Johnson (2001) reviewed the microbiology of cheese products and noted the complexity of the subject because of the great diversity in cheese manufacturing and ripening protocols, as well as composition of the different cheese types. The 60-day aging rule is based on the theory that pathogens, if present, will die-off to levels below the infectious dose during the aging process. However, the effectiveness of this system depends on the initial microbiological quality of the milk and other ingredients used, and the hygienic practices used during cheese processing (Donnelly 1990). No amount of curing or aging or even pasteurization will compensate for poor quality milk or lack of hygiene during manufacturing and storage.
The intrinsic properties of the cheesemaking process that affect pathogen survival and growth include:
- salt content
- redox potential
- cheese microbial flora including starter culture (microbial community)
Individually and in combination, these factors can have significant impacts on whether a foodborne pathogen survives or grows in cheese during curing. The effectiveness of these natural processes is ultimately dependent on the initial contamination level of the cheese. A high inoculum of a pathogen, especially one with a low infectious dose, will overwhelm these control systems. The soft and semi-soft surface-mold-ripened cheeses are at the greatest risk of contamination due to their higher pH and moisture content (D’Amico 2008a).
The presence of pathogens in milk used for production of raw milk cheeses represents a risk for consumers. Oliver (2009) reviewed the literature on pathogen prevalence in US bulk tank milk and found these levels.
- Campylobacter: 2 – 9.2%
- E. coli O157:H7: 0 – 0.75%
- Listeria monocytogenes: 2.8 – 7.0%
- Salmonella spp: 0 – 11%
- Shiga-toxin E. coli: 2.4 – 3.96%
- Yersinia enterocolitica: 1.2 – 6.1%
D’Amico (2008b and 2010) surveyed milk used to produce small-scale farmstead cheese in Vermont and found an overall low level of contamination, but documented variations from farm-to-farm indicating that some operations practice strict hygienic controls while other need improvement in their food safety practices.
Experimental studies of the behavior of pathogens in aged cheese show mixed results (Bachmann 1995; Back 1993; D’Amico 2008a; D’Amico 2008b; D’Amico 2010; Govaris 2002; Marth 1969; Reitsma 1996; Schlesser 2006). The studies are difficult to compare because of different experimental methods, and variations in how the cheese was manufactured for the experiments. For example, Reitsma (1996) found viable E. coli O157:H7 in cheddar cheese at 158 days, but used pasteurized milk in their comparisons. Schlesser (2006) inoculated cheddar cheese with a 5-strain E. coli O157:H7 cocktail and demonstrated an inadequate reduction at 60 days (1 log) and 120 days (2 logs); in contrast, heat treating the milk resulted in a 5-log reduction. D’Amico (2010) examined the behavior of E. coli O157:H7 in aged Gouda and stirred-cured cheddar cheeses manufactured from raw milk and was able to recover viable cells for more than 270 days in both cheese types using selective enrichment.
Listeria monocytogenes can be a pervasive problem in the dairy processing environment. There is evidence that L. monocytogenes can survive aging in both pasteurized and surface-mold-ripened cheeses if the pathogen is introduced post-processing (D’Amico 2008b). These findings underscore the importance of hygienic practices at cheesemaking facilities regardless of pasteurization status. D’Amico (2008a) provides a more comprehensive review of experimental studies using different pathogens and cheese types.
1. 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 61:1405-7.
2. Bachmann, H. P., and U. Spahr. 1995. The fate of potentially pathogenic bacteria in Swiss hard and semihard cheeses made from raw milk. J Dairy Sci 78:476-83.
3. Back, J. P., S. A. Langford, and R. G. Kroll. 1993. Growth of Listeria monocytogenes in Camembert and other soft cheeses at refrigeration temperatures. J Dairy Res 60:421-9.
4. CDC. 2000. Outbreak of Escherichia coli O157:H7 infection associated with eating fresh cheese curds–Wisconsin, June 1998. MMWR Morb Mortal Wkly Rep 49:911-3.
5. CDC. 2001. From the Centers for Disease Control and Prevention. Outbreak of Listeriosis associated with homemade Mexican-style cheese–North Carolina, October 2000-January 2001. JAMA 286:664-5.
6. CDC. 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 57:432-5.
7. CDC. 2009. Campylobacter jejuni Infection Associated with Unpasteurized Milk and Cheese — Kansas, 2007. MMWR Morb Mortal Wkly Rep 57:1377-1379.
8. CDC. OutbreakNet. Foodborne Outbreak Online Database. Available from: http://www.cdc.gov/foodborneoutbreaks/Default.aspx
9. CDC. 2010. Investigation Update: Multistate Outbreak of E. coli O157:H7 Infections Associated with Cheese. Available from: http://www.cdc.gov/ecoli/2010/cheese0157/index.html
10. Cody, S. H., S. L. Abbott, A. Marfin, B. Schulz, P. Wagner, K. Robbins, J. C. Mohle-Boetani, and D. J. Vugia. 1999. Two outbreaks of multidrug-resistant Salmonella serotype typhimurium DT104 infections linked to raw-milk cheese in Northern California. JAMA 281:1805-10.
11. D’Amico, D. 2008a. Incidence, ecology, and fate of target foodborne pathogens in the cheesemaking continuum. University of Vermon. Available from: http://library.uvm.edu/jspui/bitstream/123456789/165/1/damicofinal.pdf
12. D’Amico, D. J., M. J. Druart, and C. W. Donnelly. 2008b. 60-day aging requirement does not ensure safety of surface-mold-ripened soft cheeses manufactured from raw or pasteurized milk when Listeria monocytogenes is introduced as a postprocessing contaminant. J Food Prot 71:1563-71.
13. D’Amico, D. J., E. Groves, and C. W. Donnelly. 2008c. Low incidence of foodborne pathogens of concern in raw milk utilized for farmstead cheese production. J Food Prot 71:1580-9.
14. D’Amico, D. J., and C. W. Donnelly. 2010a. Microbiological quality of raw milk used for small-scale artisan cheese production in Vermont: effect of farm characteristics and practices. J Dairy Sci 93:134-47.
15. D’Amico, D. J., M. J. Druart, and C. W. Donnelly. 2010b. Behavior of Escherichia coli O157:H7 during the manufacture and aging of gouda and stirred-curd cheddar cheeses manufactured from raw milk. J Food Prot 73:2217-2224.
16. Deschenes, G., C. Casenave, F. Grimont, J. C. Desenclos, S. Benoit, M. Collin, S. Baron, P. Mariani, P. A. Grimont, and H. Nivet. 1996. Cluster of cases of haemolytic uraemic syndrome due to unpasteurised cheese. Pediatr Nephrol 10:203-5.
17. Desenclos, J. C., P. Bouvet, E. Benz-Lemoine, F. Grimont, H. Desqueyroux, I. Rebiere, and P. A. Grimont. 1996. Large outbreak of Salmonella enterica serotype paratyphi B infection caused by a goats’ milk cheese, France, 1993: a case finding and epidemiological study. BMJ 312:91-4.
18. De Valk, H., E. Delarocque-Astagneau, G. Colomb, S. Ple, E. Godard, V. Vaillant, S. Haeghebaert, P. H. Bouvet, F. Grimont, P. Grimont, and J. C. Desenclos. 2000. A community–wide outbreak of Salmonella enterica serotype Typhimurium infection associated with eating a raw milk soft cheese in France. Epidemiol Infect 124:1-7.
19. Dominguez, M., N. Jourdan-Da Silva, V. Vaillant, N. Pihier, C. Kermin, F. X. Weill, G. Delmas, A. Kerouanton, A. Brisabois, and H. de Valk. 2009. Outbreak of Salmonella enterica serotype Montevideo infections in France linked to consumption of cheese made from raw milk. Foodborne Pathog Dis 6:121-8.
20. Donnelly, C. W. 1990. Concerns of microbial pathogens in association with dairy foods. J Dairy Sci 73:1656-61.
21. FDA. 21 C.F.R. Part 133–Cheeses and Related Cheese Products. Available from: http://law.justia.com/us/cfr/title21/21cfr133_main_02.html
22. FDA. 21 C.F.R. Part 1240.61–Mandatory pasteurization for all milk and milk products in final package form intended for direct human consumption. Available from: http://law.justia.com/us/cfr/title21/21-220.127.116.11.18.104.22.168.html
23. FSANZ. 2006. A risk profile of dairy products in Australia. Available from: http://www.foodstandards.gov.au/_srcfiles/P296%20Dairy%20PPPS%20FAR%20Attach%202%20FINAL%20-%20mr.pdf
24. Govaris, A., D. K. Papageorgiou, and K. Papatheodorou. 2002. Behavior of Escherichia coli O157:H7 during the manufacture and ripening of feta and telemes cheeses. J Food Prot 65:609-15.
25. Haeghebaert, S., P. Sulem, L. Deroudille, E. Vanneroy-Adenot, O. Bagnis, P. Bouvet, F. Grimont, A. Brisabois, F. Le Querrec, C. Hervy, E. Espie, H. de Valk, and V. Vaillant. 2003. Two outbreaks of Salmonella enteritidis phage type 8 linked to the consumption of Cantal cheese made with raw milk, France, 2001. Euro Surveill 8:151-6.
26. Headrick, M. L., S. Korangy, N. H. Bean, F. J. Angulo, S. F. Altekruse, M. E. Potter, and K. C. Klontz. 1998. The epidemiology of raw milk-associated foodborne disease outbreaks reported in the United States, 1973 through 1992. Am J Public Health 88:1219-21.
27. 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 96:182-4.
28. Jaros, P., N. Cogger and N. French. 2008. A systematic review of the human disease evidence associated with the consumption of raw milk and raw milk cheeses. A report prepared for the New Zealand Food Safety Authority (NZFSA). Availabel from: http://www.nzfsa.govt.nz/science/research-projects/final-report-rawmilk.pdf
29. Johnson, M.E. 2002. Cheese products. In: Applied Dairy Microbiology, 2nd Ed., Marth, E. H. and J.L. Steele (eds), Ch. 11, p.345-384.
30. MacDonald, P. D., R. E. Whitwam, J. D. Boggs, J. N. MacCormack, K. L. Anderson, J. W. Reardon, J. R. Saah, L. M. Graves, S. B. Hunter, and J. Sobel. 2005. Outbreak of listeriosis among Mexican immigrants as a result of consumption of illicitly produced Mexican-style cheese. Clin Infect Dis 40:677-82.
31. Marler, W. 2009. Comparing the food safety record of pasteurized and raw milk products – Part 3. Available from: https://www.marlerblog.com/lawyer-oped/comparing-the-food-safety-record-of-pasteurized-and-raw-milk-products—part-3/.
32. Marth, E. H. 1969. Salmonellae and salmonellosis associated with milk and milk products. A review. J Dairy Sci 52:283-315.
33. Oliver, S. P., K. I., Boor, S. C. Murphy, and S.e E. Murinda. 2009. Food safety hazards associated with consumption of raw milk. Foodborne Pathog Dis. 6:793-806.
34. 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.
35. Reitsma, C. and D. H. Henning. 1996. Survival of enterohemmorrhagic Escherichia coli O157:H7 during the manufacture and curing of cheddar cheese. J Food Prot 59:460-464.
36. Schlesser, J. E., R. Gerdes, S. Ravishankar, K. Madsen, J. Mowbray, and A. Y. Teo. 2006. Survival of a five-strain cocktail of Escherichia coli O157:H7 during the 60-day aging period of cheddar cheese made from unpasteurized milk. J Food Prot 69:990-8.
37. Sheehan, J., R. Childers, and S. Clanci. 2004. Ask the regulators: enhancing the safety of dairy and other animal based foods. Available from: http://www.foodsafetymagazine.com/article.asp?id=1354&sub=sub1
38. Villar, R. G., M. D. Macek, S. Simons, P. S. Hayes, M. J. Goldoft, J. H. Lewis, L. L. Rowan, D. Hursh, M. Patnode, and P. S. Mead. 1999. Investigation of multidrug-resistant Salmonella serotype typhimurium DT104 infections linked to raw-milk cheese in Washington State. Jama 281:1811-6.
39. Werner, S. B., G. L. Humphrey, and I. Kamei. 1979. Association between raw milk and human Salmonella dublin infection. Br Med J 2:238-41.