Elsevier

Food Microbiology

Volume 89, August 2020, 103374
Food Microbiology

Effect of temperature on the growth of Staphylococcus aureus in ready-to-eat cooked rice with pork floss

https://doi.org/10.1016/j.fm.2019.103374Get rights and content

Highlights

  • Growth parameters for S. aureus in CRPF were determined for the first time.

  • Different primary and secondary models were used to describe the growth.

  • Combination of Huang primary and Huang square-root models is proper than others.

  • Performance of the developed models was validated by RMSE, Bf, and Af.

Abstract

Cooked rice with pork floss (CRPF) wrapped in dried seaweed is one of the most popular ready-to-eat (RTE) foods in many Asian countries, particularly in Taiwan. The products are susceptible to Staphylococcus aureus contamination and temperature abuse during manufacturing, distribution, and storage. The objective of this study was to examine the effect of temperature on its growth in RTE CRPF for use in risk assessment and prevention of staphylococcal food poisoning (SFP). Inoculated CRPF samples were stored at 4, 12, 18, 25, and 35°C, and the change in the populations of S. aureus during storage were analyzed using three primary models to determine specific growth rate (μmax), lag-phase duration (λ), and maximum population density (ymax). The Ratkowsky square-root and Huang square-root (HSR) models were used as the secondary models to describe the effect of temperature on μmax, and a linear and an exponential regression models were used to describe the effect of temperature on λ and ymax, respectively. The model performance was evaluated by the root mean square error (RMSE), bias factor (Bf), and accuracy factor (Af) when appropriate. Results showed that three primary models were suitable for describing the growth curves, with RMSE ≤ 0.3 (log MPN/g). Using μmax obtained from the Huang model, the minimum growth temperature (Tmin) estimated by the HSR model was 7.0°C, well in agreement with the reported Tmin. The combination of primary and secondary models for predicting S. aureus growth was validated by additional growth curves at 30°C, which showed that the RMSE was 0.6 (log MPN/g). Therefore, the developed models were acceptable for predicting the growth of S. aureus in CRPF under likely temperature abuse conditions and can be applied to assess the risk of S. aureus in CRPF and design temperature controls to reduce the risk of SFP.

Introduction

Staphylococcus aureus is one of the most common causes of reported foodborne diseases around the world. It is an ongoing concern in public health since the bacterium can survive adverse environmental conditions and produce highly heat-stable enterotoxins, causing staphylococcal food poisoning (SFP) (Kadariya et al., 2014). It can grow at temperatures between 7 and 47.8°C, pH 4.5 and 9.3, and water activity (aw) ≥ 0.83, while most of the other foodborne pathogens need higher aw (≥ 0.90) for growth (USFDA, 2012). SFP is commonly associated with starchy foods that are manually prepared and are not properly processed and handled (Wallin-Carlquist et al., 2010). Recent studies have documented that S. aureus is the main pathogen of concern for various ready-to-eat (RTE) foods in the Eastern European Union, China, Japan, and Korea (Ciolacu et al., 2016; Kaneko et al., 1999; Oh et al., 2007; Yang et al., 2016).

In many Asian countries, cooked rice products, such as rice balls (with meat or vegetables), Sushi (with raw seafood), and Kimbab (with kimchi) in Taiwan, Japan, and Korea, are consumers’ favorite RTE foods sold in retail outlets. It has been reported that these types of RTE products may be contaminated with S. aureus since they are usually prepared by hands (Atanassova et al., 2008; Bahk et al., 2006; Shimamura et al., 2006). RTE cooked rice products are high in water activity and are exposed to temperatures between 4°C and ambient temperature during manufacturing, distribution, and storage. No heating is required prior to consumption of cooked rice products. Therefore, they may pose a high risk of SFP if the storage temperature and time allows S. aureus to grow to a population of 105 CFU/g or produce 100-200 ng of enterotoxin (USFDA, 2012).

The first objective of this study was to examine how storage temperature affects the growth of S. aureus in cooked rice with pork floss (CRPF) wrapped with dry seaweed, a top-selling RTE product sold for breakfast, lunch, and dinner in Taiwan year-round and a major concern of SFP identified by the local food safety regulatory authorities. The second objective of this study was to develop mathematical models that may be used to predict the growth of S. aureus in CRPF as affected by storage temperature. Such models would be useful for conducting risk assessment of S. aureus in this type of products and developing control strategies to prevent the overgrowth of S. aureus and formation of staphylococcal enterotoxins during storage and distribution.

Section snippets

S. aureus and inoculum preparation

S. aureus BCRC 13962, an enterotoxin A-producing strain, was obtained from the Bioresource Collection and Research Center (Hsinchu, Taiwan) and incubated on tryptic soy agar (TSA; Becton, Dickinson and Company (BD), Sparks, MD, USA) at 35°C for 24 h. One typical colony was selected and inoculated in tryptic soy broth (TSB; BD) at 35°C for 24 h to reach the stationary phase (108 to 109 MPN/mL). The culture was diluted with phosphate-buffered saline (PBS; pH 7.2) and used as inoculum.

Sample preparation and inoculation

Samples of

Microbial populations, pH, and aw of CRPF

The initial concentration of the background microorganisms in CRPF samples was approximately 3.7 log MPN/g. The pH and aw were 5.85 and 0.95, respectively. According to USFDA (2012), S. aureus can grow in the pH range between 4.5 and 9.3. Its optimum pH is between 7.0 and 7.5. It is an atypical pathogen that can grow at low aw (0.83) and is highly tolerant of salts and sugars. Therefore, the pH and aw of the CRPF samples were well within the growth range of S. aureus.

Growth curves of S. aureus and estimates of kinetic parameters

The growth of S. aureus in

Conclusion

This study investigated the growth of S. aureus in CRPF and used different primary and secondary models to describe the growth of this microorganism as affected by storage temperature. According to the secondary model (HSR model), the estimated minimum growth temperature is around 7°C, which agrees with the biological minimum growth temperature generally recognized for this microorganism. The combination of the Huang primary model and HSR model was validated by a growth curve observed at 30°C.

Declaration of competing interest

All authors have no conflicts of interest to declare.

Acknowledgment

The authors would like to thank Prof. Wei-Chiang Shen, National Taiwan University for technical support. This study was conducted under the cooperative agreement No. 58-8072-5-037-FN between the Agricultural Research Service, United States Department of Agriculture and the National Taiwan University. The project was supported by grants (104AS-3.1.1-AD-U1 and 105AS-3.1.2-AD-U1) from the Council of Agriculture, Taiwan.

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