Control of Growth and Toxin Production

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The safety of certain foods is achieved by using one or more methods to inhibit the growth of C. botulinum and toxin production. This is the best solution for foods with a high humidity content that cannot be treated at temperatures high enough to kill C. botulinum spores without altering their organoleptic characteristics.

1. Control Through Food Storage Temperature

As the lowest growth temperatures for proteolytic and nonproteolytic strains of C. botulinum are 10°C (190) and 3.3°C (191), respectively, refrigerated (4-8°C) storage cannot be the sole protection against botulism. In nonproteolytic strains, growth and toxin production in food may occur when the shelf life of the product is sufficiently long. Proteolytic strains grow in food when temperature abuse occurs during storage. Proteolytic strains have been shown to produce neurotoxin after one week at 15 °C or after 2-3 days at 20°C (190). At the same storage temperature, the higher the number of bacteria inoculated, the earlier the production of the toxin (192,193).

2. Control Through pH

The minimum pH value required for most proteolytic strains to grow is 4.6 (188), but for several strains it may be over 5.0 (177). For nonproteolytic strains the limiting pH is above 5.0. The inhibition of spore outgrowth and toxin production in high-moisture, low-protein foods such as vegetables is achieved by the addition of acidulants to obtain an equilibrium pH of 4.6. However, the inhibiting action of pH is neutralized if molds, yeasts (194), or bacilli (195) grow in food because their presence increases pH (effect of metabiosis). In high-protein foods, control using pH is counteracted by the buffering activity of proteins (196). In cured meats, starters, either natural or added to the product, ferment rapidly to prevent toxin production. The risk of C. botulinum growing in fish is higher because fish ferment more slowly and have a low carbohydrate concentration, delaying acidification. Fish are rendered safe by the additional measures of salt or refrigerated storage. In dairy products, pH plays a decisive role in the control of C. botulinum. Fermented milks have never been involved in botulism cases.

3. Control Through aw or NaCl

Growth and toxin production are influenced by the quantity of free water available for metabolic activity. Salt, like other solutes such as potassium chloride, saccarose, or lactose, reduces aw values. While proteolytic strains are incapable of growing at aw = 0.935, a condition obtained with a 10% NaCl solution in the substrate, nonproteolytic strains require a higher value (aw 0.970), which is obtained with a 5% NaCl solution (177). However, curing at higher temperatures does not prevent the production of botulinum toxin in home-made raw ham (197). In fish, a NaCl content of 5% in the aqueous phase if products are refrigerated, or of 10% if they are stored at room temperature, is enough to prevent the risk of botulism. Since the effect of salt is influenced by pH, the amount of NaCl used for these products can be greatly reduced by decreasing pH values (198).

4. Control Through Additives

Nitrite has long been used in the meat-processing industry to inhibit outgrowth and toxin production. Its efficacy, however, depends on the complex interaction of several other factors (pH, aw, T, etc.) (177). The risks of carcinogenicity and teratogenicity posed by nitrosamines, resulting from the reaction of nitrite with amines, have spurred the search for alternatives to permit the reduction or removal of nitrite. Sorbic acid and its salts are capable of delaying outgrowth and toxin production in several types of cured meat (199). Their action increases as pH decreases; the inhibiting effect depends on the concentration of undissociated sorbic acid. As a secondary function, polyphosphates also enhance other inhibiting techniques (200,201). Ascorbic acid can reduce the requirement or nitrite in meat (202), and liquid smoke can reduce the salting of fish (203), while C. botulinum growth and toxin formation remain inhibited. Essential oils (garlic, onion, black pepper, cloves, origanum), or alcohol extracts (nutmeg, garlic, rosemary, thyme, sage) of several aromatic plants have been found to inhibit spore germination or vegetative growth (204-206). The presence of essential oils was inadequate to prevent botulism from garlic in oil-fried onions in the United States and from pesto sauce containing garlic and basil in Italy (L. Fenicia and P. Aureli unpublished data, 1997). A good safety margin against C. botulinum may also be obtained by adding natural preservatives, or biopreservatives, such as lactic acid bacteria or their purified metabolites, bacteriocines. Biopreservatives decrease pH either by transforming carbohydrates into organic acids, lactic acid in particular, or through production of acidic metabolites such as carbon dioxide, oxygen peroxide, carbon anhydride, and bacteriocines. Nisin, a well-known biopreservative used in vegetables and spread cheeses, has an indirect antibotulinal effect. Nisin permits a reduction in thermal treatments and in salt and phosphate levels, which in turn increases the water concentration of products stored at room temperature (207). Lysozyme has been proposed to control C. botulinum growth, but it has been recently demonstrated that the presence of this enzyme increases the risk of growth of nonproteolytic C. botulinum strains (208).

5. Control Through Combined Factors

In the preparation of several foods, the growth of C. botulinum growth is controlled by using a combination of different factors: pH, aw, and preservatives coupled with various processes and storage conditions. This approach has also been adopted to reduce the risk of C. botulinum growth in fresh, minimally processed foods refrigerated for extended duration, which pose a greater risk of intoxication if abused. There are several studies of combined control methods for various foods.

These results are only valid for the specific products or testing conditions and may not be extrapolated to other foods. Yet another recent approach utilizes predictive models to quantify the effects of the different factors that influence C. botulinum growth and toxin production (209).

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