in Japan in July 2000 (more than 13 000 people were intoxicated by powdered or liquid milk), Ikeda et al. (2005) developed a PCR-based methodology whereby sea, seg, seh and sei genes could be detected in the incriminated powdered skim milk, although cultivable S. aureus were not recovered from the sample.

Moreover, to evaluate the toxic potential of strains isolated from SFPOs, various authors (Lee et al., 2007; Akineden et al., 2008; Derzelle et al., 2009) have recently designed primers to perform PCR and reverse transcription PCR (RT-PCR) for se genes.

Finally, Duquenne et al. (2010) developed an efficient method for extracting bacterial RNA accessible for RT-quantitative PCR (RT-qPCR) from cheese and adapted a simple, sensitive and reproducible, method for quantifying relative transcript levels to evaluate S. aureus enterotoxin gene expression during cheese manufacture. These approaches demonstrate possible transcription of mRNA from those genes, but do not indicate whether those strains were able to produce detectable or poisonous levels of toxins in food.

Immunological methods

The third and most commonly used method for detecting SEs in food is based on the use of anti-enterotoxin polyclonal or monoclonal antibodies. Commercially available kits have been developed according to two different principles: (1) enzyme immunoassay (EIA) comprising ELISA and enzyme-linked fluorescent assay (ELFA); and (2) RPLA. It is widely recognized that the use of immunological methods to detect contaminants in food matrices is a difficult task, mainly because of the lack of specificity and sensitivity of the assay. Many drawbacks impair the development and use of these techniques for detecting SEs. First, highly purified toxins are needed to raise specific antibodies to develop an EIA; purified toxins are difficult and expensive to obtain. Moreover, and until very recently, only antibodies against SEA to SEE, SEG, SEH and SElQ were available (Schlievert & Case, 2007). The ELISA test will not detect the other SEs, which could partly explain why some outbreaks remained uncharacterized without a known aetiological agent. Another drawback is the low specificity of some commercial kits, where false positives may occur depending on food components (Wieneke, 1991) as it is well known that some proteins, such as protein A, can interfere with binding to the Fc fragment (and, to a lesser extent, Fab fragments) in immunoglobulin G from several animal species, such as mouse or rabbit, but not rat or goat. Other interferences are associated with endogenous enzymes, such as alkaline phosphatase or lactoperoxidase.

Whatever the detection method used and owing to the low amount of SEs present in food, it is crucial to concentrate the extract before performing detection assays. For this purpose, various methodologies have been tested (Macaluso et al., 1998; Meyrand et al., 1999; Lapeyre et al., 2001). Among them, only extraction followed by dialysis concentration has been approved by the European Union for extracting SEs from food (Anonymous, 2007b).

However, up to now, after enumerating CPS strains, conclusive diagnosis of SFPs has mainly been based on demonstrating the presence of SEs in food using commercial EIA kits designed to detect SEA to SEE (Bennett, 2005) or using a confirmatory in-house ELISA method (Lapeyre et al., 1988) to differentiate and quantify these types of SEs.

Mass spectrometry-based methods

Owing to the drawbacks with currently available detection methods and the lack of available antibodies against the newly described SEs, other strategies based on physicochemical techniques have been developed very recently. Among these, mass spectrometry (MS) has newly emerged as a very promising and suitable technique for analysing protein and peptide mixtures (Mamone et al., 2009). It is among the most sensitive techniques currently available because it provides specific, rapid and reliable analytical quantification of the amount of enterotoxins (Brun et al., 2007). The development of two soft ionization methods, such as electrospray ionization (ESI) and matrix-assisted laser desorption/ionization (MALDI), and the use of appropriate mass analyzers such as time-of flight (TOF) have revolutionized the analysis of biomolecules. Given the wide range of methodologies available, a single MS technique cannot be used for all proteins. The MS method thus requires the development of a series of techniques, individually suited for each particular case.

In the case of food analysis, the situation is complex because the matrix can contain many proteins, lipids and many other molecular species that interfere with the detection of the targeted toxin and may distort quantification. Sample preparation remains the critical step of the analysis. Several authors have tried to improve this step, by, for example, optimizing digestion parameters (Norrgran et al., 2009) or by adding a purification step (Oeljeklaus et al., 2009). The strategy of incorporating an isotopically labelled internal standard into the samples has also been developed. In the case of SE detection, some authors have developed MS tools to detect these toxins in culture supernatants and in spiked samples, such as water or apple juice. For example, Bernardo et al. (2002) developed a MALDI-TOF method for detecting S. aureus virulence factors such as enterotoxins and demonstrated that this technique was suitable for detecting SEs other than SEA to SEE in culture supernatants. Callahan et al. (2006) detected and quantified SEB using liquid chromatography coupled to ESI/MS detection in apple juice used as a model food matrix. In this study, enterotoxin types SEA and SEB were detected in spiked cheese. More recently, Brun et al. (2007) developed an MS approach able to perform absolute quantification of SEA and TSST1 in spiked water or urine samples. To improve characterization and quantification of SEs, this latter methodology was successfully used to carry out absolute quantification of SEA in a naturally contaminated cheese sample (Dupuis et al., 2008) and applied to a recent case of food poisoning outbreak (Hennekinne et al., 2009). In this outbreak, MS tools in combination with tools presented earlier were used by the European Union Reference Laboratory for CPS. This MS-based method overcame specific technical limitations of existing ELISA for SE characterization but its throughput and cost per analysis compared unfavourably with ELISA (€650 vs. €280). This last method was no doubt the gold standard of low-cost and high-throughput techniques for the detection and quantification of protein compounds down to subnanomolar concentrations in large sample cohorts. However, the timescale for ELISA assay development was of the order of 1 year and high developmental costs precluded systematic ELISA optimization. This cost also made ELISA less suitable for the characterization of small panels such as SFP elucidation. In this regard, the versatility and low development cost of the absolute quantification methodology positioned it as a good alternative to ELISA for these specific applications, keeping in mind that purified SEs standards were also needed to establish the accuracy and specificity of MS-based methods.

Thus, combining classical microbiology for enumerating CPS strains with immunological techniques, molecular biology and mass spectrometry-based methods, the diagnosis was reinforced and these outbreaks could be attributed to the presence of SEs.

Concluding remarks

  1. Top of page
  2. Abstract
  3. A worldwide review of outbreaks related to coagulase-positive staphylococci and their toxins: the story
  4. Characteristics and behaviour of S. aureus in the food environment
  5. Toxinogenic conditions and characteristics of SEs
  6. SFPOs: symptomatology; reporting system including EU control; monitoring schemes; occurrence and analytical methods used
  7. Concluding remarks
  8. References
  9. Supporting Information

Staphylococcal food poisoning is one of the most common food-borne diseases, resulting from ingestion of SEs produced in food by enterotoxigenic strains of staphylococci, mainly CPS and only occasionally CNS. From 2006 to 2008, the European Food Safety Authority reported that SEs were involved in 5% of food poisoning outbreaks, but this percentage is certainly underestimated owing to poor analytical performance in the detection and identification of SEs in food remnants.

Prevention of staphylococcal food-borne poisoning is based on hygiene measures to avoid or reduce contamination of food by S. aureus. These procedures must include control of raw materials, proper handling, cleaning and disinfection of equipment from farm to fork. However, as these requirements are usually not sufficient, it is necessary to destroy staphylococci through appropriate treatment, thermal or otherwise, to prevent their growth under refrigerated conditions. Respect for the cold chain is critical in regard to staphylococci especially for foods served at large gatherings such as social events.

To improve SFPO characterization, various techniques, such as immunological and molecular-based methodologies, have been integrated in the diagnosis strategy. The PCR approach is known to provide information on the presence or absence of genes encoding SEs, but not their expression. To complete SFPO characterization, MS tools have also been used in combination with those presented earlier. Thus, an overall approach combining classical microbiology to enumerate CPS strains with immunological techniques, molecular biology and mass spectrometry-based methods offers an interesting alternative for attributing outbreaks to SEs (Fig. 3). While the quantitative MS method overcomes specific technical limitations of existing ELISA methods for detecting and quantifying SEs, its throughput and cost per analysis compare unfavourably with ELISA. For this reason, when the MS-based method becomes available for all SEs involved in SFPOs, it will not be employed for routine analysis, but only in special cases to confirm outbreaks because of SEs.


Figure 3. General overview of analytical methods used to improve SFPO characterization. 2D PAGE; two dimension gel electrophoresis; CPS, coagulase positive staphylococci; DC, dialysis concentration; IAC, immunoaffinity chromatography; anoLC/ESI/MS, nano-liquid chromatrography/electrospray-ionization/mass spectrometry; RPLA, reversed passive latex agglutination; RT-PCR, reverse transcriptase PCR; SE, staphylococcal enterotoxin; SFPO, staphylococcal food poisoning outbreak. Continuous line: analysis performed from food sample; discontinuous line: analysis performed from strains or culture supernatant. Brown: microbiological methods; green: molecular methods; blue: immunological methods; red: mass spectrometry-based methods.

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  1. Top of page
  2. Abstract
  3. A worldwide review of outbreaks related to coagulase-positive staphylococci and their toxins: the story
  4. Characteristics and behaviour of S. aureus in the food environment
  5. Toxinogenic conditions and characteristics of SEs
  6. SFPOs: symptomatology; reporting system including EU control; monitoring schemes; occurrence and analytical methods used
  7. Concluding remarks
  8. References
  9. Supporting Information
  • Akineden O , Hassan AA , Schneider E & Usleber E (2008) Enterotoxigenic properties of Staphylococcus aureus isolated from goats’ milk cheese. Int J Food Microbiol 124: 211216.
  • Altboum Z , Hertman I & Sarid S (1985) Penicillinase plasmid-linked genetic determinants for enterotoxins B and C1 production in Staphylococcus aureus. Infect Immun 47: 514521.
  • Alves PDD , McCulloch JA , Even S , Le Marechal C , Thierry A , Grosset N , Azevedo V , Rosa CA , Vautor E & Le Loir Y (2009) Molecular characterisation of Staphylococcus aureus strains isolated from small and large ruminants reveals a host rather than tissue specificity. Vet Microbiol 137: 190195.
  • Anonymous (1968) CDC. MMWR Morb Mortal Wkly Rep 17: 109110.
  • Anonymous (1976) CDC. MMWR Morb Mortal Wkly Rep 25: 317318.
  • Anonymous (1983a) CDC. MMWR Morb Mortal Wkly Rep 32: 183184.
  • Anonymous (1983b) CDC. MMWR Morb Mortal Wkly Rep 32: 294295.
  • Anonymous (1986) CDC. MMWR Morb Mortal Wkly Rep 35: 715716.
  • Anonymous (1989) CDC. MMWR Morb Mortal Wkly Rep 38: 417418.
  • Anonymous (1992) U.S. Food and Drug Administration. The Center for Food Safety and Applied Nutrition. (US FDA/CFSAN, 1992). Foodborne Pathogenic Microorganisms and Natural Toxins Handbook: Staphylococcus aureus. Retrieved March 2010, from
  • Anonymous (1997) CDC. MMWR Morb Mortal Wkly Rep 46: 11891191.
  • Anonymous (2003) Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 on the monitoring of zoonoses and zoonotic agents, amending Council Decision 90/424/EEC and repealing Council Directive 92/117/EEC. Off J Eur Union L325: 3140.
  • Anonymous (2007a) Report of the Task Force on Zoonoses Data Collection on harmonising the reporting of food-borne outbreaks through the Community reporting system in accordance with Directive 2003/99/EC. EFSA J 123: 116.
  • Anonymous (2007b) Commission Regulation No. 1441/2007 of 5 December 2007. Off J Eur Union L322: 1229.
  • Anonymous (2007c) The Community Summary Report 2006: Trends and Sources of Zoonoses, Zoonotic Agents, Antimicrobial Resistance and Foodborne Outbreaks in the European Union in 2006. EFSA J 130: 1352.
  • Anonymous (2009) The Community Summary Report 2007: Trends and Sources of Zoonoses, Zoonotic Agents, Antimicrobial Resistance and Foodborne Outbreaks in the European Union in 2007. EFSA J 271: 1223.
  • Anonymous (2010) The Community Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and food-borne outbreaks in the European Union in 2008. EFSA J 1496: 1376.
  • Argudin MA , Mendoza MC & Rodicio MR (2010) Food poisoning and Staphylococcus aureus Enterotoxins. Toxins 2: 17511773.
  • Asao T , Kumeda Y , Kawai T , Shibata T , Oda H , Haruki K , Nakazawa H & Kozaki S (2003) An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: estimation of enterotoxin A in the incriminated milk and powdered skim milk. Epidemiol Infect 130: 3340.
  • Baerthlein K (1922) Ueber: uogcdehnte Wurstvergiftungen, bedingt durch Bacillus proteus vulgaris. Munch Med Wochenschr 69: 155156.
  • Balaban N & Rasooly A (2000) Staphylococcal enterotoxins. Int J Food Microbiol 61: 110.
  • Barber MA (1914) Milk poisoning due to a type of Staphylococcus albus occurring in the udder of a healthy cow. Philipp J Sci 9: 515519.
  • Bayles KW & Iandolo JJ (1989) Genetic and molecular analysis of gene encoding staphylococcal enterotoxin D. J Bacteriol 171: 47994806.
  • Becker K , Keller B , von Eiff C , Bruck M , Lubritz G , Etienne J & Peters G (2001) Enterotoxigenic potential of Staphylococcus intermedius. Appl Environ Microbiol 67(12): 55515557.
  • Belay N & Rasooly A (2002) Staphylococcus aureus growth and enterotoxin A production in an anaerobic environment. J Food Prot 65: 199204.
  • Bennett RW (1996) Atypical toxigenic Staphylococcus and non-Staphylococcus aureus species on the horizon? An update. J Food Protect 59: 11231126.
  • Bennett RW (2005) Staphylococcal enterotoxin and its rapid identification in foods by enzyme-linked immunosorbent assay-based methodology. J Food Prot 68: 12641270.
  • Bergdoll MS (1989) Staphylococcus aureus. Foodborne Bacterial Pathogens ( Doyle MP , ed), pp. 463523. Marcel Dekker Inc., New York, Basel.
  • Bergdoll MS , Surgalla MJ & Dack GM (1959) Staphylococcal enterotoxin. I. Purification. Arch Biochem Biophys 85: 6269.
  • Bernardo K , Pakulat N , Macht M , Krut O , Seifert H , Fleer S , Hunger F & Kronke M (2002) Identification and discrimination of Staphylococcus aureus strains using matrix-assisted laser desorption/ionization-time of flight mass spectrometry. Proteomics 2: 747753.
  • Betley MJ & Mekalanos JJ (1985) Staphylococcal enterotoxin A is encoded by a phage. Science 229: 185187.
  • Bohach GA & Schlievert PM (1987) Nucleotide sequence of the staphylococcal enterotoxin C1 gene and relatedness to other pyrogenic toxins. Mol Gen Genet 209: 1520.
  • Bone FJ , Bogie D & Morgan-Jone SC (1989) Staphylococcal food poisoning from sheep milk cheese. Epidemiol Infect 103: 449458.
  • Bonnetain F , Carbonel S , Stoll J & Legros D (2003) Toxi-infection alimentaire collective due à Staphylococcus aureus, Longevelle-sur-le-Doubs, juillet 2003. BEH 47: 231232.
  • Borst DW & Betley MJ (1994) Phage-associated differences in staphylococcal enterotoxin A gene (sea) expression correlate with sea allele class. Infect Immun 62: 113118.
  • Brink EL & Van Metter CT (1960) A study of an epidemic of staphylococcal enterotoxin food poisoning, Ad 419937, Defense documentation center for technical information. Cameron Station, Alexandria, Virginia Contract No. DA 18-064-Cml-2733: 10 October 1960.
  • Brun V , Dupuis A , Adrait A , Marcellin M , Thomas D , Court M , Vandenesch F & Garin J (2007) Isotope-labeled protein standards: toward absolute quantitative proteomics. Mol Cell Proteomics 6: 21392149.
  • Callahan JH , Shefcheck KJ , Williams TL & Musser SM (2006) Detection, confirmation, and quantification of staphylococcal enterotoxin B in food matrixes using liquid chromatography-mass spectrometry. Anal Chem 78: 17891800.
  • Casman EP (1960) Further serological studies of staphylococcal enterotoxin. J Bacteriol 79: 849856.
  • Chang HC & Bergdoll MS (1979) Purification and some physicochemical properties of staphylococcal enterotoxin D. Biochemistry 18: 19371942.
  • Cheung AL , Koomey JM & Butler CA (1992) Regulation of exoprotein expression in Staphylococcus aureus by a locus (sar) distinct from agr. P Natl Acad Sci USA, 89: 64626466.
  • Chi YI , Sadler I , Jablonski LM , Callantine SD , Deobald CF , Stauffacher CV & Bohach GA (2002) Zinc-mediated dimerization and its effect on activity and conformation of staphylococcal enterotoxin type C. J Biol Chem 277: 2283922846.
  • Chiou CS , Wei HL & Yang LC (2000) Comparison of pulsed-field gel electrophoresis and coagulase gene restriction profile analysis techniques in the molecular typing of Staphylococcus aureus. J Clin Microbiol 38: 21862190.
  • Coleman DC , Sullivan DJ , Russell RJ , Arbuthnott JP , Carey BF & Pomeroy HM (1989) Staphylococcus aureus bacteriophages mediating the simultaneous lysogenic conversion of beta-lysin, staphylokinase and enterotoxin A: molecular mechanism of triple conversion. J Gen Microbiol 135: 16791697.
  • Couch JL , Soltis MT & Betley MJ (1988) Cloning and nucleotide sequence of type E staphylococcal enterotoxin gene. J Bacteriol 17: 29542960.
  • Dack GM , Cary WE , Woolpert O & Wiggers H (1930) An outbreak of food poisoning proved to be due to a yellow hemolytic staphylococcus. J Prev Med 4: 167175.
  • de Boer E , Zwartkruis-Nahuis JT , Wit B , Huijsdens XW , de Neeling AJ , Bosch T , van Oosterom RA , Vila A & Heuvelink AE (2008) Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int J Food Microbiol 134: 5256.
  • De Buyser ML , Dilasser F , Hummel R & Bergdoll MS (1987) Enterotoxin and toxic shock syndrome toxin-1 production by staphylococci isolated from goat's milk. Int J Food Microbiol 5: 301309.
  • De Buyser ML , Dufour B , Maire M & Lafarge V (2001) Implication of milk and milk products in food-borne diseases in France and indifferent industrialized countries. Int J Food Microbiol 67: 117.
  • De la Fuente R , Suarez G & Schleifer KH (1985) Staphylococcus aureus subsp. anaerobius subsp. nov., the causal agent of abscess disease of sheep. Int J Syst Bacteriol 35: 99102.
  • de Neeling AJ , van den Broek MJ , Spalburg EC , van Santen-Verheuvel MG , Dam-Deisz WD , Boshuizen HC , van de Giessen AW , van Duijkeren E & Huijsdens XW (2007) High prevalence of methicillin resistant Staphylococcus aureus in pigs. Vet Microbiol 122: 366372.
  • DeLay PD (1944) Staphylococcal enterotoxin in bread pudding. Bull US Army Med Dept 72: 7273.
  • Dellabona P , Peccoud J , Kappler J , Marrack P , Benoist C & Mathis D (1990) Superantigens interact with MHC class II molecules outside of the antigen groove. Cell 62: 11151121.
  • Denison GA (1936) Epidemiology and symptomatology of staphylococcus food poisoning. A report of recent outbreaks. Am J Public Health 26: 11681175.
  • Denys J (1894) Présence de Staphylocoque dans une viande qui a déterminé des cas d'empoisonnement. Bull Acad R Med Belg 8: 496.
  • Derzelle S , Dilasser F , Duquenne M & Deperrois V (2009) Differential temporal expression of the staphylococcal enterotoxins genes during cell growth. Food Microbiol 26: 896904.
  • Devriese LA (1984) A simplified system for biotyping Staphylococcus aureus strains isolated from different animal species. J Appl Bacteriol 56: 215220.
  • Devriese LA , Yde M , Godard C & Isigidi BK (1985) Use of biotyping to trace the origin of Staphylococcus aureus in foods. Int J Food Microbiol 2: 365369.
  • Devriese LA , Vancanneyt M , Baele M et al. (2005) Staphylococcus pseudointermedius sp. nov., a coagulase positive species from animals. Int J Syst Bacteriol 55: 15691573.
  • Diep BA , Gill SR , Chang RF et al. (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367: 731739.
  • Dinges MM , Orwin PM & Schlievert PM (2000) Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 13: 1634.
  • Do Carmo LS , Cummings C , Linardi VR , Souza Diaz R , De Souza JM , De Sena MJ , Dos Santos DA , Shupp JW , Peres Pereira RK & Jett M (2004) A case study of a massive staphylococcal food poisoning incident. Foodborne Pathog Dis 1: 241246.
  • Dolman CE (1934) Ingestion of staphylococcus exotoxin by human volunteers, with special reference to staphylococci food poisoning. J Infect Dis 55: 172183.
  • Dupuis A , Hennekinne JA , Garin J & Brun V (2008) Protein Standard Absolute Quantification (PSAQ) for improved investigation of staphylococcal food poisoning outbreaks. Proteomics 8: 46334636.
  • Duquenne M , Fleurot I , Aigle M , Darrigo C , Borezée-Dupont E , Derzelle S , Bouix M , Deperrois-Lafarge V & Delacroix-Buchet A (2010) Tool for quantification of staphylococcal enterotoxin gene expression in cheese. Appl Environ Microbiol 76: 13671374.
  • Eisenberg MS , Gaarslev K , Brown W & Horwitz D (1975) Hill staphylococcal food poisoning aboard a commercial aircraft. Lancet 2: 595599.
  • Even S , Leroy S , Charlier C et al. (2010) Low occurrence of safety hazards in coagulase negative staphylococci isolated from fermented foodstuffs. Int J Food Microbiol 139: 8795.
  • Evenson ML , Hinds MW , Bernstein RS & Bergdoll MS (1988) Estimation of human dose of staphylococcal enterotoxin A from a large outbreak of staphylococcal food poisoning involving chocolate milk. Int J Food Microbiol 7: 311316.
  • Ewald S & Notermans S (1988) Effect of water activity on growth and enterotoxin D production of Staphylococcus aureus. Int J Food Microbiol 6: 2530.
  • Fernandez MM , Guan R , Swaminathan CP , Malchiodi EL & Mariuzza RA (2006) Crystal structure of staphylococcal enterotoxin I (SEI) in complex with a human major histocompatibility complex class II molecule. J Biol Chem 281: 2535625364.
  • Fernandez MM , Cho S , De Marzi MC , Kerzic MC , Robinson H , Mariuzza RA & Malchiodi EL (2011) Crystal structure of staphylococcal enterotoxin G (SEG) in complex with a mouse T-cell receptor {beta} chain. J Biol Chem 286: 11891195.
  • Fitzgerald JR , Monday SR , Foster TJ , Bohach GA , Hartigan PJ , Meaney WJ & Smyth CJ (2001) Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J Bacteriol 183: 6370.
  • Fitz-James I , Botteldoorn N , in't Veld P & Dierick C (2008) Joined investigation of a large outbreak involving Staphylococcus aureus. Proceeding FoodMicro 2008, Aberdeen, UK, September, 2.
  • Foster G , Ross HM , Hutson RA & Collins MD (1997) Staphylococcus lutrae sp. nov., a new coagulase-positive species isolated from otters. Int J Syst Bacteriol 47: 724726.
  • Genigeorgis CA (1989) Present state of knowledge on staphylococcal intoxication. Int J Food Microbiol 9: 327360.
  • Gunther S , Varma AK , Moza B et al. (2007) A novel loop domain in superantigens extends their T cell receptor recognition site. J Mol Biol 371: 210221.
  • Gutierrez C , Abee T & Booth IR (1995) Physiology of the osmotic stress response in microorganisms. Int J Food Microbiol 28: 233244.
  • Haines WC & Harmon LG (1973) Effect of selected lactic acid bacteria on growth of Staphylococcus aureus and production of enterotoxin. Appl Microbiol 25: 436441.
  • Hajek V (1976) Staphylococcus intermedius, a new species isolated from animals. Int J Syst Bacteriol 26: 401408.
  • Hâkansson M , Petersson K , Nilsson H , Forsberg G , Björk P , Antonsson P & Svensson LA (2000) The crystal structure of staphylococcal enterotoxin H: implications for binding properties to MHC class II and TcR molecules. J Mol Biol 302: 527537.
  • Halpin-Dohnalek MI & Marth EH (1989) Staphylococcus aureus: production of extracellular compounds and behavior in foods – a review. J Food Prot 52: 267282.
  • Hamad AR , Marrack P & Kappler JW (1997) Transcytosis of staphylococcal superantigen toxins. J Exp Med 185: 14471454.
  • Harris TO , Grossman D , Kappler JW , Marrack P , Rich RR & Betley MJ (1993) Lack of complete correlation between emetic and T-cell-stimulatory activities of staphylococcal enterotoxins. Infect Immun 61: 31753183.
  • Hennekinne JA , Kérouanton A , Brisabois A & De Buyser ML (2003) Discrimination of Staphylococcus aureus biotypes by pulsed-field gel electrophoresis of DNA macro-restriction fragments. J Appl Microbiol 94: 321329.
  • Hennekinne JA , Brun V , De Buyser ML , Dupuis A , Ostyn A & Dragacci S (2009) Innovative contribution of mass spectrometry to characterise staphylococcal enterotoxins involved in food outbreaks. Appl Environ Microbiol 75: 882884.
  • Hirooka EY , Muller EE , Freitas JC , Vicente E , Yoshimoto Y & Bergdoll MS (1988) Enterotoxigenicity of Staphylococcus intermedius of canine origin. Int J Food Microbiol 7: 185191.
  • Hovde CJ , Hackett SP & Bohach GA (1990) Nucleotide sequence of the staphylococcal enterotoxin C3 gene: sequence comparison of all three type C staphylococcal enterotoxins. Mol Gen Genet 220: 329333.
  • Hovde CJ , Marr JC , Hoffmann ML , Hackett SP , Chi YI , Crum KK , Stevens DL , Stauffacher CV & Bohach GA (1994) Investigation of the role of the disulphide bond in the activity and structure of staphylococcal enterotoxin C1. Mol Microbiol 13: 897909.
  • Hu DL , Omoe K , Shimoda Y , Nakane A & Shinagawa K (2003) Induction of emetic response to staphylococcal enterotoxins in the House Musk Shrew (Suncus murinus). Infect Immun 71: 567570.
  • Hu DL , Suga S , Omoe K , Abe Y , Shinagawa K , Wakui M & Nakane A (2005) Staphylococcal enterotoxin A modulates intracellular Ca2+ signal pathway in human intestinal epithelial cells. FEBS Lett 579: 44074412.
  • Hu DL , Zhu G , Mori F , Omoe K , Okada M , Wakabayashi K , Kaneko S , Shinagawa K & Nakane A (2007) Staphylococcal enterotoxin induces emesis through increasing serotonin release in intestine and it is downregulated by cannabinoid receptor 1. Cell Microbiol 9: 22672277.
  • Huijsdens XW , van Dijke BJ , Spalburg E , van Santen-Verheuvel MG , Heck ME , Pluister GN , Voss A , Wannet WJ & de Neeling AJ (2006) Community-acquired MRSA and pig-farming. Ann Clin Microbiol Antimicrob 5: 26.
  • Igimi S , Takahashi E & Mitsouka T (1990) Staphylococcus schleiferi subsp. coagulans subsp. nov., isolated from the external auditory meatus of dogs with external ear otitis. Int J Syst Bacteriol 40: 409411.
  • Ikeda T , Tamate N , Yamaguchi K & Makino S (2005) Mass outbreak of food poisoning disease caused by small amounts of staphylococcal enterotoxins A and H. Appl Environ Microbiol 71: 27932795.
  • Isigidi BK , Devriese LA , Godard C & Van Hoof J (1990) Characteristics of Staphylococcus aureus associated with meat products and meat workers. Lett Appl Microbiol 11: 145147.
  • Jablonski LM & Bohach GA (1997) Staphylococcus aureus. Food Microbiology Fundamentals and Frontiers ( Doyle MP , Beuchat LR & Montville TJ , eds), pp. 353357. American Society for Microbiology Press, Washington, DC.
  • Jarraud S , Peyrat MA , Lim A , Tristan A , Bes M , Mougel C , Etienne J , Vandenesch F , Bonneville M & Lina G (2001) egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J Immunol 166: 669677.
  • Jarraud S , Mougel C , Thioulouse J , Lina G , Meugnier H , Forey F , Nesme X , Etienne J & Vandenesch F (2002) Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 70: 631641.
  • Jarvis AW , Lawrence RC & Pritchard GG (1975) Glucose repression of enterotoxins A, B and C and other extracellular proteins in staphylococci in batch and continuous culture. J Gen Microbiol 86: 7587.
  • Jedrzkiewicz S , Kataeva G , Hogaboam CM , Kunkel SL , Strieter RM & McKay DM (1999) Superantigen immune stimulation evokes epithelial monocyte chemoattractant protein 1 and RANTES production. Infect Immun 67: 61986202.
  • Jones CL & Khan SA (1986) Nucleotide sequence of enterotoxin B gene from Staphylococcus aureus. J Bacteriol 166: 2933.
  • Jones TF , Kellum ME , Porter SS , Bell M & Schaffner W (2002) An outbreak of community-acquired foodborne illness caused by methicillin-resistant Staphylococcus aureus. Emerg Infect Dis 8: 8284.
  • Jordan EO (1930) The production by staphylococci of a substance causing food poisoning. JAMA 94: 1648.
  • Jordan EO & Burrows W (1934) Further observations on staphylococcus food poisoning. Am J Hyg 20: 604.
  • Keller GM , Hanson RS & Bergdoll MS (1978) Effect of minerals on staphylococcal enterotoxin B production. Infect Immun 20: 158160.
  • Kerouanton 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: 369375.
  • Khambaty FM , Bennett RW & Shah DB (1994) Application of pulse field gel electrophoresis to the epidemiological characterisation of Staphylococcus intermedius implicated in a food-related outbreak. Epidemiol Infect 113: 7581.
  • Khan SA , Nawaz MS , Khan AA & Cerniglia CE (2000) Transfer of erythromycin resistance from poultry to human clinical strains of Staphylococcus aureus. J Clin Microbiol 38: 18321838.
  • Kitai S , Shimizu A , Kawano J , Sato E , Nakano C , Uji T & Kitagawa H (2005) Characterization of methicillin-resistant Staphylococcus aureus isolated from retail raw chicken meat in Japan. J Vet Med 67: 107110.
  • Kitamoto M , Kito K , Niimi Y et al. (2009) Food poisoning by Staphylococcus aureus at a university festival. Jpn J Infect Dis 62: 242243.
  • Kornblum JB , Kreiswirth N & Projan SJ (1990) A polycistronic locus regulating exoprotein synthesis in Staphylococcus aureus. Molecular Biology of the Staphylococci ( Novick RP , ed), pp. 373402. VCH Publishers Inc., New York.
  • Kuroda M , Ohta T & Uchiyama I (2001) Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet 357: 12251240.
  • Kwon NH , Park KT , Jung WK et al. (2006) Characteristics of methicillin-resistant Staphylococcus aureus isolated from chicken meat and hospitalized dogs in Korea and their epidemiological relatedness. Vet Microbiol 117: 304312.
  • Lapeyre C , Janin F & Kaveri SV (1988) Indirect double sandwich ELISA using monoclonal antibodies for detection of staphylococcal enterotoxins A, B, C1 and D in food samples. Food Microbiol 5: 2531.
  • Lapeyre C , Maire T , Messio S & Dragacci S (2001) Enzyme immunoassay of staphylococcal enterotoxins in dairy products with cleanup and concentration by immunoaffinity column. J AOAC Int 84: 15871592.
  • Larkin EA , Carman RJ , Krakauer T & Stiles BG (2009) Staphylococcus aureus: the toxic presence of a pathogen extraordinaire. Curr Med Chem 16: 40034019.
  • Le Loir Y , Baron F & Gautier M (2003) Staphylococcus aureus and food poisoning. Genet Mol Res 2: 6376.
  • Lee YD , Moon BY , Park JH , Chang HI & Kim WJ (2007) Expression of enterotoxin genes in Staphylococcus aureus isolates based on mRNA analysis. J Microbiol Biotechnol 17: 461467.
  • Letertre C , Perelle S , Dilasser F & Fach P (2003) Identification of a new putative enterotoxin SEU encoded by the egc cluster of Staphylococcus aureus. J Appl Microbiol 95: 3843.
  • Li H , Llera A , Malchiodi EL & Mariuzza RA (1999) The structural basis of T cell activation by superantigens. Annu Rev Immunol 17: 435466.
  • Lina G , Bohach GA , Nair SP , Hiramatsu K , Jouvin-Marche E & Mariuzza R (2004) Standard nomenclature for the superantigens expressed by Staphylococcus. J Infect Dis 189: 23342336.
  • Macaluso L , Lapeyre C & Dragacci S (1998) Determination of influential factors during sample preparation for staphylococcal enterotoxin detection in dairy products. Analusis 26: 300304.
  • Mamone G , Picariello S , Caira F , Addeo P & Ferranti P (2009) Analysis of food proteins and peptides by mass spectrometry based techniques. J Chromatogr A 1216: 71307142.
  • Marrack P & Kappler J (1990) The staphylococcal enterotoxins and their relatives. Science 248: 705711.
  • Martin SE , Myers ER & Iandolo JJ (2001) Staphylococcus aureus. Foodborne Disease Handbook, Vol. 1 – Bacterial Pathogens ( Hui YH , Pierson MD & Gorham JR , eds), pp. 345381. Marcel Dekker Inc., New York, Basel.
  • McKay DM & Singh PK (1997) Superantigen activation of immune cells evokes epithelial (T84) transport and barrier abnormalities via IFN-gamma and TNF alpha: inhibition of increased permeability, but not diminished secretory responses by TGF-beta2. J Immunol 159: 23822390.
  • Mead PS , Slutsker L , Dietz V , McCaig LF , Bresee JS , Shapiro C , Griffin PM & Tauxe RV (1999) Food-related illness and death in the United States. Emerg Infect Dis 5: 607625.
  • Meyrand A , Atrache V , Bavai C , Montet MP & Vernozy-Rozand C (1999) Evaluation of an alternative extraction procedure for enterotoxin determination in dairy products. Lett Appl Microbiol 28: 411415.
  • Minor TE & Marth EH (1972) Staphylococcus aureus and staphylococcal food intoxications. A review. IV. Staphylococci in meat, bakery products and other foods. J Milk Food Technol 35: 228241.
  • Mitchell DT , Levitt DG , Schlievert PM & Ohlendorf DH (2000) Structural evidence for the evolution of pyrogenic toxin superantigens. J Mol Evol 51: 520531.
  • Morita TN , Patterson JE & Woodburn MJ (1979) Magnesium and iron addition to casein hydrolysate medium for production of staphylococcal enterotoxins A, B, and C. Appl Environ Microbiol 38: 3942.
  • Morris CA , Conway HD & Everall PH (1972) Food-Poisoning due to staphylococcal enterotoxin E. Lancet 300: 13751376.
  • Morse SA , Mah RA & Dobrogosz WJ (1969) Regulation of staphylococcal enterotoxin B. J Bacteriol 98: 49.
  • Mossel DAA , Corry JEL , Struijk CB & Baird RM (1995) Essentials of the microbiology of foods. A Textbook for Advanced Studies, pp. 146150. J. Wiley & Sons, Chichester.
  • Munson SH , Tremaine MT & Betley MJ (1998) Identification and characterization of staphylococcal enterotoxins types G and I from Staphylococcus aureus. Infect Immun 66: 33373348.
  • Normanno G , Corrente M , La Salandra G , Dambrosio A , Quaglia NC , Parisi A , Greco G , Bellacicco AL , Virgilio S & Celano GV (2007) Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy. Int J Food Microbiol 117: 219222.
  • Norrgran J , Williams TL , Woolfitt AR , Solano MI , Pirkle JL & Barr JR (2009) Optimization of digestion parameters for protein quantification. Anal Biochem 393: 4855.
  • Notermans S , Dufrenne J & In't Veld P (1991) Feasibility of a reference material for staphylococcal enterotoxin A. Int J Food Microbiol 14: 325331.
  • Noto MJ & Archer GL (2006) A subset of Staphylococcus aureus strains harboring staphylococcal cassette chromosome mec (SCCmec) type IV is deficient in CcrAB-mediated SCCmec excision. Antimicrob Agents Chemother 50: 27822788.
  • Novick RP , Schlievert P & Ruzin A (2001) Pathogenicity and resistance islands of staphylococci. Microbes Infect 3: 585594.
  • Oeljeklaus S , Meyer HE & Warscheid B (2009) New dimensions in the study of protein complexes using quantitative mass spectrometry. FEBS Lett 583: 16741683.
  • Omoe K , Hu DL , Takahashi-Omoe H , Nakane A & Shinagawa K (2003) Identification and characterization of a new staphylococcal enterotoxin-related putative toxin encoded by two kinds of plasmids. Infect Immun 71: 60886094.
  • Omoe K , Imanishi K , Hu DL et al. (2005) Characterization of novel staphylococcal enterotoxin-like toxin type P. Infect Immun 73: 55405546.
  • Ono HK , Omoe K , Imanishi K , Iwakabe Y , Hu DL , Kato H , Saito N , Nakane A , Uchiyama T & Shinagawa K (2008) Identification and characterization of two novel staphylococcal enterotoxins types S and T. Infect Immun 76: 49995005.
  • Orwin PM , Leung DY , Donahue HL , Novick RP & Schlievert PM (2001) Biochemical and biological properties of staphylococcal enterotoxin K. Infect Immun 69: 360366.
  • Orwin PM , Leung DYM , Tripp TJ , Bohach GA , Earhart CA , Ohlendorf DH & Schlievert PM (2002) Characterization of a novel staphylococcal enterotoxin-like superantigen, a member of the group V subfamily of pyrogenic toxins. Biochemistry 41: 1403314040.
  • Orwin PM , Fitzgerald JR , Leung DYM , Gutierrez JA , Bohach GA & Schlievert PM (2003) Characterization of Staphylococcus aureus Enterotoxin L. Infect Immun 71: 29162919.
  • Ostyn A , De Buyser ML , Guillier F , Groult J , Félix B , Salah S , Delmas G & Hennekinne JA (2010) First evidence of a food-poisoning due to staphylococcal enterotoxin type E in France. Eurosurveillance 15: 19528.
  • Papageorgiou A & Acharya K (2000) Microbial superantigens: from structure to function. Trends Microbiol 8: 369375.
  • Papageorgiou AC , Tranter HS & Acharya KR (1998) Crystal structure of microbial superantigen staphylococcal enterotoxin B at 1.5 A resolution: implications for superantigen recognition by MHC class II molecules and T-cell receptors. J Mol Biol 277: 6179.
  • Pereira ML , Do Carmo L , Dos Santos EJ , Pereira JL & Bergdoll MS (1996) Enterotoxin H in staphylococcal food poisoning. J Food Prot 59: 559561.
  • Pesavento G , Ducci B , Comodo N & Nostro AL (2007) Antimicrobial resistance profile of Staphylococcus aureus isolated from raw meat: a research for methicillin resistant Staphylococcus aureus (MRSA). Food Control 18: 196200.
  • Pinchuk IV , Beswick EJ , Saada JI , Suarez G , Winston J , Mifflin RC , Di Mari JF , Powell DW & Reyes VE (2007) Monocyte chemoattractant protein-1 production by intestinal myofibroblasts in response to staphylococcal enterotoxin a: relevance to staphylococcal enterotoxigenic disease. J Immunol 178: 80978106.
  • Pumphrey N , Vuidepot A , Jakobsen B , Forsberg G , Walse B & Lindkvist-Petersson K (2007) Cutting edge: evidence of direct TCR alphachain interaction with superantigen. J Immunol 179: 27002704.
  • Qi Y & Miller KJ (2000) Effect of low water activity on staphylococcal enterotoxin A and B biosynthesis. J Food Prot 63: 473478.
  • Ren K , Bannan JD , Pancholi V , Cheung AL , Robbins JC , Fischetti VA & Zabriskie JB (1994) Characterization and biological properties of a new staphylococcal exotoxin. J Exp Med 180: 16751683.
  • Rosec JP , Guiraud JP , Dalet C & Richard N (1997) Enterotoxin production by staphylococci isolated from foods in France. Int J Food Microbiol 35: 213221.
  • Rosenbach FJ (1884) Microorganismen bei den Wund-Infections. Krankheiten des Menschen. pp. 1122. J. F. Bergmann, Wiesbaden, Germany.
  • Schad EM , Zaitseva I , Zaitsev VN , Dohlsten M , Kalland T , Schlievert PM , Ohlendorf DH & Svensson LA (1995) Crystal structure of the superantigen staphylococcal enterotoxin type A. EMBO J 14: 32923301.
  • Schlievert PM & Case LC (2007) Molecular analysis of staphylococcal superantigens. Methods Mol Biol 391: 113126.
  • Schmid D , Fretz R , Winter P et al. (2009) Outbreak of staphylococcal food intoxication after consumption of pasteurized milk products, June 2007, Austria. Wien Klin Wochenschr 121: 125131.
  • Schmitt M , Schuler-Schmidt U & Schmidt-Lorenz W (1990) Temperature limits of growth, TNase and enterotoxin production of Staphylococcus aureus strains isolated from foods. Int J Food Microbiol 11: 120.
  • Shafer WM & Iandolo JJ (1978) Chromosomal locus for staphylococcal enterotoxin B. Infect Immun 20: 273278.
  • Shalita Z , Hertman I & Sarid S (1977) Isolation and characterization of a plasmid involved with enterotoxin B production in Staphylococcus aureus. J Bacteriol 129: 317325.
  • Sheehan DG , Jervis HR , Takeuchi A & Sprinz H (1970) The effect of staphylococcal enterotoxin on the epithelial mucosubstance of the small intestine of rhesus monkeys. Am J Pathol 60: 118.
  • Shimizu A , Fujita M , Igarashi H , Takagi M , Nagase N , Sasaki A & Kawano J (2000) Characterization of Staphylococcus aureus Coagulase Type VII Isolates from Staphylococcal Food Poisoning Outbreaks (1980-1995) in Tokyo, Japan, by Pulsed-Field Gel Electrophoresis. J Clin Microbiol 38: 37463749.
  • Shupp JW , Jett M & Pontzer CH (2002) Identification of a transcytosis epitope on staphylococcal enterotoxins. Infect Immun 70: 21782186.
  • Smith JL , Buchanan RL & Palumbo SA (1983) Effect of food environment on staphylococcal enterotoxin synthesis: a review. J Food Prot 46: 545555.
  • Su YC & Wong AC (1996) Detection of staphylococcal enterotoxin H by an enzyme-linked immunosorbent assay. J Food Prot 59: 327330.
  • Sugiyama H & Hayama T (1965) Abdominal viscera as site of emetic action for staphylococcal enterotoxin in monkey. J Infect Dis 115: 330336.
  • Sullivan R (1969) Effects of enterotoxin B on intestinal transport in vitro. Proc Soc Exp Biol Med 131: 11591162.
  • Surgalla M , Bergdoll MS & Dack GM (1953) Some observations on the assay of staphylococcal enterotoxin by the monkey feeding test. J Lab Clin Med 41: 782788.
  • Swaminathan S , Furey W , Pletcher J & Sax M (1995) Residues defining V beta specificity in staphylococcal enterotoxins. Nat Struct Biol 2: 680686.
  • Tatini SR (1973) Influence of food environments on growth of Staphylococcus aureus and production of various enterotoxins. J Milk Food Technol 36: 559563.
  • Tatini SR (1976) Thermal stability of enterotoxins in food. J Milk Food Technol 39: 432438.
  • Thaikruea L , Pataraarechachai J , Savanpunyalert P & Naluponjiragul U (1995) An unusual outbreak of food poisoning. Southeast Asian J Trop Med Public Health 26: 7885.
  • Thomas DY , Jarraud S , Lemercier B , Cozon G , Echasserieau K , Etienne J , Gougeon ML , Lina G & Vandenesch F (2006) Staphylococcal enterotoxin-like toxins U2 and V, two new staphylococcal superantigens arising from recombination within the enterotoxin gene cluster. Infect Immun 74: 47244734.
  • Thomas D , Chou S , Dauwalder O & Lina G (2007) Diversity in Staphylococcus aureus enterotoxins. Chem Immunol Allergy 93: 2441.
  • Thomas D , Dauwalder O , Brun V , Badiou C , Ferry T , Etienne J , Vandenesch F & Lina G (2009) Staphylococcus aureus superantigens elicit redundant and extensive human Vbeta patterns. Infect Immun 77: 20432050.
  • Thota H , Tatini SR & Bennett RW (1973) Effects of temperature, pH and NaCl on production of staphylococcal enterotoxins E and F. Abstr Ann Meet Am Soc Microbiol, 1: 11.
  • Todd E , Szabo R , Gardiner MA et al. (1981) Intoxication staphylococcique liée à du caillé de fromagerie – Québec. Rapport hebdomadaire des maladies du Canada 7: 171172.
  • Tremaine MT , Brockman DK & Betley MJ (1993) Staphylococcal enterotoxin A gene (sea) expression is not affected by the accessory gene regulator (agr). Infect Immun 61: 356359.
  • Troller JA (1971) Effect of water activity on enterotoxin B production and growth of Staphylococcus aureus. Appl Microbiol 21: 435439.
  • Troller JA (1986) The water relations of foodborne bacterial pathogens – an updated review. J Food Prot 49: 656670.
  • Troller JA & Stinson JV (1975) Influence of wateractivity on growth and enterotoxin formation by Staphylococcus aureus in foods. J Food Sci 40: 802804.
  • Van den Bussche RA , Lyon JD & Bohach GA (1993) Molecular evolution of the staphylococcal and streptococcal pyrogenic toxin gene family. Mol Phylogenet Evol 2: 281292.
  • Van Duijkeren E , Ikawaty R , Broekhuizen-Stins MJ , Jansen MD , Spalburg EC , de Neeling AJ , Allaart JG , van Nes A , Wagenaar JA & Fluit AC (2007) Transmission of methicillin-resistant Staphylococcus aureus strains between different kinds of pig farms. Vet Microbiol 126: 383389.
  • Van Loo IHM , Diederen BMW , Savelkoul PHM , Woudenberg JHC , Roosendaal R , van Belkum A , Lemmens-den Toom N , Verhulst C , van Keulen PHJ & Kluytmans JAJW (2007) Methicillin-resistant Staphylococcus aureus in meat products, the Netherlands. Emerg Infect Dis 13: 17531755.
  • Varaldo PE , Kilpper-Balz R , Biavasco F , Satta G & Scheifer KH (1988) Staphylococcus delphini sp. nov., a coagulase-positive species isolated from dolphins. Int J Syst Bacteriol 38: 436439.
  • Vernozy-Rozand C , Mazuy C , Prevost G , Lapeyre C , Bes M , Brun Y & Fleurette J (1996) Enterotoxin production by coagulase negative staphylococci isolated from goats’ milk and cheese. Int J Food Microbiol 30: 271280.
  • Vojtov N , Ross HF & Novick RP (2002) Global repression of exotoxin synthesis by staphylococcal superantigens. P Natl Acad Sci USA 99: 1010210107.
  • Wei HL & Chiou CS (2002) Molecular Subtyping of Staphylococcus aureus from an Outbreak Associated with a Food Handler. Epidemiol Infect 128: 1520.
  • Wieneke AA (1991) Comparison of four kits for the detection of staphylococcal enterotoxin in foods from outbreaks of food poisoning. Int J Food Microbiol 14: 305312.
  • Woodburn MJ , Morita TN , Rowe K & Park SS (1978) Staphylococcal enterotoxin A and C production with various sugars as energy source. J Food Prot 41: 643646.
  • Woolaway MC , Bartlett CLR , Wieneke AA , Gilbert RJ , Murell HC & Aureli P (1986) International outbreak of staphylococcal food poisoning caused by contaminated lasagne. J Hyg 96: 6773.
  • Wulf M & Voss A (2008) MRSA in livestock animals – an epidemic waiting to happen? Clin Microbiol Infect 14: 519521.
  • Zell C , Resch M , Rosenstein R , Albrecht T , Hertel C & Gotz F (2008) Characterization of toxin production of coagulase negative staphylococci isolated from food and starter cultures. Int J Food Microbiol 49: 15771593.
  • Zhang S , Iandolo JJ & Stewart GC (1998) The enterotoxin D plasmid of Staphylococcus aureus encodes a second enterotoxin determinant (sej). FEMS Microbiol Lett 168: 227233.

Supporting Information

  1. Top of page
  2. Abstract
  3. A worldwide review of outbreaks related to coagulase-positive staphylococci and their toxins: the story
  4. Characteristics and behaviour of S. aureus in the food environment
  5. Toxinogenic conditions and characteristics of SEs
  6. SFPOs: symptomatology; reporting system including EU control; monitoring schemes; occurrence and analytical methods used
  7. Concluding remarks
  8. References
  9. Supporting Information
fmr311-sup-0001-FigureS1.docWord document271KFigure S1. Reporting scheme for food poisoning outbreaks at European Union level.

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