General properties of SEs and SEls and genomic location of the encoding genes.
Staphylococcal enterotoxins (SEs) and SE-like toxins (SEls) are the most notable virulence factors associated with Staphylococcus aureus. They are involved in food poisoning, toxic shock syndrome and staphylococcal infectious diseases in human. In dairy practise, the initial numbers of S. aureus play an important role especially at the beginning of the milk fermentation within the first 6 h or in 24-h-old cheese. As we presented in our previous works, one of the most effective tools to inhibit S. aureus growth is by adding a sufficient amount of active dairy starters, which are able to produce lactic acid very rapidly. Thus, by inhibiting the growth of S. aureus the production of SEs may be reached. Based on this study focusing on the effect of temperature, pH, water activity and initial numbers of lactic acid bacteria on the growth and the ability of S. aureus 14733 to produce SED, we consider it as a strong SED producer. The SED production was not limited with the incubation temperatures and the NaCl addition related to traditional cheese manufacture. As this isolate comes originally from such an artisanal cheese production, we can expect that other strong SE producer could be present in milk or environment. Besides strict prerequisites approach in production hygiene, it is necessary to add the starters ensuring the initial dominance of lactic acid bacteria (LAB) and supporting the growth of the natural LAB present in raw milk.
- staphylococcal enterotoxins
- growth inhibition
- water activity
- lactic acid bacteria
- predictive microbiology
In Slovakia, the manufacture of “Bryndza” cheese from ewes’ lump cheese is of great importance to preserve the national gastronomic heritage. In the traditional way of production, it is produced immediately after milking from raw milk in upland cottages. The cheese is curdled with rennet, fermented by native lactic acid bacteria (LAB) and ripened for 7–10 days. Then, it is usually sent to a cheese factory, where the next technology processes (including salting) take part resulting in the production of the final soft “Bryndza” cheese [1, 2].
As coagulase-positive staphylococci are ubiquitous in milk, the control of
The growth of
As a pathogen,
In addition, some strains of
1.1. Biological characteristics of staphylococcal enterotoxins
To date, 23 SEs and enterotoxin-like (SEls) types have been described based on their antigenicity. They have sequentially been assigned a letter of the alphabet in order of their discovery (SEA, SEB, ….., SElX) [10–12]. SEA and SEB were the first one SEs characterized by Casman and Bergdoll in 1959 and 1960. From the late 1990s, new toxins were discovered one after another by sequencing the entire genome of
SEs and SEls proteins are globular, single peptides with molecular weights ranging from 19 to 29 kDa [16, 19]. Their molecular composition is characterized by containing only two residues of half cystine and one or two residues of tryptophane . They are rich in lysine, aspartic and glutamic acids and tyrosine. Most of them possess a cysteine loop required for proper conformation and which is probably involved in the emetic activity . Overall, 15% of amino acid residues are entirely conserved in SEs and occurred in four stretches of primary sequence located either centrally or at the C-terminus .
As it is seen in Table 1, all genes for SEs and SEls are located on mobile genetic elements, including plasmids, transposons, prophages,
|Toxin||Molecular weight (kDa)||Emetic activity||Super-antigenic activity||gene||Genetic element||Accessory genetic element|
|SEA||27.1||+||+||prophage||ΦSa3ms; ΦSa3mw; Φ252B; ΦNM3; ΦMu50a|
|SEB||28.4||+||+||chromosome, SaPI, plasmid||pZA10; SaPI3|
|SEC1-SEC3||27.5-27.6||+||+||SaPI||SaPIn1; SaPIm1; SaPImw2; SaPIbov1|
|SElJ||28.6||nd||+||plasmid (pIB485, pF5)||pIB485-like; pF5|
|SElK||25.3||nd||+||SaPI||ΦSa3ms; ΦSa3mw; SaPI1; SaPI3; SaPIbov1; SaPI5|
|SElL||24.7||-||+||SaPI||SaPIn1; SaPIm1; SaPImw2; SaPIbov1|
|SElP||26.7||nd||+||prophage (Sa3n)||ΦN315; ΦMu3A|
|SElQ||25.2||-||+||SaPI||ΦSa3ms; ΦSa3mw; SaPI1; SaPI3; SaPI5|
|SER||27.0||+||+||plasmid (pIB485, pF5)||pIB485-like; pF5|
Distribution of superantigens (SAg) gene is strain dependent. As reported by Jin and Yamada , 80% of human isolates contain at least one of these genes, including 50% which contain the
Staphylococcal enterotoxins (SEs) and SE-like toxins (SEls) are the most notable virulence factors associated with
Besides superantigen activity, SEs (but not SEls) act also as a potent gastrointestinal toxins causing emesis. SEs can penetrate the epithelium, accumulate in the submucosa, enter the blood stream and circulate through the body allowing activation of local and systemic immune response by their interaction with antigen-presenting- and T-cells [16, 25]. SEA binds in submucosa to the submucosal mast cells or directly to neuron cells [10, 26]. The binding of SEA to an unidentified receptor expressed on the surface of these cells induces the degranulation, resulting in the release of 5-hydroxytryptamine (5-HT). This stimulates 5-HT receptor on adjacent vagal afferent nerves in the intestine resulting in depolarization of the vagal nerves and stimulation of the vomiting centre in the brain [10, 16]. The release of 5-HT can be direct after interaction of SEA with enterochromaffin cells or neurons or indirect through the release of pro-inflammatory molecules or free-radical formation [13, 26]. It appears that besides 5-HT, also the serotonin pathway is involved in emesis, since serotonin is an important signalling mediator in the gastrointestinal tract and can activate enteric neurons, stimulate muscle responses and enhance secretion . Release of inflammatory mediators (histamine, leukotrienes and neuroenteric peptide substance P) is responsible for local damage of gastrointestinal tract. The most severe lesions appear in the stomach and the upper part of the small intestine. Due to the inhibition of water and electrolyte reabsorption in small intestine, diarrhoea may occur [16, 25]. The dose of SEs inducing emetic activity in monkeys after oral administration ranged from 5 to 600 μg/animal . The minimal dose required for intoxication in human is 144 ± 50 ng/humans for SEA and 0.4 μg/humans for SEB. All the SEls that were tested induced emetic reaction in monkeys at a dose of 100 μg/kg .
Although emetic and superantigenic activities are two separate functions localized on separate domains of the proteins, there is a high correlation between these activities and in most cases a loss of superantigen activity results in loss of emetic activity as [11, 18]. However, the role of SEls in human food-poisoning outbreaks currently remains unclear .
1.2. Prevalence of staphylococcal enterotoxins in humans and animals
Approximately 20–60% of humans are permanent or intermittent carriers of
For SEB and SEC, the amounts may exceed 100 μg/ml, compared with 1–10 μg/ml for SEA and SED. Some indications exists that low amounts of SEB are produced already in early exponential growth phase and it can appear in cultures as early as 4–6 h. However, SEA and SED are produced in foods under a wider range of pH, redox potential (
1.3. Resistance of staphylococcal enterotoxins to environmental factors
SEs are highly stable, resist most proteolytic enzymes (pepsin or trypsin) thus keeping their activity in the digestive tract after ingestion. They are also resisting chymotrypsin, rennin and papain. Based on the poor ability of proteolytic enzymes to affect the biological activity of SEs, it is not surprising that SE levels are unaffected by proteolytic or enteric bacteria. Lactic acid bacteria (LAB), however, do decrease SE concentrations. It could not be accounted for the addition of lactic acid alone, suggesting the involvement of specific enzymes of other metabolites. Alternatively, selective physical adsorption of toxin to LAB may have occurred during removal of cells to obtain supernatants from toxin assays .
1.3.1. Heat resistance
SEs are in general produced in a temperature range of 10–46°C, with the optimum at 40–45°C. Their production is substantially reduced at 20–25°C and it is unlikely that they are produced at temperatures below 10°C [19, 33, 34]. They can resist both the process of milk pasteurization and sterilization of canned foods [20, 36]. The heat stability of SEs is not the same for all of them and depends on the food matrix and toxin concentration. It decreases in the order SEC>SEB>SEA and significantly reduces in acidic conditions .
The thermal inactivation can generally be described by
1.3.2. Acid tolerance
The pH range allowing the production of SEs is limited in higher degree as the growth of a producing strain. Optimum enterotoxin production occurs at pH 6–7 and it is influenced by environmental conditions, carbon and nitrogen source and salt level . Already pH 5.0 is generally considered as a lower limit pH value. The SEA is produced under a wider range of pH than SEB or SEC [19, 38]. SEB can be destroyed by pepsin digestion at pH 2 but it is resistant at higher pHs, which are normal conditions in the stomach after food ingestion .
1.3.3. Salt resistance
A characteristic feature that distinguishes
With respect to enterotoxins production requirements, values of water activity for their production are mostly in the same range as for the growth of the producer. In food with decreased water activity and at aerobic conditions, the enterotoxins can be produced even if the
2. Effect of intrinsic and extrinsic factors on the growth dynamics of
S. aureus and enterotoxin D production
Many intrinsic and extrinsic factors affect not only the growth of food-borne microbial pathogens but also metabolism and production of toxins. As SEs are extremely heat-stable and cannot be inactivated by measures such as heating of food, it is crucial to prevent their formation by preventing
2.1. Effect of temperature and water activity on the growth dynamics of
S. aureus and enterotoxin D production
The growth of
|Model equation/validation coefficients|
In general, a decrease of water activity prolonged the lag-phase duration and slowed down growth rate, until the minimal water activity was reached. At 18°C and
It was also noticed that except for cases when
The range in which the SED was (full markers) or was not (empty markers) detected during the growth of
At 21°C, the SED was not produced as sooner as after 24 h of incubation and even not at almost optimal water activity value (
The most rapid SED production was naturally observed at 37°C. At the higher water activity values,
Further, the Gibson’s model secondary model Gibson et al.  was used to characterise the influence of water activity and temperature on the specific growth rate of S. aureus 14733. Growth of S. aureus 14733 in nutrient broth was positively determined with the increasing value of water activity, resulting in shortening of the lag phase duration and more intensive growth in exponential phase. The growth of S. aureus in dependence on water activity at 18, 21 and 37 °C can be characterised by equations summarised in
For the Gibson’s model, the discrepancy factors ranged from 9.6% to 17.5%, so the model can be considered as very consistent. This model can be also used for the determination of optimal water activity value at each temperature. So, the optimal growth of S. aureus 14733 in nutrient broth at 18 °C can be expected at aw = 0.994, at 21°C at aw = 0.980 and at 37°C at water activity value of 0.986. The prediction of lag phase duration would be estimated with 22-33 % error according to Davey’s model. Taking into account that 12-37% of the bound of reliability during cultivation methods is tolerable; these finding demonstrate that the duration of lag phase and also the growth rate of S.
With regard to the EU Commission Regulation 1441/2007 , the total
Based on the results,
2.2. Effect of temperature, pH value and water activity on the growth dynamics of
S. aureus and enterotoxin D production
As it was mentioned above, the traditional artisanal production of “Bryndza” cheese includes fermentation in the presence of LAB, ripening at temperatures from 18 to 21°C and salting with 2–5% NaCl resulting in final soft cheese [1, 2]. In this context, the growth and the production of SED by
As it is shown in Figure 4, the combination of reduced pH value (to values 6.0 and 5.5) and water activity value (0.99 and 0.97) did not inhibit the growth dynamic of
Taking into account the SED production by
|pH||(+) log CFU/ml|
|18||6.0||–||0.221||5.8 (28 h)|
|5.5||–||0.320||5.7 (42 h)|
|5.0||–||0.119||4.9 (42 h)|
|6.0||0.99||0.246||5.5 (28 h)|
|6.0||0.97||0.239||4.9 (28 h)|
|5.5||0.99||0.364||5.4 (28 h)|
|21||6.0||–||0.392||6.2 (22 h)|
|5.5||–||0.375||6.3 (22 h)|
|5.0||–||0.306||6.1 (32 h)|
|6.0||0.99||0.378||6.1 (22 h)|
|6.0||0.97||0.295||6.5 (32 h)|
|5.5||0.99||0.389||6.0 (22 h)|
|5.5||0.97||0.258||6.2 (32 h)|
|37||6.0||–||2.287||5.2 (4 h)|
|5.5||–||2.057||3.9 (4 h)|
|5.0||–||1.064||3.3 (6 h)|
|6.0||0.99||1.847||4.8 (4 h)|
|6.0||0.97||1.534||3.6 (4 h)|
|5.5||0.99||1.403||3.9 (4 h)|
|5.5||0.97||1.073||4.9 (6 h)|
In the term of SEs production inhibition during cheese manufacture, a rapid decrease in pH value down to pH 5.0 as fast as possible within first 6 h of cheese production is strongly recommended. This was also emphasized by Delbes et al. . They observed that the critical phase of exponential phase of staphylococci occurs mainly within the first 6 h and the rapid pH decrease within this phase significantly contributed to the inhibition of staphylococci in young cheese. Moreover, if pH exceeded 6.3 within the first 6 h, also the SEs production was detected in cell concentration higher than 5 log CFU/g.
With regard to the study of Valihrach et al. , based on a total of 24 examinations of SED presence in the nutrient broth in dependence to mutual effect of water activity (
2.3. Effect of lactic acid bacteria addition and temperature on the growth dynamics of
S. aureus and enterotoxin D production
In dairy practise, the initial numbers of
During co-cultivation of
So, even pH and lactic acid play only a minor role in growth inhibition, we may suppose that the expression of genes responsible for SEs production may be influenced negatively. In addition, the
During co-cultivation of 14733 isolate with Fresco culture, the SED was produced only after reaching
Based on this study focusing on the effect of temperature, pH, water activity and initial numbers of lactic acid bacteria on the growth and the ability of
In terms of SEs production inhibition during cheese manufacture, a rapid decrease in pH value down to pH 5.0 as fast as possible within the first 6 h of cheese production is strongly recommended. The minimal starter culture addition needed for
Artisanal raw milk cheese production poses a few critical factors limiting its safety. With reference to the growth of
We thank MSc. Zuzana Sirotná, MPH, and her co-workers for the SED detection. The results of the research in this chapter were supported by the Slovak Research and Development Agency, project no. APVV-15-0006.
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