A Comprehensive Review of Variability in the Thermal Resistance (D-Values) of Food-Borne Pathogens—A Challenge for Thermal Validation Trials

Abstract

The thermal processing of food relies heavily on determining the right time and temperature regime required to inactivate bacterial contaminants to an acceptable limit. To design a thermal processing regime with an accurate time and temperature combination, the D-values of targeted microorganisms are either referred to or estimated. The D-value is the time required at a given temperature to reduce the bacterial population by 90%. The D-value can vary depending on various factors such as the food matrix, the bacterial strain, and the conditions it has previously been exposed to; the intrinsic properties of the food (moisture, water activity, fat content, and pH); the method used to expose the microorganism to the thermal treatment either at the laboratory or commercial scale; the approach used to estimate the number of survivors; and the statistical model used for the analysis of the data. This review focused on Bacillus cereus, Cronobacter sakazakii, Escherichia coli, Listeria monocytogenes, and Clostridium perfringens owing to their pathogenicity and the availability of publications on their thermal resistance. The literature indicates a significant variation in D-values reported for the same strain, and it is concluded that when designing thermal processing regimes, the impact of multiple factors on the D-values of a specific microorganism needs to be considered. Further, owing to the complexity of the interactions involved, the effectiveness of regimes derived laboratory data must be confirmed within industrial food processing settings.

Genetic determinants of thermal resistance in foodborne bacterial pathogens

“…The survivors are typically determined by linear and Weibull mathematical models, which can thereby predict the outcome/effect of any processing treatment using heat on the inactivation of these bacteria (Forghani et al, 2018). A review by Soni et al (2022b) indicated the variability in D values reported in literature, wherein there are serval factors that contribute to their resistance. However, at times the mechanism is not acquired but is inherited.…”

“…A review by Soni et al. (2022b) indicated the variability in D values reported in literature, wherein there are serval factors that contribute to their resistance. However, at times the mechanism is not acquired but is inherited.…”

“…There is evidence on thermal tolerance and resistance of Listeria species in different food matrices, for example, in milk, where the minimum high‐temperature, short‐time treatment regime imposed by U.S. Food and Drug Administration (71.7°C, 15 s) was not enough to eliminate L. monocytogenes (Shen et al., 2014). However, effect of the food matrix on thermal resistance is a mechanism well understood and reported (Soni et al., 2022b). It has been demonstrated that the orphan response regulator in L. monocytogenes is reported to respond to heat stress by autoregulation and upregulation of the hrcA‐grpE‐dnaK‐dnaJ operon, which in turn leads to expression of heat shock proteins (Figure 2) (Cheng et al., 2021).…”

“…Resistance to heat, otherwise reported as thermal resistance in foodborne bacteria can be due to several factors such as the cell growth stage and environmental conditions, including pH, water activity (aw), temperature, heat shock, and the presence of osmoprotectants (Den Besten et al., 2018; Soni et al., 2022a). Also, the expression of certain proteins during stationary growth phases or in response to stress can lead to increased heat resistance; for instance, in Bacillus and Listeria , the sigma B stress response is known to facilitate such cross‐resistance (Soni et al., 2022a; van Schaik et al., 2004). This expression could be triggered as a stress response to various factors, and therefore, it is evident that the mechanisms underlying heat resistance are remarkably diverse, and the environmental context in which cells exist plays a crucial role.…”

“…It assumes that all microbial cells exhibit equal heat sensitivity. However, evidence challenges this theory, leading to deviations like shoulders and tails in survival curves (Cebrián et al., 2017; Soni et al., 2022a). Various factors including stress, bacterial strain, and food matrix as well as genetic determinants could contribute to thermal resistance of certain bacterial strains, which are considered pathogenic.…”