Inhibition of <i>Clostridium perfringens</i> Spore Germination and Outgrowth by Lemon Juice and Vinegar Product in Reduced NaCl Roast Beef

Li, Lin; Valenzuela-Martínez, Carol; Redondo, Mauricio; Juneja, Vijay K.; Burson, Dennis E.; Thippareddi, Harshavardhan

doi:10.1111/j.1750-3841.2012.02922.x

Cited by 20 publications

(10 citation statements)

References 17 publications

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“…Spore germination is a necessary step in resuming vegetative growth; thus, the probability that the spores germinate in food products needs to be taken into account when assessing the risk of spoilage or outgrowth of pathogenic spore formers. Moreover, both inhibition of spore germination and induction of germination before inactivation treatments (which renders the spore sensitive) are used in the food industry to improve food safety (7)(8)(9)(10)(11)(12). However, none of these strategies is completely effective.…”

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confidence: 99%

Spore Heat Activation Requirements and Germination Responses Correlate with Sequences of Germinant Receptors and with the Presence of a Specific spoVA ^2mob Operon in Foodborne Strains of Bacillus subtilis

Krawczyk

Jong

Omony

et al. 2017

Appl Environ Microbiol

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Spore heat resistance, germination, and outgrowth are problematic bacterial properties compromising food safety and quality. Large interstrain variation in these properties makes prediction and control of spore behavior challenging. Highlevel heat resistance and slow germination of spores of some natural Bacillus subtilis isolates, encountered in foods, have been attributed to the occurrence of the spoVA 2mob operon carried on the Tn1546 transposon. In this study, we further investigate the correlation between the presence of this operon in high-level-heat-resistant spores and their germination efficiencies before and after exposure to various sublethal heat treatments (heat activation, or HA), which are known to significantly improve spore responses to nutrient germinants. We show that high-level-heat-resistant spores harboring spoVA 2mob required higher HA temperatures for efficient germination than spores lacking spoVA 2mob . The optimal spore HA requirements additionally depended on the nutrients used to trigger germination, L-alanine (L-Ala), or a mixture of L-asparagine, D-glucose, D-fructose, and K ϩ (AGFK). The distinct HA requirements of these two spore germination pathways are likely related to differences in properties of specific germinant receptors. Moreover, spores that germinated inefficiently in AGFK contained specific changes in sequences of the GerB and GerK germinant receptors, which are involved in this germination response. In contrast, no relation was found between transcription levels of main germination genes and spore germination phenotypes. The findings presented in this study have great implications for practices in the food industry, where heat treatments are commonly used to inactivate pathogenic and spoilage microbes, including bacterial spore formers.IMPORTANCE This study describes a strong variation in spore germination capacities and requirements for a heat activation treatment, i.e., an exposure to sublethal heat that increases spore responsiveness to nutrient germination triggers, among 17 strains of B. subtilis, including 9 isolates from spoiled food products. Spores of industrial foodborne isolates exhibited, on average, less efficient and slower germination responses and required more severe heat activation than spores from other sources. High heat activation requirements and inefficient, slow germination correlated with elevated resistance of spores to heat and with specific genetic features, indicating a common genetic basis of these three phenotypic traits. Clearly, interstrain variation and numerous factors that shape spore germination behavior challenge standardization of methods to recover highly heat-resistant spores from the environment and have an impact on the efficacy of preservation techniques used by the food industry to control spores.

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confidence: 99%

Spore Heat Activation Requirements and Germination Responses Correlate with Sequences of Germinant Receptors and with the Presence of a Specific spoVA ^2mob Operon in Foodborne Strains of Bacillus subtilis

Krawczyk

Jong

Omony

et al. 2017

Appl Environ Microbiol

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“…The cooling data contain both single‐ and dual‐rate cooling profiles. For most single‐rate cooling profiles, the temperature decreases exponentially from 54.4 to 7.2 °C or 4.4 °C in 6.5, 9, 12, 15, 18, and 21 h (Thippareddi and others ; Zaika ; Juneja and Thippareddi , ; Smith and others ; Smith and Schaffner ; Sánchez‐Plata and others ; Juneja and others , ; Olds and others ; Juneja and Friedman ; Velugoti and others ; Singh and others ; Li and others ; Decker and others ; Juneja and others ; Kennedy and others ; Redondo‐Solano and others ; King and others ). The single‐rate cooling profiles also include 2 linear cooling profiles from 54.4 to 7.2 °C (King and others ) and 5 customized cooling profiles (Olds and others ; Decker and others ).…”

Section: Methodsmentioning

confidence: 99%

Evaluating the Performance of a New Model for Predicting the Growth of Clostridium perfringens in Cooked, Uncured Meat and Poultry Products under Isothermal, Heating, and Dynamically Cooling Conditions

Huang

2016

Journal of Food Science

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Clostridium perfringens type A is a significant public health threat and its spores may germinate, outgrow, and multiply during cooling of cooked meats. This study applies a new C. perfringens growth model in the USDA Integrated Pathogen Modeling Program-Dynamic Prediction (IPMP Dynamic Prediction) Dynamic Prediction to predict the growth from spores of C. perfringens in cooked uncured meat and poultry products using isothermal, dynamic heating, and cooling data reported in the literature. The residual errors of predictions (observation-prediction) are analyzed, and the root-mean-square error (RMSE) calculated. For isothermal and heating profiles, each data point in growth curves is compared. The mean residual errors (MRE) of predictions range from -0.40 to 0.02 Log colony forming units (CFU)/g, with a RMSE of approximately 0.6 Log CFU/g. For cooling, the end point predictions are conservative in nature, with an MRE of -1.16 Log CFU/g for single-rate cooling and -0.66 Log CFU/g for dual-rate cooling. The RMSE is between 0.6 and 0.7 Log CFU/g. Compared with other models reported in the literature, this model makes more accurate and fail-safe predictions. For cooling, the percentage for accurate and fail-safe predictions is between 97.6% and 100%. Under criterion 1, the percentage of accurate predictions is 47.5% for single-rate cooling and 66.7% for dual-rate cooling, while the fail-dangerous predictions are between 0% and 2.4%. This study demonstrates that IPMP Dynamic Prediction can be used by food processors and regulatory agencies as a tool to predict the growth of C. perfringens in uncured cooked meats and evaluate the safety of cooked or heat-treated uncured meat and poultry products exposed to cooling deviations or to develop customized cooling schedules. This study also demonstrates the need for more accurate data collection during cooling.

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“…Growth inhibition of C. perfringens also has been noted in beef patties at a level of 2 or 3% potassium lactate with no negative effects on the product's sensory aspects (6). Li et al (13) found that the addition of lemon juice and vinegar products inhibited C. perfringens spore germination and outgrowth. This research suggests that either organic acids or their neutralized salts have an effect on the germination and growth of C. perfringens spores.…”

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confidence: 99%

Inhibition of Clostridium perfringens Growth by Potassium Lactate during an Extended Cooling of Cooked Uncured Ground Turkey Breasts

Kennedy

Milkowski

Glass

2013

Journal of Food Protection

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The U.S. Department of Agriculture's Food Safety and Inspection Service compliance guideline known as Appendix B specifies chilling time and temperature limits for cured and uncured meat products to inhibit growth of spore-forming bacteria, particularly Clostridium perfringens. Sodium lactate and potassium lactate inhibit toxigenic growth of Clostridium botulinum, and inhibition of C. perfringens has been reported. In this study, a cocktail of spores of three C. perfringens strains (ATCC 13124, ATCC 12915, and ATCC 12916) were inoculated into 100-g samples of ground skinless, boneless turkey breast formulated to represent deli-style turkey breast. Three treatment groups were supplemented with 0 (control), 1, or 2% potassium lactate (pure basis), cooked to 71 °C, and assayed for C. perfringens growth during 10 or 12 h of linear cooling to 4 °C. In control samples, populations of C. perfringens increased 3.8 to 4.7 log CFU/g during the two chilling protocols. The 1% potassium lactate treatment supported only a 2.5- to 2.7-log increase, and the 2% potassium lactate treatment limited growth to a 0.56- to 0.70-log increase. When compared with the control, 2% potassium lactate retarded growth by 2.65 and 4.21 log CFU/g for the 10- and 12-h cooling protocols, respectively. These results confirm that the addition of 2% potassium lactate inhibits growth of C. perfringens and that potassium lactate can be used as an alternative to sodium nitrite for safe extended cooling of uncured meats.

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Inhibition of Clostridium perfringens Spore Germination and Outgrowth by Lemon Juice and Vinegar Product in Reduced NaCl Roast Beef

Cited by 20 publications

References 17 publications

Spore Heat Activation Requirements and Germination Responses Correlate with Sequences of Germinant Receptors and with the Presence of a Specific spoVA ^2mob Operon in Foodborne Strains of Bacillus subtilis

Spore Heat Activation Requirements and Germination Responses Correlate with Sequences of Germinant Receptors and with the Presence of a Specific spoVA ^2mob Operon in Foodborne Strains of Bacillus subtilis

Evaluating the Performance of a New Model for Predicting the Growth of Clostridium perfringens in Cooked, Uncured Meat and Poultry Products under Isothermal, Heating, and Dynamically Cooling Conditions

Inhibition of Clostridium perfringens Growth by Potassium Lactate during an Extended Cooling of Cooked Uncured Ground Turkey Breasts

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Inhibition of Clostridium perfringens Spore Germination and Outgrowth by Lemon Juice and Vinegar Product in Reduced NaCl Roast Beef

Cited by 20 publications

References 17 publications

Spore Heat Activation Requirements and Germination Responses Correlate with Sequences of Germinant Receptors and with the Presence of a Specific spoVA 2mob Operon in Foodborne Strains of Bacillus subtilis

Spore Heat Activation Requirements and Germination Responses Correlate with Sequences of Germinant Receptors and with the Presence of a Specific spoVA 2mob Operon in Foodborne Strains of Bacillus subtilis

Evaluating the Performance of a New Model for Predicting the Growth of Clostridium perfringens in Cooked, Uncured Meat and Poultry Products under Isothermal, Heating, and Dynamically Cooling Conditions

Inhibition of Clostridium perfringens Growth by Potassium Lactate during an Extended Cooling of Cooked Uncured Ground Turkey Breasts

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Spore Heat Activation Requirements and Germination Responses Correlate with Sequences of Germinant Receptors and with the Presence of a Specific spoVA ^2mob Operon in Foodborne Strains of Bacillus subtilis

Spore Heat Activation Requirements and Germination Responses Correlate with Sequences of Germinant Receptors and with the Presence of a Specific spoVA ^2mob Operon in Foodborne Strains of Bacillus subtilis