Quantitative Microbial Risk Assessment for Clostridium perfringens in Natural and Processed Cheeses

  • Lee, Heeyoung (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Lee, Soomin (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Kim, Sejeong (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Lee, Jeeyeon (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Ha, Jimyeong (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Yoon, Yohan (Department of Food and Nutrition, Sookmyung Women's University)
  • Received : 2015.12.09
  • Accepted : 2016.02.10
  • Published : 2016.08.01


This study evaluated the risk of Clostridium perfringens (C. perfringens) foodborne illness from natural and processed cheeses. Microbial risk assessment in this study was conducted according to four steps: hazard identification, hazard characterization, exposure assessment, and risk characterization. The hazard identification of C. perfringens on cheese was identified through literature, and dose response models were utilized for hazard characterization of the pathogen. For exposure assessment, the prevalence of C. perfringens, storage temperatures, storage time, and annual amounts of cheese consumption were surveyed. Eventually, a simulation model was developed using the collected data and the simulation result was used to estimate the probability of C. perfringens foodborne illness by cheese consumption with @RISK. C. perfringens was determined to be low risk on cheese based on hazard identification, and the exponential model ($r=1.82{\times}10^{-11}$) was deemed appropriate for hazard characterization. Annual amounts of natural and processed cheese consumption were $12.40{\pm}19.43g$ and $19.46{\pm}14.39g$, respectively. Since the contamination levels of C. perfringens on natural (0.30 Log CFU/g) and processed cheeses (0.45 Log CFU/g) were below the detection limit, the initial contamination levels of natural and processed cheeses were estimated by beta distribution (${\alpha}1=1$, ${\alpha}2=91$; ${\alpha}1=1$, ${\alpha}2=309$)${\times}$uniform distribution (a = 0, b = 2; a = 0, b = 2.8) to be -2.35 and -2.73 Log CFU/g, respectively. Moreover, no growth of C. perfringens was observed for exposure assessment to simulated conditions of distribution and storage. These data were used for risk characterization by a simulation model, and the mean values of the probability of C. perfringens foodborne illness by cheese consumption per person per day for natural and processed cheeses were $9.57{\times}10^{-14}$ and $3.58{\times}10^{-14}$, respectively. These results indicate that probability of C. perfringens foodborne illness by consumption cheese is low, and it can be used to establish microbial criteria for C. perfringens on natural and processed cheeses.


Quantitative Microbial Risk Assessment;Clostridium perfringens;Cheese


Supported by : Ministry of Food and Drug Safety


  1. Bemrah, N., M. Sanaa, M. H. Cassin, M. W. Griffiths, and O. Cerf. 1998. Quantitative risk assessment of human listeriosis from consumption of soft cheese made from raw milk. Prev. Vet. Med. 37:129-145.
  2. Brynestad, S. and P. E. Granum. 2002. Clostridium perfringens and foodborne infections. Int. J. Food Microbiol. 74:195-202.
  3. Byrne, B., G. Dunne, and D. J. Bolton. 2006. Thermal inactivation of Bacillus cereus and Clostridium perfringens vegetative cells and spores in pork luncheon roll. Food Microbiol. 23:803-808.
  4. CDC (Centers for Disease Control and Prevention). 2014. Clostridium perfringens. Accessed August 15, 2014.
  5. CDC (Centers for Disease Control and Prevention). 2016. Foodborne outbreak tracking and reporting. Accessed February 05, 2016.
  6. Codex. 1999. Principles and guidelines for the conduct of microbiological risk assessment. CAC/GL-30. Accessed October 3, 2014.
  7. Ding, T., J. Iwahori, F. Kasuga, J. Wang, F. Forghani, M. S. Park, and D. H. Oh. 2013. Risk assessment for Listeria monocytogenes on lettuce from farm to table in Korea. Food Control 30:190-199.
  8. Farber, J. M., W. H. Rossb, and J. Harwig. 1996. Health risk assessment of Listeria monocytogenes in Canada. Int. J. Food Microbiol. 30:145-156.
  9. Feligini, M., E. Brambati, S. Panelli, M. Ghitti, R. Sacchi, E. Capelli, and C. Bonacina. 2014. One-year investigation of Clostridium spp. occurrence in raw milk and curd of Grana Padano cheese by the automated ribosomal intergenic spacer analysis. Food Control 42:71-77.
  10. FDA (Food and Drug Administration). 2012. Bad bug book, foodborne pathogenic microorganisms and natural toxins. Second edition. Accessed October 3, 2014.
  11. FDA-CFSANC and USDA-FSIS (Food and Drug Administration-Center for Food Safety and Applied Nutrition, and U.S. Department of Agriculture-Food Safety and Inspection Service). 2003. Quantitative assessment of the relative risk to public health from foodborne Listeria monocytogenes among selected categories of ready-to-eat foods. Accessed October 3, 2014.
  12. Forsythe, S. J. 2002. Food-borne microbial pathogens in world trade. In: The Microbiological Risk Assessment of Food (Ed. S. J. Forsythe). Blackwell Publishing, Oxford, UK. pp. 1-33.
  13. Gao, Z. and B. A. McClane. 2012. Use of Clostridium perfringens enterotoxin and the enterotoxin receptor-binding domain (C-CPE) for cancer treatment: Opportunities and challenges. J. Toxicol. 2012:Article ID 981626, 9 pages.
  14. Golden, N. J., E. A. Crouch, H. Latmer, A. R. Kadrt, and J. Kause. 2009. Risk assessment for Clostridium perfringens in ready-to-eat and partially cooked meat and poultry products. J. Food Prot. 72:1376-1384.
  15. Grass, J. E., L. H. Gould, and B. E. Mahon. 2013. Epidemiology of foodborne disease outbreaks caused by Clostridium perfringens, United States, 1998-2010. Foodborne Pathog. Dis. 10:131-135.
  16. Heidinger, J. C., C. K. Winter, and J. S. Cullor. 2009. Quantitative microbial risk assessment for Staphylococcus aureus and Staphylococcus enterotoxin A in raw milk. J. Food Prot. 72:1641-1653.
  17. Juneja, V. K., H, Marks, and H. Thippareddi. 2009. Predictive model for growth of Clostridium perfringens during cooling of cooked ground chicken. Innov. Food Sci. Emerg. Technol. 10:260-266.
  18. Juneja, V. K., J. S. Novak, L. Huang, and B. S. Eblen. 2003. Increased thermotolerance of Clostridium perfringens spores following sublethal heat shock. Food Control 14:163-168.
  19. Ko, E. K., J. S. Moon, S. H. Wee, and G. J. Bahk. 2012. Quantitative microbial risk assessment of Clostridium perfringens on ham and sausage products in Korea. Korean J. Food Sci. An. 32:118-124.
  20. Kousta, M., M. Mataragas, P. Skandamis, and E. H. Drosinos. 2010. Prevalence and sources of cheese contamination with pathogens at farm and processing levels. Food Control 21:805-815.
  21. Labbe, R. J. and V. K. Juneja. 2006. Clostridium perfringens gastroenteritis. In: Foodborne Infections and Intoxications (Eds. H. Riemann and D. O. Cliver). Academic Press, Inc., San Diego, CA, USA. pp. 137-184.
  22. Labbe, R. G. 2001. Clostridium perfringens. In: Compendium of Methods for the Microbiological Examination of Foods (Eds. F. P. Downs and K. Ito). American Public Health Association, Washington, DC, USA. pp. 325-330.
  23. Le Loir, Y., F. Baron, and M. Gautier. 2003. Staphylococcus aureus and food poisoning. Genet. Mol. Res. 2:63-76.
  24. Le Marc, Y., J. Plowman., C. F. Aldus, M. Munoz-Cuevas, J. Baranyi, and M. W. Peck. 2008. Modelling the growth of Clostridium perfringens during the cooling of bulk meat. Int. J. Food Microbiol. 128:41-50.
  25. Li, J. and B. A. McClane. 2006a. Comparative effects of osmotic, sodium nitrite-induced, and pH-induced stress on growth and survival of Clostridium perfringens type A isolates carrying chromosomal or plasmid-borne enterotoxin genes. Appl. Environ. Microbiol. 72:7620-7625.
  26. Li, J. and B. A. McClane. 2006b. Further comparison of temperature effects on growth and survival of Clostridium perfringens type A isolates carrying a chromosomal or plasmid-borne enterotoxin gene. Appl. Environ. Microbiol. 72:4561-4568.
  27. Little, C. L., J. R. Rhoades, S. K. Sagoo, J. Harris, M. Greenwood., and V. Mithani. 2008. Microbiological quality of retail cheese made from raw, thermised or pasteurized milk in UK. Food Microbiol. 25:304-312.
  28. McClane, B. A. 2007. Clostridium perfringens. In: Food Microbiology: Fundamentals and Frontiers (Eds. M. P. Doyle and L. R. Beuchat). ASM Press, Washington, DC, USA. pp. 423-444.
  29. MFDS (Ministry of Food and Drug Safety). 2007. Suggestion of specification on temperature management of refrigerator-storing foods. Accessed March 16, 2015.
  30. MFDS (Ministry of Food and Drug Safety). 2014a. Standard for livestock product processing ingredients. pp. 42-45.
  31. MFDS (Ministry of Food and Drug Safety). 2014b. Status of food poisoning outbreaks in Korea. Accessed February 11, 2015.
  32. Paredes-Sabja, D., M. Gonzalez, M. R. Sarker, and J. A. Torres. 2007. Combined effects of hydrostatic pressure, temperature, and pH on the inactivation of spores of Clostridium perfringens type A and Clostridium sporogenes in buffer solutions. J. Food Sci. 72:M202-M206.
  33. Park, G. J. 2010. Statistical probability analysis for storage temperatures of domestic refrigerator as a risk factor of foodborne illness outbreak. Korean J. Food Sci. Technol. 42:373-376.
  34. Sarker, M. R., R. P. Shivers, S. G. Sparks, V. K. Juneja, and B. A. McClane. 2000. Comparative experiments to examine the effects of heating on vegetative cells and spores of Clostridium perfringens isolates carrying plasmid genes versus chromosomal enterotoxin genes. Appl. Environ. Microbiol. 66:3234-3240.
  35. Schneider, K. R., R. Goodrich-Schneider, M. A. Hubbard, and S. Richardson. 2014. Preventing Foodborne Illness Associated with Clostridium perfringens. University of Florida IFAS Extension. Accessed September 29, 2014.
  36. Udompijitkul, P., M. Alnoman, and M. R. Sarker. 2013. Inactivation strategy for Clostridium perfringens spores adhered to food contact surfaces. Food Microbiol. 34:328-336.
  37. Vose, D. J. 1998. The application of quantitative risk assessment to microbial food safety. J. Food Prot. 61:640-648.