Critical environmental limits growth and ochratoxin A production

The most important abiotic factors influencing growth and ochratoxin A production include water availability, temperature and, when the grain is moist, gas composition (Magan et al., 2003a). The interaction between these variables usually determines whether mold growth will occur and, if so, the composition and relative rate of development of the fungal community. An accurate determination of the marginal conditions for growth and ochratoxin A production by species such as P. verrucosum and A. ochraceus is important, since it can be used to develop guidelines and risk prediction tools for the entire food chain. Such studies must generate detailed information on the ability of numerous isolates of these species to colonize grain matrices over a relatively wide range of interacting conditions.

During respiration of damp grain, O2 is utilized and CO2 is produced. The O2 and CO2 in the inter-granular atmosphere are important factors in determining the pattern of fungal colonization of grain during storage. Most molds, including P. verrucosum and A. ochra-ceus, are obligate aerobes, so increasing the level of CO2 should inhibit their growth. Yet, only a few studies have been conducted regarding the impact and interactions of CO2 level, water activity (aw) and temperature on fungal growth, particularly P. verrucosum and A. ochraceus, the main ochratoxin A producers on wheat during storage.

The occurrence of ochratoxin A in grain on farms usually is attributed to insufficient drying or to excessively long pre-drying storage (Jonsson and Pettersson, 1992). Studies of the safe storage period for cereal grains are few, and are based on visible molding (Kreyger, 1972), dry-matter loss (Steel et al., 1969; White et al., 1982) or loss of seed germination

(Kreyger, 1972; White et al., 1982) rather than on ochratoxin A accumulation. For maize, the maximum allowable storage time has been estimated based on the time before dry matter loss exceeds 0.5% (Steel et al., 1969). This loss is estimated to correspond to the loss of one US grade, which is based on visible inspection. Visible molding may be an unreliable criterion for ochratoxin A production, because considerable losses can occur before molding is visible, depending on whether the conditions favor fungal growth and sporulation (Seitz et al., 1982).

Measurement of respiration is widely used to estimate fungal growth, biomass and dry-matter loss. The rate of CO2 production also has been used to estimate total living microbial biomass in soil (Anderson and Domsch, 1975). CO2 production was highly correlated with ergosterol content (r = 0.98) when Eurotium repens colonized maize (Martin et al., 1989). Studies of respiration rates under different environmental conditions have enabled the development of a mathematical model, that describes the effect of aw, i.e., water availability, and temperature on safe storage time for cereal grain before obvious growth of P. verruco-sum and formation of ochratoxin A. Thus, the logistic model of Lindblad et al. (2004) relates populations of P. verrucosum, measured as colony forming units (CFUs), to the probability of exceeding the European legislative limit of 5 ng/g of ochratoxin A in cereal grains under different aw x temperature storage regimes. They suggested a threshold of 1000 CFUs of P. verrucosum per gram of grain as a threshold limit for the probability of risk of excessive ochratoxin A contamination. Cairns-Fuller et al. (2005) suggested that growth could occur under some conditions at aw = 0.80, although ochratoxin A production may be limited, if it occurs at all, if aw < 0.83. Thus, there is a "zone of uncertainty" (Fig. 2) for ochratoxin A contamination between 15 and 17.5% moisture content in terms of whether there is a high risk that ochratoxin A will be produced.

The general relationship between water availability, temperature, growth and ochratoxin A production has been discerned (Cairns-Fuller, 2004; Cairns-Fuller et al., 2005). Rapid growth by P. verrucosum and A. ochraceus occurs at aw = 0.98-0.99, i.e., 27-30% moisture content, between 10 and 25°C, but is almost completely inhibited at aw = 0.80-0.83, i.e., 17.5-18% moisture content. No ochratoxin A is produced at aw = 0.80, although some toxin may be produced at aw = 0.85 (19% moisture content) at 15 and 20°C. Optimum conditions for ochratoxin A production were aw = 0.93-0.98 (23.5-27.5% moisture content) at 10-25°C on wheat grain incubated for up to 56 days. On wheat grain, 7-14 days are required for ochratoxin A to begin to be produced at levels above the legislative limit (Cairns-Fuller et al., 2005). Contour maps of the optimum and marginal conditions of water and temperature for growth and OTA production have been constructed. Approximately 17-18% moisture content, i.e., aw = 0.80-0.83, is the lower limit for growth and/or ochratoxin A production in wheat grain (Cairns-Fuller et al., 2005). Thus, it is essential that grain is dried to lower moisture contents as quickly as possible regardless of the drying system employed. To avoid initiation of molding by xerophilic Eurotium species, drying to < 14.5% moisture content, i.e., aw = 0.70 (Magan et al., 2003b) is essential. This level must be maintained during storage and transport to effectively prevent the accumulation of ochratoxin A.

Tests of controlled atmospheres to control ochratoxin A contamination in cereal grains have found that spore germination is not affected, but that germ tube elongation is significantly inhibited by 50% CO2, especially at aw = 0.90-0.995, for both P. verrucosum and A. ochraceus (Cairns-Fuller, 2004). Growth and ochratoxin A production were highest in air, followed by 25% and 50% CO2 regardless of the aw level tested. Generally, increased CO2 and decreased aw work together to reduce growth, although this interaction was not necessarily synergistic.

Table 1. The key control points, tools and potential effects on the entrance of ochratoxin A into the food production chain.

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