Advanced SearchSearch Tips
Cheese Microbial Risk Assessments - A Review
facebook(new window)  Pirnt(new window) E-mail(new window) Excel Download
 Title & Authors
Cheese Microbial Risk Assessments - A Review
Choi, Kyoung-Hee; Lee, Heeyoung; Lee, Soomin; Kim, Sejeong; Yoon, Yohan;
  PDF(new window)
Cheese is generally considered a safe and nutritious food, but foodborne illnesses linked to cheese consumption have occurred in many countries. Several microbial risk assessments related to Listeria monocytogenes, Staphylococcus aureus, and Escherichia coli infections, causing cheese-related foodborne illnesses, have been conducted. Although the assessments of microbial risk in soft and low moisture cheeses such as semi-hard and hard cheeses have been accomplished, it has been more focused on the correlations between pathogenic bacteria and soft cheese, because cheese-associated foodborne illnesses have been attributed to the consumption of soft cheeses. As a part of this microbial risk assessment, predictive models have been developed to describe the relationship between several factors (pH, Aw, starter culture, and time) and the fates of foodborne pathogens in cheese. Predictions from these studies have been used for microbial risk assessment as a part of exposure assessment. These microbial risk assessments have identified that risk increased in cheese with high moisture content, especially for raw milk cheese, but the risk can be reduced by preharvest and postharvest preventions. For accurate quantitative microbial risk assessment, more data including interventions such as curd cooking conditions (temperature and time) and ripening period should be available for predictive models developed with cheese, cheese consumption amounts and cheese intake frequency data as well as more dose-response models.
Predictive Model;Cheese;Microbial Risk Assessment;
 Cited by
Microbiological quality and safety assessment in the production of moderate and high humidity cheeses, Ciência Rural, 2017, 47, 11  crossref(new windwow)
Altekruse, S. F., B. B. Timbo, J. C. Mowbray, N. H. Bean, and M. E. Potter. 1998. Cheese-associated outbreaks of human illness in the United States, 1973 to 1992: Sanitary manufacturing practices protect consumers. J. Food Prot. 61:1405-1407. crossref(new window)

Bille, J., D. S. Blanc, H. Schmid, K. Boubaker, A. Baumgartner, H. H. Siegrist, M. L. Tritten, R. Lienhard, D. Berner, R. Anderau, M. Treboux, J. M. Ducommun, R. Malinverni, D. Genne, P. H. Erard, and U. Waespi. 2006. Outbreak of human listeriosis associated with tomme cheese in northwest Switzerland, 2005. Euro Surveill. 11:91-93.

Bozkurt, H. and O. Erkmen. 2001. Predictive modeling of Yersinia enterocolitica inactivation in Turkish Feta cheese during storage. J. Food Eng. 47:81-87. crossref(new window)

CDC (Centers for Disease Control and Prevention). 2001. Outbreak of listeriosis associated with homemade Mexicanstyle cheese-North Carolina, October 2000-January 2001. MMWR Morb. Mortal. Wkly. Rep. 50:560-562.

CDC (Centers for Disease Control and Prevention). 2008. Outbreak of multidrug-resistant Salmonella enterica serotype Newport infections associated with consumption of unpasteurized Mexican-style aged cheese-Illinois, March 2006-April 2007. MMWR Morb. Mortal. Wkly. Rep. 57:432-435.

CDC (Centers for Disease Control and Prevention). 2010a. Staphylococcal food poisoning. Accessed January 6, 2015.

CDC (Centers for Disease Control and Prevention). 2010b. Investigation update: Multistate outbreak of E. coli O157:H7 infections associated with cheese. Accessed January 8, 2015.

CDC (Centers for Disease Control and Prevention). 2013a. Listeria (Listeriosis). Accessed January 12, 2015.

CDC (Centers for Disease Control and Prevention). 2013b. Vital signs: Listeria illnesses, deaths, and outbreaks-United States, 2009-2011. MMWR Morb. Mortal. Wkly. Rep. 62:448-452.

CDC (Centers for Disease Control and Prevention) 2013c Listeria and food. Accessed January 21, 2015.

CDC (Centers for Disease Control and Prevention). 2014a. Foodborne outbreak online database. Accessed January 6, 2015.

CDC (Centers for Disease Control and Prevention). 2014b. Multistate outbreak of listeriosis linked to Roos Foods dairy products (final update). Accessed January 9, 2015.

CDC (Centers for Disease Control and Prevention). 2014c. Multistate outbreak of Salmonella Stanley Infections linked to raw Cashew cheese (final update). Accessed January 8, 2015.

CDC (Centers for Disease Control and Prevention). 2014d. List of Selected Multistate Foodborne Outbreak Investigations. Accessed January 4, 2014.

CDIC (Canadian Dairy Information Centre). 2014. Global consumption per capita of dairy products: Total cheese consumption. Accessed January 5, 2015.

CCE (Clemson Cooperative Extension). 2008. Handling of cheese for safety & quality. Accessed July 29, 2015.

Codex. 1999. Principles and guidelines for the conduct of microbiological risk assessment. CAC/GL-30. Accessed December 28, 2014.

Codex. 2000. Codex general standard for cheese (Codex Standard 283-1978). Accessed January 15, 2015.

Delbes, C., J. Alomar, N. Chougui, J. F. Martin, and M. C. Montel. 2006. Staphylococcus aureus growth and enterotoxin production during the manufacture of uncooked, semihard cheese from cows' raw milk. J. Food Prot. 69:2161-2167. crossref(new window)

European Commission. 2007. Commission regulation EC No 1441/2007 of 5 December 2007. OJEU. 322:12-29.

EFSA/ECDC (European Food Safety Authority/European Centre for Disease Prevention and Control). 2011. The European Union summary report on trends and sources of zoonosis, zoonotic agents and food-borne outbreaks in 2009. EFSA J. 9:2090. crossref(new window)

FDA (Food and Drug Administration). 2003. Quantitative assessment of relative risk to public health from foodborne Listeria monocytogenes among selected categories of ready-toeat foods. Accessed January 5, 2014.

FDA (Food and Drug Administration). 2012a. Joint FDA/Health Canada quantitative assessment of the risk of listeriosis from soft-ripened cheese consumption in the United States and Canada: draft interpretative summary. Accessed January 5, 2015.

FDA (Food and Drug Administration). 2012b. Bad Bug Book: Handbook of foodborne pathogenic microorganisms and natural toxins. Accessed January 12, 2015.

FDA/USDA (Food and Drug Administration/U.S. Department of Agriculture). 2003. Quantitative assessment of the relative risk to public health from foodborne Listeria monocytogenes among selected categories of ready-to-eat foods. Accessed January 5, 2015.

Food Standards. 2009. Microbiological risk assessment of raw milk cheese. Accessed January 5, 2015.

Fratamico, P. M. and D. O. Bayles. 2005. Molecular approaches for detection, identification, and anlysis of foodborne pathogens. In: Foodborne pathogens: Microbiology and molecular biology (Eds. P. M. Fratamico, A. K. Bhunia, and J. L. Smith). Caister Academic Press, Norfolk, UK. pp. 1-14.

Fretz, R., U. Sagel, W. Ruppitsch, A. T. Pietzka, A. Stoger, S. Huhulescu, S. Heuberger, J. Pichler, P. Much, G. Pfaff, K. Stark, R. Prager, A. Flieger, O. Feenstra, and F. Allerberger. 2010. Listeriosis outbreak caused by acid curd cheese 'Quargel', Austria and Germany 2009. Euro Surveill. 15:pii=19477.

Genigeorgis, C., M. Carniciu, D. Dutulescu, and T. B. Farver. 1991. Growth and survival of Listeria monocytogenes in market cheeses stored at 4 to 30$^{\circ}C$. J. Food Prot. 54:662-668. crossref(new window)

Goldin, B. R. and S. L. Gorbach. 1992. Probiotics for humans. In. Probiotics. The scientific basis (Ed. R. Fuller) Chapman & Hall, London, UK. pp. 355-376.

Gould, L. H., E. Mungai, and C. B. Behravesh. 2014. Outbreaks attributed to cheese: Differences between outbreaks caused by unpasteurized and pasteurized dairy products, United States, 1998-2011. Foodborne Pathog. Dis. 11:545-551. crossref(new window)

Gyles, C. L. 2007. Shiga toxin-producing Escherichia coli: An overview. J. Anim. Sci. 85(13 Suppl):E45-E62. crossref(new window)

Honish, L., G. Predy, N. Hislop, L. Chui, K. Kowalewska-Grochowska, L. Trottier, C. Kreplin, and I. Zazulak. 2005. An outbreak of E. coli O157:H7 hemorrhagic colitis associated with unpasteurized Gouda cheese. Can. J. Public Health. 96:182-184.

Institute of Medicine (US) Committee to Review Dietary Reference Intakes for Vitamin D and Calcium; A. C. Ross, C. L. Taylor, A. L. Yaktine, and H. B. Del Valle. 2011. Dietary reference intakes for calcium and vitamin D. National Academies Press, Washington, DC, USA.

Jackson, K. A., M. Biggerstaff, M. Tobin-D'Angelo, D. Sweat, R. Klos, J. Nosari, O. Garrison, E. Boothe, L. Saathoff-Huber, L. Hainstock, and R. P. Fagan. 2011. Multistate outbreak of Listeria monocytogenes associated with Mexican-style cheese made from pasteurized milk among pregnant, Hispanic women. J. Food Prot. 74:949-953. crossref(new window)

Janstova, B., L. Necidova, A. Skockova, and B. Janstova. 2014. Staphylococcal enterotoxin production in model samples of milk and fresh cheese. J. Food Nutr. Res. 53:389-392.

Johnson, M. E. 2001. Cheese products. In: Applied dairy microbiology, 2nd ed. (Eds. E. H. Marth and J. L. Steele). Marcel Dekker, Inc., New York, NY, USA. pp. 345-384.

Kathariou, S. 2002. Listeria monocytogenes virulence and pathogenicity, a food safety perspective. J. Food Prot. 65:1811-1829. crossref(new window)

Kosikowski, F. and V. V. Mistry. 1997. Cheese and fermented milk foods. 3rd edn. F. V. Kosikowski, Westport, CT, USA.

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. crossref(new window)

Kowalik, J. and A. Lobacz. 2015. Development of predictive model describing the growth of Yersinia enterocolitica in Camembert-type chees. Int. J. Food Sci. Technol. 50:811-818. crossref(new window)

Lake, R., A. Hudson, P. Cressey, and S. Gilbert. 2005a. Risk profile: Listeria monocytogenes in low moisture cheeses. Client report FW0440 of New Zealand Food Safety Authority. Accessed January 5, 2015.

Lake, R., A. Hudson, P. Cressey, and S. Gilbert. 2005b. Risk profile: Listeria monocytogenes in soft cheeses. Client report FW0382 of New Zealand Food Safety Authority. Accessed January 5, 2015.

Le Loir, Y., F. Baron, and M. Gautier. 2003. Staphylococcus aureus and food poisoning. Genet. Mol. Res. 2:63-67.

Lee, H., K. Kim, S. Lee, M. Han, and Y. Yoon. 2014. Growth kinetics of Staphylococcus aureus on Brie and Camembert cheeses. J. Dairy Res. 81:252-256. crossref(new window)

Lindqvist, R., S. Sylven, and I. Vagsholm. 2002. Quantitative microbial risk assessment exemplified by Staphylococcus aureus in unripened cheese made from raw milk. Int. J. Food Microbiol. 78:155-170. crossref(new window)

Maguire, H. C., M. Boyle, M. J. Lewis, J. Pankhurst, A. A. Wieneke, M. Jacob, J. Bruce, and M. O'Mahony. 1991. A large outbreak of food poisoning of unknown aetiology associated with Stilton cheese. Epidemiol. Infect. 106:497-505. crossref(new window)

Makino, S. I., K. Kawamoto, K. Takeshi, Y. Okada, M. Yamasaki, S. Yamamoto, and S. Igimi. 2005. An outbreak of food-borne listeriosis due to cheese in Japan, during 2001. Int. J. Food Microbiol. 104:189-196. crossref(new window)

MDA (Missouri Department of Agriculture). 2010. Missouri agriculture, health officials investigate reports of bacteria found in Missouri cheese sold in California. Accessed January 4, 2015.

Moreno-Enriquez, R. I., A. Garcia-Galaz, E. Acedo-Felix, I. H. Gonzalez-Rios, J. E. Call, J. B. Luchansky, and M. E. Diaz-Cinco. 2007. Prevalence, types, and geographical distribution of Listeria monocytogenes from a survey of retail Queso Fresco and associated cheese processing plants and dairy farms in Sonora, Mexico. J. Food Prot. 70:2596-2601. crossref(new window)

Moustafa, M. K. 1990. Isolation of Yersinia enterocolitica from raw milk and soft cheese in Assiut city. Assiut Vet. Med. J. 23:106-109.

Mozaffarian, D., H. Cao, I. B. King, R. N. Lemaitre, X. Song, D. S. Siscovick, and G. S. Hotamisligil. 2010. Trans-palmitoleic acid, metabolic risk factors, and new-onset diabetes in U.S. adults: A cohort study. Ann. Intern. Med. 153:790-799. crossref(new window)

Normanno, G., G. La Salandra, A. Dambrosio, N. C. Quaglia, M. Corrente, A. Parisi, G. Santagada, A. Firinu, E. Crisetti, and G. V. Celano. 2007. Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. Int. J. Food Microbiol. 115:290-296. crossref(new window)

Northolt, M. D. 1984. Growth and inactivation of pathogenic microorganisms during manufacture and storage of fermented dairy products: A review. Neth. Milk Dairy J. 38:135-150.

Ostyn, A., M. L. De Buyser, F. Guillier, J. Groult, B. Felix, S. Salah, G. Delmas, and J. A. Hennekinne. 2010. First evidence of a food poisoning outbreak due to staphylococcal enterotoxin type E, France, 2009. Euro Surveill. 15:pii=19528.

Pelisser, M. R., C. S. Klein, K. R. Ascoli, T. R. Zotti, and A. C. Arisi. 2009. Ocurrence of Staphylococcus aureus and multiplex PCR detection of classic enterotoxin genes in cheese and meat products. Braz. J. Microbiol. 40:145-148. crossref(new window)

Perrin, F., F. Tenenhaus-Aziza, V. Michel, S. Miszczycha, N. Bel, and M. Sanaa. 2015. Quantitative risk assessment of haemolytic and uremic syndrome linked to O157:H7 and non-O157:H7 shiga-toxin producing Escherichia coli strains in raw milk soft cheeses. Risk Anal. 35:109-128. crossref(new window)

Rabello, R. F., B. M. Moreira, R. M. Lopes, L. M. Teixeira, L. W. Riley, and A. C. Castro. 2007. Multilocus sequence typing of Staphylococcus aureus isolates recovered from cows with mastitis in Brazilian dairy herds. J. Med. Microbiol. 56(Pt 11):1505-1511. crossref(new window)

Reiter, B., B. G. Fewins, T. F. Fryer, and M. E. Sharpe. 1964. Factors affecting the multiplication and survival of coagulase positive Staphylococci in Cheddar cheese. J. Dairy Res. 31:261-272. crossref(new window)

Rosshaug, P. S., A. Detmer, H. Ingmer, and M. H. Larsen. 2012. Modeling the growth of Listeria monocytogenes in soft bluewhite cheese. Appl. Environ. Microbiol. 78:8505-8514.

Rosso, L. 1995. Modeling and Predictive Microbiology: Development of a New Tool for the Food Industry. Ph.D. Thesis, University Claude Bernard, Lyon, France.

Ryser, E. T. 2001. Public Health Concerns. In: Applied dairy microbiology, 2nd ed. (Eds. E. H. Marth and J. L. Steele). Marcel Dekker, Inc., New York, NY, USA. pp. 397-546.

Ryser, E. T. and E. H. Marth. 1987a. Behavior of Listeria monocytogenes during the manufacture and ripening of cheddar cheese. J. Food Prot. 50:7-13. crossref(new window)

Ryser, E. T. and E. H. Marth. 1987b. Fate of Listeria monocytogenes during the manufacture and ripening of Camembert cheese. J. Food Prot. 50:372-378. crossref(new window)

Sanaa, M., L. Coroller, and O. Cerf. 2004. Risk assessment of listeriosis linked to the consumption of two soft cheeses made from raw milk: Camembert of Normandy and Brie of Meaux. Risk Anal. 24:389-399. crossref(new window)

Schvartzman, M. S., U. Gonzalez-Barron, F. Butler, and K. Jordan. 2014. Modeling the growth of Listeria monocytogenes on the surface of smear-or mold-ripened cheese. Front. Cell Infect. Microbiol. 4:90.

Simeao do Carmoa, L., R. Souza Dias, V. R. Linardi, M. Jose de Sena, D. Aparecida dos Santos, M. Eduardo de Faria, E. Castro Pena, M. Jett, and L. Guilherme Heneine. 2002. Food poisoning due to enterotoxigenic strains of Staphylococcus present in Minas cheese and raw milk in Brazil. Food Microbiol. 19:9-14. crossref(new window)

USDA/ARS (U.S. Department of Agriculture/Agricultural Research Service). 2011. National nutrient database for standard reference release 27. January 5, 2015.

USDA/ERS (U.S. Department of Agriculture/Economic Research Service). 2014. Dairy products: Per capita consumption, United State (Annual). Accessed January 15, 2015.

EPA (U.S. Environmental Protection Agency). 2012. Microbial risk assessment guideline: pathogenic microorganisms with focus on food and water. Accessed January 4, 2015.

van Cauteren, D., N. Jourdan-da Silva, F. X. Weill, L. King, A. Brisabois, G. Delmas, V. Vaillant, and H. de Valk. 2009. Outbreak of Salmonella Enterica serotype Muenster infections associated with goat's cheese, France March 2008. Euro Surveill. 14:pii=19290.

Wing, E. J. and S. H. Gregory. 2002. Listeria monocytogenes: Clinical and experimental update. J. Infect. Dis. 185(Suppl 1):S18-S24. crossref(new window)

Yousef, A. E. and E. H. Marth. 1988. Behavior of Listeria monocytogenes during the manufacture and storage of Colby cheese. J. Food Prot. 51:12-15. crossref(new window)