Effect of temperature on the growth of Staphylococcus aureus in ready-to-eat cooked rice with pork floss
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.
References (25)
- et al.
Microbiological quality of sushi from sushi bars and retailers
J. Food Prot.
(2008) - et al.
Modeling the level of contamination of Staphylococcus aureus in ready-to-eat kimbab in Korea
J. Food Prot.
(2006) - et al.
Mathematics of predictive food microbiology
Int. J. Food Microbiol.
(1995) - et al.
Mathematical modeling and growth kinetics of Clostridium sporogenes in cooked beef
Food Control
(2016) Optimization of a new mathematical model for bacterial growth
Food Control
(2013)IPMP 2013 - a comprehensive data analysis tool for predictive microbiology
Int. J. Food Microbiol.
(2014)- et al.
Bacterial contamination of ready-to-eat foods and fresh products in retail shops and food factories
J. Food Prot.
(1999) - et al.
Occurrence of toxigenic Staphylococcus aureus in ready-to-eat food in Korea
J. Food Prot.
(2007) - et al.
Microbial risk assessment of staphylococcal food poisoning in Korean kimbab
Int. J. Food Microbiol.
(2007) - et al.
Prolonged expression and production of Staphylococcus aureus enterotoxin A in processed pork meat
Int. J. Food Microbiol.
(2010)
Summary Report (Validation Study According to EN ISO 16140-2:2016): TEMPO® STA Method (Certificate Number: BIO 12/28 - 04/10) for the Enumeration of Coagulase-Positive Staphylococci in Human Food and Pet Food
Summary Report (Validation Study According to AOAC® Performance Tested MethodsSM Program): TEMPO® STA (Staphylococcus aureus) Method Is an Automated System for the Enumeration of Coagulase‐positive Staphylococci in Foods
Cited by (17)
Comparative genomic analysis and multilocus sequence typing of Staphylococcus aureus reveals candidate genes for low-temperature tolerance
2024, Science of the Total EnvironmentGenotypic diversity of staphylococcal enterotoxin B gene (seb) and its association with molecular characterization and antimicrobial resistance of Staphylococcus aureus from retail food
2024, International Journal of Food MicrobiologyModelling the growth of Staphylococcus aureus with different levels of resistance to low temperatures in glutinous rice dough
2023, LWTCitation Excerpt :A Korean study showed that the rice products, such as rice balls, sushi, and nori wrap rice, are susceptible to contamination by S. aureus in many Asian countries (Rodrigo et al., 2021). If the storage temperature and time allow cell grow to a certain number, a high risk of food poisoning will inevitably happened (Lu et al., 2020). Predictive microbiology is increasingly involved in quantitative microbial risk assessment to reduce the uncertainty of food safety issues (Cassani et al., 2020).
Growth simulation of Pseudomonas fluorescens in pork using hyperspectral imaging
2022, Meat ScienceCitation Excerpt :Combined with the Ratkowsky square-root model, the values of a obtained were both 0.01, in which the nominal minimum growth temperatures were − 14.19 °C and − 13.50 °C, respectively. In this study, the estimated minimum growth temperature may represent the minimum biological growth temperature (Lu, Sheen, Huang, Kao, & Sheen, 2019). Goncalves, Piccoli, Peres, and Saude (2017) estimated that the minimum growth temperature of P. fluorescens in pork was −14.67 °C, which was similar to that observed in other food products (Robazza, Teleken, Galvão, Miorelli, & Stolf, 2017; Tarlak, Ozdemir, & Melikoglu, 2020).
- 1
These authors contributed equally to this work.