Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Predictive modeling of Salmonella Thompson growth in unpasteurized liquid egg products

  • Chang-Geun Lim (Department of Animal Convergence Science, Hankyoung National University) ;
  • Seung-Hee Baek (Research Center for Environment Friendly and Quality Livestock Production Technology, Hankyoung National University) ;
  • In-Sik Nam (Department of Animal Convergence Science, Hankyoung National University)
  • Received : 2025.09.08
  • Accepted : 2025.12.29
  • Published : 2026.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: Salmonella Thompson is a major cause of large-scale foodborne disease outbreaks worldwide; however, research on S. Thompson remains limited. This study investigates the development of a predictive model for the growth of S. Thompson in unpasteurized liquid egg products, such as liquid egg white, liquid egg yolk, and liquid whole egg, to understand the associated health risks. Methods: Unpasteurized liquid egg products, confirmed to be free of Salmonella spp., were inoculated with S. Thompson and incubated at various temperatures. Growth kinetic parameters were estimated using both primary and secondary predictive models, including the Baranyi and Roberts model and second-order polynomial models. The effects of environmental factors on S. Thompson growth were analyzed to establish a comprehensive risk assessment framework. Results: The growth curves of S. Thompson exhibited a typical bacterial sigmoidal pattern characteristic of bacterial proliferation, with the Baranyi model providing the best fit for describing the growth kinetics. The secondary model accurately predicted the effect of temperature on growth rate, demonstrating that S. Thompson proliferates rapidly under specific environmental conditions. Model validation indicated high accuracy, confirming the reliability of the developed model for risk assessment applications. Conclusion: The established predictive model enables quantitative assessment of the growth behavior of S. Thompson in unpasteurized liquid egg products. This model can be used in risk assessment and food safety management strategies to mitigate the risk of food-borne pathogen contamination in the food industry.

Keywords

References

  1. El-Sharkawy H, Tahoun A, Rizk AM, et al. Evaluation of Bifidobacteria and Lactobacillus probiotics as alternative therapy for Salmonella typhimurium infection in broiler chickens. Animals 2020;10:1023. https://doi.org/10.3390/ani10061023
  2. Whiley H, Ross K. Salmonella and eggs: from production to plate. Int J Environ Res Public Health 2015;12:2543-56. https://doi.org/10.3390/ijerph120302543
  3. Eun Y, Jeong H, Kim S, et al. A large outbreak of Salmonella enterica serovar Thompson infections associated with chocolate cake in Busan, Korea. Epidemiol Health 2019;41:e2019002. https://doi.org/10.4178/epih.e2019002
  4. Majowicz SE, Musto J, Scallan E, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 2010;50:882-9. https://doi.org/10.1086/650733
  5. Braden CR. Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States. Clin Infect Dis 2006;43:512-7. https://doi.org/10.1086/505973
  6. Toyofuku H. Epidemiological data on food poisonings in Japan focused on Salmonella, 1998–2004. Food Addit Contam A 2008;25:1058-66. https://doi.org/10.1080/02652030802225965
  7. Harker KS, Lane C, Gormley FJ, Adak GK. National outbreaks of Salmonella infection in the UK, 2000–2011. Epidemiol Infect 2014;142:601-7. https://doi.org/10.1017/S0950268813001210
  8. Hwang MJ, Park SY, Kim H, Yang SJ, Yang S, Yang JS. Waterborne and foodborne disease outbreaks in the Republic of Korea, 2023. Public Health Wkly Rep 2024;18:17-32. https://doi.org/10.56786/PHWR.2025.18.1.2
  9. Kang GH, Cho SH, Seong PN, et al. Microbial and physicochemical properties of liquid egg during cold storage. Food Sci Anim Resour 2011;31:557-62. https://doi.org/10.5851/kosfa.2011.31.4.557
  10. Gurtler JB, Hinton A Jr, Bailey RB, et al. Salmonella isolated from ready-to-eat pasteurized liquid egg products: thermal resistance, biochemical profile, and fatty acid analysis. Int J Food Microbiol 2015;206:109-17. https://doi.org/10.1016/j.ijfoodmicro.2015.04.010
  11. Bermudez-Aguirre D, Niemira BA. Effect of nisin, EDTA, and abuse temperature on the growth of Salmonella typhimurium in liquid whole egg during refrigerated storage. Food Res Int 2023;174:113568. https://doi.org/10.1016/j.foodres.2023.113568
  12. Huang S, Hui TB, Yuk HG, Zheng Q. Development of an effective two-step enrichment process to enhance bax system detection of healthy and injured Salmonella enteritidis in liquid whole egg and egg yolk. J Food Prot 2020;83:397-404. https://doi.org/10.4315/0362-028X.JFP-19-280
  13. Lee W, Kim E, Zin H, et al. Genomic characteristics and comparative genomics analysis of Salmonella enterica subsp. enterica serovar Thompson isolated from an outbreak in South Korea. Sci Rep 2022;12:20553. https://doi.org/10.1038/s41598-022-22168-2
  14. Van Abel N, Schoen ME, Kissel JC, Meschke JS. Comparison of risk predicted by multiple norovirus dose–response models and implications for quantitative microbial risk assessment. Risk Anal 2017;37:245-64. https://doi.org/10.1111/risa.12616
  15. Possas A, Pérez-Rodríguez F. Detection, control, risk assessment, and prevention of foodborne microorganisms. Foods 2024;13:1551. https://doi.org/10.3390/foods13101551
  16. Kim YJ, Moon HJ, Lee SK, et al. Development and validation of predictive model for Salmonella growth in unpasteurized liquid eggs. Korean J Food Sci Anim Resour 2018;38:442-50. https://doi.org/10.5851/kosfa.2018.38.3.442
  17. Singh A, Korasapati NR, Juneja VK, Subbiah J, Froning G, Thippareddi H. Dynamic predictive model for the growth of Salmonella spp. in liquid whole egg. J Food Sci 2011;76:M225-32. https://doi.org/10.1111/j.1750-3841.2011.02074.x
  18. Baranyi J, Roberts TA. A dynamic approach to predicting bacterial growth in food. Int J Food Microbiol 1994;23:277-94. https://doi.org/10.1016/0168-1605(94)90157-0
  19. Park JH, Kang MS, Park KM, et al. A dynamic predictive model for the growth of Salmonella spp. and Staphylococcus aureus in fresh egg yolk and scenario-based risk estimation. Food Control 2020;118:107421. https://doi.org/10.1016/j.foodcont.2020.107421
  20. McMeekin TA, Olley J, Ross T, Ratkowsky DA. Predictive microbiology: theory and application. Research Studies Press; 1993. p. 94.
  21. Baranyi J, Pin C, Ross T. Validating and comparing predictive models. Int J Food Microbiol 1999;48:159-66. https://doi.org/10.1016/S0168-1605(99)00035-5
  22. Moon HJ, Lim JG, Yoon KS. Comparative study of change in Salmonella enteritidis and Salmonella typhimurium populations in egg white and yolk. J Food Hyg Saf 2016;31:342-8. https://doi.org/10.13103/JFHS.2016.31.5.342
  23. Guillén S, Marcén M, Álvarez I, Mañas P, Cebrián G. Influence of the initial cell number on the growth fitness of Salmonella enteritidis in raw and pasteurized liquid whole egg, egg white, and egg yolk. Foods 2021;10:1621. https://doi.org/10.3390/foods10071621
  24. Baron F, Gautier M, Brule G. Factors involved in the inhibition of growth of Salmonella enteritidis in liquid egg white. J Food Prot 1997;60:1318-23. https://doi.org/10.4315/0362-028X-60.11.1318
  25. Zhang Q, Zhao Y, Yao Y, et al. Characteristics of hen egg white lysozyme, strategies to break through antibacterial limitation, and its application in food preservation: a review. Food Res Int 2024;181:114114. https://doi.org/10.1016/j.foodres.2024.114114
  26. Ye K, Wang H, Zhang X, et al. Development and validation of a molecular predictive model to describe the growth of Listeria monocytogenes in vacuum-packaged chilled pork. Food Control 2013;32:246-54. https://doi.org/10.1016/j.foodcont.2012.11.017
  27. Huang L. Direct construction of predictive models for describing growth of Salmonella enteritidis in liquid eggs: a one-step approach. Food Control 2015;57:76-81. https://doi.org/10.1016/j.foodcont.2015.03.051
  28. Kang MS, Park JH, Kim HJ. Predictive modeling for the growth of Salmonella spp. in liquid egg white and application of scenario-based risk estimation. Microorganisms 2021;9:486. https://doi.org/10.3390/microorganisms9030486
  29. Elias SO, Alvarenga VO, Longhi DA, Sant'Ana AS, Tondo EC. Modeling growth kinetic parameters of Salmonella enteritidis SE86 on homemade mayonnaise under isothermal and nonisothermal conditions. Foodborne Pathog Dis 2016; 13:462-7. https://doi.org/10.1089/fpd.2015.2045