SAFETY OF PASTEURIZED-CHILLED FOOD
Copyright 1997 by O. Peter Snyder, Jr., Ph.D.
Hospitality Institute of Technology and Management
670 Transfer Road, Suite 21A
St. Paul, Minnesota  55114   USA
Revised March 2003


What Is A Retail "Chilled" Food System?
Actually, a retail "chilled" food system is misnamed. It is simply an extension of conventional retail pasteurized food systems.

1. Food is cooked and transferred hot to a package, which is sealed and cooled, or
2. Food is cooked, cooled, transferred without pathogen contamination to a package, and sealed or
3. Packaged food is cooked, cooled, and then, kept chilled to control the outgrowth of spores that survive pasteurization.

The important principle is that the more severe the heating (cooking) process after pasteurization has been achieved (e.g., above 130F for 87 minutes), the further the spoilage microorganisms are reduced. Hence, the refrigerated shelf life of the product is extended. A second principle is that the closer the temperature of the food product during storage is to freezing temperatures of 28 to 32F (freezing point, which depends on salt and sugar content), the longer the shelf life. Yeasts and molds can grow at temperatures as low as 14F. Bacteria can grow at 23F.

Table 1 shows holding times based on the 1997 FDA Food Code (2), which sets the standard for cold holding of food at 41F for 7 days, 45F for 4 days, and 4 hours between 45 and 140F. The other temperatures and times are derived using the Ratkowsky predictive growth equation (4).
 

Table 1. FDA-derived Holding Times at Specified Temperatures


 
Temperature
Safe Storage Time
C
Days
55
50
45*
41*
40
35
30
12.8
10.0
7.2
5.0
4.4
1.7
-1.1
1.7
2.4
4.0
7
7.5
19.3
123.8
  * FDA 1997 Food Code recommended cold food holding temperature.


Why Not Frozen Food?
What is the major advantage of refrigerated pasteurized food vs. frozen food? Mainly, it is convenience. Frozen food will have a shelf life of 6 months or more. However, frozen food must be thawed. The thawing process requires time and energy. Expensive, energy-intensive equipment is also required to freeze and hold the food products frozen. Normally, foodservice operations do not need the long shelf life of frozen food. Chilled foods, some of which can have a shelf life of 60 days, are much more efficient to handle.

Pasteurization
Pasteurization is achieved by heating food to a temperature for a time that is sufficient to reduce the vegetative pathogenic microorganism contamination in food to a safe level. Pasteurization of milk was established many years ago to ensure its safety. Pasteurized milk in the U.S. is heated to 145F for 30 minutes or to 161F and held at this temperature for 15 seconds. This standard for pasteurizing milk is well established and has never failed to make milk safe. Today, in food, the target organism is Salmonella spp., and pasteurization is designed to reduce the Salmonella population by 10-5.

The USDA / FDA pasteurization standard (1) for cooking raw beef (temperatures and times necessary to ensure the safety of ground beef, etc.) is derived from research of Goodfellow and Brown (3). The original requirements were for a 10-7 reduction in beef. When hamburger became a problem, the reduction was set at 10-5 Salmonella reduction, as shown in Table 2.
 

Table 2. Food Pasteurization Table


 
Temperature
Pasteurization Time for Destruction of Salmonella
F
C
105 to 1 / gram reduction
130
54.4
86.45 min.
135
57.2
27.35 min.
140
60.0
8.65 min.
145
62.2
2.74 min.
150
65.5
0.865 min. (51.9 sec.)
155
68.3
0.274 min. (16.5 sec.)
160
71.1
0.0865 min. (5.19 sec.)
165
73.8
0.0274 min. (1.65 sec.)

What is Safe?
"Safe" is usually defined as undetectable vegetative infective pathogens such as Salmonella spp., Listeria monocytogenes, and Escherichia coli O157:H7, usually in a 25-gram sample. The 10-5reduction for Salmonella spp. is based on the principle that there are, at most, about 103 Salmonella spp. per gram of beef normally present in the retail marketplace. Pasteurization of food reduces this hypothetical population to a safe level of 1 vegetative cell of Salmonella in 100 grams of sample.

It is important to know that naturally contaminating spores of Clostridium perfringens, Clostridium botulinum, and Bacillus cereus survive pasteurization and will be present in the food. However, the outgrowth of these pathogenic spores in extended-shelf-life, chilled food products during storage is prevented by maintaining appropriate refrigeration temperatures.

The Pasteurized Food Processes
As mentioned at the beginning, there are three basic processes used to produce pasteurized food. The first is "pasteurize, package, then cool." The second is "pasteurize, cool, then package." The third is "package, pasteurize, then cool." The third is what is generally called sous vide.

Retail, pasteurized, "chilled" food operations utilize the "pasteurize , package, then cool" method for preparing many products (e.g., soups, stews, sauces etc.). Food is pasteurized in a kettle, oven, or other cooking device, packaged while still hot in a barrier-type plastic bag, and then cooled. The hazard controls for this process are as follows.

1. The food is pasteurized (heated sufficiently to destroy vegetative pathogenic microorganisms).
2. The food is packed hot (above 160F) so that there is no vegetative pathogen contamination in the food when it is packaged (in a plastic bag or casing, a glass jar, paper carton, or can). Packaging prevents contamination during storage and transport.
3. Solid food is blast cooled less than 2 inches thick in less than 6 hours to 41F. Actually, 15-hour, continuous cooling to 45F is safe. Liquid foods are packaged in plastic casings and are tumble chilled to 45F within 0.75 hour to 1.5 hours. The food is stored at 32F or less for extended shelf life.
4. The food is stored at less than 38F to assure the control of the outgrowth of the surviving pathogenic spores. Note that the food is an anaerobic package. Anaerobic spoilage microorganisms such as the lactic acid bacteria and spores of some molds and yeasts, in addition to pathogenic spores, will survive the pasteurization process and will be present in the product. Normal storage of chilled food is 28 to 32F to control spoilage. Because some spoilage bacteria can begin to multiply at 23F, the food will eventually "spoil safe." For example, pasteurized milk and other pasteurized foods that have been kept cold spoil first as a warning that the food is old and should not be consumed.

 The second process, "pasteurize, cool, then package," is typical of normal kitchen operations. The food in this case has a much shorter shelf life (i.e., 7 to 14 days), because the holding container in which the food is stored is not sterile, and the packaging environment is not completely sterile. Hence, spoilage (not pathogenic) microorganisms get into the food during packaging. This process is very common in meat processing, whereby all deli-sliced and packaged luncheon meats with shelf lives up to 60 days are done this way. Pasteurized-cooled-packaged meats and poultry are cut and packaged in highly sanitized packaging room.

The third process, "package, pasteurize, then cool," is typical of sous vide and is illustrated by roast beef and turkey rolls, sliced to order in delis. It is easier to assure the safety of these products than pasteurized-packaged-cooled products, because these products are packaged prior to being pasteurized. The meat or other food product is either placed or pumped into a plastic package. The package may be vacuum sealed to cause the plastic to adhere to the surface of the product to assure good heat transfer. A heat-shrink plastic may also be used to accomplish the same purpose. It forms a skin-tight package, which facilitates good heat transfer when the food is heated. After the food is placed in bags and sealed, the bags are loaded into steam ovens or into water bath cook tanks. The heat is turned on, and the food is heated (cooked) to a center temperature of 130F and above, depending on the desired doneness of the food, and held at the temperature for sufficient time to assure pasteurization. A temperature control probe is inserted into the largest package of food, which is placed in the center of the mass of food being cooked. This probe is used to control the pasteurization process. The food is heated (cooked) to a desired end point for a time that always exceeds pasteurization requirements. Cook time for a typical 10-pound beef roast, about 6 inches in diameter, is 5 hours to the center food end point temperature. When the designated temperature is achieved, if it is cooked in a hot water tank, the hot water drains from the cook tank, and tap water at about 60F fills the tank. The refrigeration system in the cook tank turns on, and the food and the water cool so that the center of the package of food is less than 40F in about 5 hours. Smaller packages of food cooked in a steam oven are transferred to refrigerated rooms and cooled in less than 6 hours to 41F.

This third process also includes the so-called sous vide food, which is exactly the same process as the roast beef and turkey rolls, except that the package of food is single-portion food, and the package is typically less than 3/4 inch thick. The critical controls for the "package, pasteurize, then cool" process are the same as those already discussed for pasteurized-packaged-cooled foods.

Control of the Hazards
Table 3 (at the end of this paper) is a summary of the control of food pathogens. By examining this table, it can be seen that two major pathogens, L. monocytogenes and Yersinia enterocolitica, begin to multiply at 29.3F. Therefore, it is critical that they be destroyed by the pasteurization process. The pasteurization values for these organisms, as shown in the table, indicate that if the food is given a 10-5Salmonella spp. reduction, these pathogens will also be controlled to a safe level.

The hazard in foodservice pasteurized-chilled food systems will be the spores, which normally survive pasteurization. The pathogenic microorganisms that have the lowest temperature for spore outgrowth are non-proteolytic types of C. botulinum, which begin to multiply at 38F. These spores are destroyed at 185F and have usually only been found to be a hazard in fish stored at room temperature (70F) for a few days. Pasteurized crab is actually cooked to 185F for 15 minutes to assure destruction of this microorganism.

If pasteurized-chilled foods are kept at less than 38F, there is absolutely no hazard. There can even be food temperature fluctuations above 38F for a few days to perhaps 45F. Because the spores do not grow out and produce toxin instantly above 38F, the food remains safe. At 40F, it will take about 43 days for toxin to be produced (4). At 50F, the time for toxin production from non-proteolytic C. botulinum is about 9.4 days (4).

Another spore hazard is B. cereus, which can begin to outgrow at 39.2F (5). Proteolytic C. botulinum, which begins to produce toxin at 50F, is also hazardous. Again, like non-proteolytic C. botulinum, toxin production is very slow, even at 55F, which is the highest abusive refrigeration temperature that has been noted, and only for a small percent of the time in retail food store operations. Whenever there has been a hazard from C. botulinum, the food has been at room temperature (70F or above) for a few days.

The final threat is C. perfringens. It does not begin to multiply until the food is at a temperature of 59F. Since chilled food is stored below this temperature, it is reasonable to assume that there is no risk for growth of this pathogen in pasteurized-chilled food systems.

Spoilage Control
A very important control factor is also the presence and growth of spoilage microorganisms. Invariably, spoilage microorganisms survive pasteurization, because there are many more on raw food, and many of these are more resistant to heat inactivation than vegetative pathogenic microorganisms. Depending on the severity of the pasteurization process and level of reduction, the spoilage microorganisms will eventually multiply in the food to a level above 107 to 108 CFU per gram. Many enzymes in food must be heated to above 160 to be inactivated. When the number of spoilage microorganisms reaches this population level in food, the accumulation of waste products in the food produces such adverse changes in the food (e.g., change in color, flavor, and odor) that the food will no longer be consumed. People will consider it to be spoiled. Time at which spoilage occurs is dependent on the temperatures reached during the final cooking process. Foods such as milk pasteurized to 161F for 15 seconds remain "fresh" for about 14 days before they begin to spoil. Roast, cooked-in-bag beef (which actually takes about 5 hours to heat to pasteurization temperatures and 5 hours to cool to 40F) will be considered spoiled in about 60 days at 35 to 38F. Soup cooked to 190F can still be acceptable for 6 months if stored at less than 38F.

Cleveland Range Pasteurized-chilled Food Systems
Cleveland Range, Inc. sells a chilled food system that has been designed to control hazards. When the system is sold, the user is trained how to use the system properly to maintain hazard control. In the case of food that is cooked, packaged, then chilled, the food is heated to specified pasteurization temperatures for specified times in kettles designed by Cleveland Range. After the specified pasteurization of the food has occurred, the food is pumped under sanitary controlled conditions into microbiologically safe, sanitary bags or casings. The bags are sealed and then chilled to less than 40° F in less than 1 hour. The chilled bags of food are then transferred to cold storage at 28 to 30F until time of distribution and use. This food, when stored below 38F, can be stored until spoiled, because there are no microbiological risks. The chemical and physical hazards are controlled prior to pasteurization.

Food production personnel who prepare the chilled food products throughout production follow rigid procedures of personal sanitation and hygiene. Equipment is cleaned and sanitized following approved USDA-FDA process procedures.

In Summary - Why Pasteurized (Chilled) Food Systems Where Food Is Stored at Less Than 38F Are Totally Safe
1 Personnel and equipment are kept safe from infective pathogens through correct GMPs (Good Manufacturing Practices).
2 Vegetative pathogenic bacteria, viruses, and parasites have been inactivated by the pasteurization process time and temperature.
3. Pasteurized-packaged-cooled products are pumped under carefully controlled sanitary conditions (both personnel and equipment) in order to prevent any cross-contamination. Packaged-pasteurized-cooled items must not be contaminated after cooking. For pasteurized-cooled-packaged foods, the post-cooling handling is done in a very clean environment.
4. The food is cooled sufficiently fast so that there is no spore outgrowth.
5. Spores of C. botulinum, types A, B, and E, C. perfringens, and B. cereus will not outgrow or produce toxins at less than 38F.
6. Shelf life of products will depend on (a) flavor changes due to chemical reactions (oxidation) within the food system and (b) the accumulation of by-products resulting from the growth of some lactic and other anaerobic psychrotrophic microorganisms that may have survived the heating process and can eventually grow to a population of 106 to 107 per gram, causing the food to spoil. Chilled foods at less than 55F have been shown historically to "spoil safe." Spoilage microorganisms outgrow the pathogenic microorganisms, indicating that the food has been abused.

All of these food products are commonly produced by USDA-inspected meat plants. The USDA has never had standards for storage time for any of these foods. Apparently, the USDA does not believe that there is a hazard. Length of storage life depends on the initial level of spoilage microorganisms.

Tank-cooked (packaged-pasteurized-cooled) roast beef and turkey deli products (including sectioned and formed roasts, chunked and formed roasts, and cooked corned beef) are processed as described by 9 CFR § 318.17 (1). These products have been proven to be absolutely safe. Millions of pounds of these products have been sold in delis and retail food operations throughout the United States. It is common for these products to have a 60-day or more shelf life. This can be verified by looking at the packing dates of these products sold in delicatessens.

Conclusion
Pasteurized, extended refrigerated shelf life food has been produced for many years by trained commercial processors without any foodborne illness incidents. If a processor follows USDA guidelines [time and temperature specifications for a 5D (10-5 per gram) Salmonella reduction], products will be safe and of acceptable quality for 14 days to as long as 180 days, depending on the severity of the heating process, level of spoilage microorganisms, and refrigeration storage temperatures. A very important safety factor is that spoilage microorganisms that grow well at 30F will survive the pasteurization process. Therefore, the food spoils due to flavor changes as a result of oxidative changes and multiplication of psychrotrophic (low-temperature growth) microorganisms. The result is the remarkable history of safe, refrigerated, pasteurized food that has been enjoyed by the consuming public throughout the United States, Europe, and Japan for many years.
 

References
1. Code of Federal Regulations (CFR). 1995. Title 9. Animal and Animal Products. 200 to end. 318.17 Requirements for the production of cooked beef, roast beef, roast beef, and cooked corned beef. Superintendent of Documents. U.S. Govt. Printing Office. Washington, D.C.
2. FDA (Food and Drug Administration). 1995. Food Code. U.S. Public Health Service, U.S. Dept. of Commerce. Technology Administration, National Technical Information Service. Pub. No. PB95-265492CEH. Springfield, VA.
3. Goodfellow, S. J. and Brown, W. L. 1978. Fate of Salmonella inoculated into beef for cooking. J. Food Protect. 41:598-685.
4. Snyder, O. P. 1997. Updated guidelines for use of time and temperature specifications for holding and storing food in retail food operations. Hospitality Institute of Technology and Management. St. Paul. (Pending publication, Dairy, Food and Environ. Sanit.)
5. van Netten, P., van de Moosdijk, A., van Hoensel, P., Mossel, D.A.A., and Perales, I. 1990. Psychrotrophic strains of Bacillus cereus producing enterotoxin. J. Appl. Microbiol. 69:73-79


 Table 3. Food Pathogen Control Data Summary

Infective Microorganisms (Inactivated by pasteurization)


 
Microorganisms
Temperature range for growth
F (C)
pH range 
and minimal water activity (aw
for growth
G[ºF(ºC)] = Growth or doubling time
D[ºF(ºC)] = Death rate for 10:1 reduction time
Z = Temperature F (C)
Yersinia enterocolitica
29.3-111 (-1.5-44)(1,3)
4.6-9.0 pH(2)
G[32(0)] = 2 days(4)
G[41(5)] = 17 hours(4)
D[145(62.8)] = 0.24-0.96 min.(1)
Z = 9.2-10.4 (5.1-5.8)(1)
Listeria monocytogenes
29.3-112 (-1.5-44)(1,3,6)
4.5-9.5 pH(6)
0.93 aw(7)
G[32(0)] = 7.5 days(5)
G[40(4.4)] = 1 day(8)
D[140(60)] = 2.85 min.(9)
Z = 10.4-11.3 (5.8-6.3)(10)
Vibrio parahaemolyticus 
41-109.4 (5-43)(11)
4.5-11.0 pH(11)
0.937 aw(12)
D[116(47)[ = 0.8-48 min.(13,14)
Salmonella spp.
41.5-114 (5.5-45.6)(15,16)
4.1-9.0 pH(17)
0.95 aw(12)
D{140(60)] = 1.7 min.(18)
Z = 10 (5.6)(19)
Campylobacter jejuni
90-113 (32.2-45)(20)
4.9-8.0 pH(20)
D[137(58.3)] = 12-21 sec.(21)
Z = 10.6-11.4 (6.0-6.4)(22)

Toxin Producers and/or Spore-formers (Not inactivated by pasteurization)


 
Microorganisms
Temperature range for growth
F (C)
pH range 
and minimal water activity (aw
for growth
G[ºF(ºC)] = Growth or doubling time
D[ºF(ºC)] = Death rate for 10:1 reduction time
Z = Temperature F (C)
Clostridium botulinum
(Type E and other
non-proteolytic strains)
38-113 (3.3- 45)(23)
5.0 - 9.0 pH(23)
0.97 aw(23)
Spores
D[180(82.2)] = 0.49-0.74 min.(24)
Z = 9.9-19.3 (5.6-10.7)(25)
Toxin destruction (any botulinal toxin)
D[185(85)] = 5 min.(26)
Z = 7.2-11.2 (4.0-6.2)(26)
Staphylococcus aureus
43.8-122 (6.5-50)(27)
4.5-9.3 pH(28)
0.83 aw(12)
Vegetative cells
D[140(60)] = 5.2-7.8 min(29)
Z = 9.7-10.4 (5.8-5.4)(29)
Staphylococcus aureus
Toxin production
50-114.8 (10-46)(30)
5.15-90 pH(30)
0.86 aw(30)
Toxin destruction 
D[210(98.9)] = >2 hours(32)
Z = about 50 (27.8)(33)
Bacillus cereus
39.2-122 (4.0-50)(34,35)
4.3-9.0 pH(36)
0.912 aw(36)
Vegetative cells
D[140(60)] = 1 min.(37)
Z = 12.4 (6.9)(37)
Spores
D[212(100)] = 2.7-3.1 min.(36)
Z = 11 (6.1)(36)
Toxin destruction
Diarrheal: D[133(56.1)] = 5 min.(35)
Emetic: Stable at 249.8 (121)](35)
Clostridium botulinum
(Type A and 
proteolytic B strains)
50-118 (10-47.8)(23)
4.6-9.0 pH(23)
0.94 aw(23)
Spores
D[250(121.1)] = 0.2 min.(24)
Z = 18 (10)(24)
Toxin destruction (See above)
Clostridium perfringens
59-126.5 (15-52.3)(38,39)
5.0-9.0 pH(40)
0.95 aw(38)
Vegetative cells
G[105.8(41)] = 7.1 min.(41)
D[138(59)] = 7.2 min.(42)
Z = 6.8°F (3.8)(42)
Spores
D[210(98.9)] = 26-31 min (43)
Z = 13 (7.2)(43)
References for Food Pathogen Control Data Summary
1. Lovett, J., Bradshaw, J.G., and Peeler, J.T. 1982. Thermal inactivation of Yersinia enterocolitica in milk. Appl. Environ. Microbiol. 44:517-519.
2. Stern, N.J., Pierson, M.D., and Kotoula, A.W. 1980. Effects of pH and sodium chloride on Yersinia enterocolitica growth at room temperature and refrigeration temperatures. J. Food Sci. 4564-67.
3. Hudson, J.A., Mott, S.J., and Penney, N. 1994. Growth of Listeria monocytogenes, Aeromonas hydrophila, Yersinia enterocolitica on vacuum and saturated carbon dioxide controlled atmosphere-packaged sliced roast beef. J. Food Protect. 57(3):204-208.
4. Hanna, M.O., Stewart, J.C., Carpenter, Z.I., and Vanderzant, C. 1977a. Effect of heating, freezing, and pH on Yersinia enterolcolitica-like organisms from meat. J. Food Protect. 40:689-692.
5. Grau, F.H., and Vanderline, P.B. 1990. Growth of Listeria monocytogenes on vacuum packaged beef. J. Food Protect. 53(9):452-459.
6. Lovett, J. 1989. Listeria monocytogenes. In Foodborne Bacterial Pathogens. Doyle, M.P., ed. Marcel Dekker, Inc. New York, NY.
7. Farber, J.M., Coates, F. and Daley, E. 1992. Minimum water activity requirements for the growth of Listeria monocytogenes. Letters in App. Microbiol. 15:103-105.
8. Rosenow, E.M., and Marth, E.H. 1987. Growth of Listeria Monocytogenes in skim, whole and chocolate milk, and in whipping cream during incubation at 4ºC, 8ºC, 13ºC, 21ºC, and 35ºC J. Food Protect. 50:452-459.
9. USDA, FSIS. 1990. Recommendations of the National Advisory Committee on Microbiological Criteria for Foods for Refrigeration foods containing cooked, uncured meat or poultry products that are packaged for extended refrigerated shelf life and that are ready-to-eat or prepared with little or no additional heat treatment. USDA, FSIS, Washington, D.C.
10. Bradshaw, J.G., Peeler, J.T., Coorwing, J.J., Hunt, J.M., Tierney, J.T., Larken, E.P., and Twedt, R.M. 1985. Thermal resistance of Listeria monocytogenes in milk. J. Food Protect. 48:743-745.
11. Twedt, R.M. 1989. Vibrio parahaemolyticus. In Foodborne Bacterial Pathogens. Doyle, M.P., ed. Marcel Dekker, Inc. New York, NY.
12. Sperber, W.H. 1983. Influence of water activity on foodborne bacteria - A review. J. Food Protect. 46:142-150.
13. Beuchat, L.R. and Worthington, R.E. 1976. Relationship between heat resistance and phospholipid fatty acid composition of Vibrio parahaemolyticus: Appl. Environ. Microbiol. 31:80-83.
14. Beuchat, L.R. 1982. Vibrio parahaemolyticus: Public health significance. Food Technol. 36(3):80.
15. Matches, J.R. and Liston, J. 1968. Low temperature growth of Salmonella. J. Food Sci. 33:641.
16. Angelotti, R., Foter, M.J., and Lewis, K.H. 1961a. Time-temperature effects on Salmonellae and Staphylococci in Foods. I. Behavior in refrigerated foods. II. Behavior at warm holding temperatures. Am J. Pub. Health 51: 3.
17. Silliker, J.H. 1982. Salmonella foodborne illness. In Microbiological Safety of Foods in Feeding Systems. A.B.M.P.S. Report 125. pp. 22-31.
18. Code of Federal Regulations (CFR) 9. 1987. 318.17 Requirements for the production of cooked beef, roast beef, roast beef, and cooked corned beef. Office of Federal Register National Archives and Records and Administration.
19. Goodfellow, S.J. and Brown, W.L. 1978. Fate of Salmonella inoculated into beef for cooking. J. Food Protect. 41:598-685.
20. Doyle, M.P. and Roman, D.J. 1981. Growth and survival of Campylobacter fetus subsp. jejuni as a function of temperature and pH. J. Food Protect. 44(8):596-601.
21. Koidis, P. and Doyle, M.P. 1983. Survival of Campylobacter jejuni in fresh and heated red meat. J. Food Protect. 46:771-774.
22. Blankenship, L.C., and Craven, S.E. 1982. Survival of Campylobacter jejuni in chicken meats as a function of temperature. Appl. Microbiol. 44:88-92.
23. Hauschild, A.H.W. 1989. Clostridium botulinum. In Foodborne Bacterial Pathogens. Doyle, M.P., ed., Marcel Dekker, Inc. New York, NY.
24. Lynt, R.K., Kautter, D.A. and Solomon, H.M. 1982. Differences and similarities among proteolytic and nonproteolytic strains of Clostridium botulinum Types A.B, E, and F: A review. J. Food Protect. 45(5):466-474.
25. Riemann, H. and Bryan, F.L. 1979 Foodborne Infections and Intoxications. 2nd edition. Academic Press. New York, N.Y. p. 625.
26. Woodburn, M.J., Somers, E., Rodriguez, J., and Shantz, E.J. 1979. Heat inactivation rates of botulism toxins A, B, E and F in some foods and buffers. J. Food Sci. 44:1658-1661.
27. Halpin-Dohnalek, M.I., and Marth, E.H. 1989b. Staphylococcus aureus: Production of extracellular compounds and behavior in foods - A review. J. Food Protect. 52(4):267.
28. Bergdoll, M.D. 1989. Staphylococcus aureus. In Foodborne Bacterial Pathogens. Doyle, M.P. ed. Marcel Dekker. New York, NY. pp. 463-523.
29. Angelotti, R., Foter, M.J., and Lewis, K.H. 1961b. Time-temperature effects on salmonellae and staphylococci in foods. III. Thermal death time studies. Appl. Microbiol. 9:308-315.
30. Tatini, S.R. 1973. Influence of food environments of growth of Staphylococcus aureus and production of various enterotoxins. J. Milk Food Technol. 36:474.
31. Schneusner, D.L., Hood, L.L., and Harmon, L.G. 1973. Effect of temperature and pH on growth and enterotoxin production by Staphylococcus aureus. J. Milk Food Technol. 36:249-252.
32. Read, R.B. and Bradshaw, J.G. 1966. Staphylococcal enterotoxin B thermal inactivation in milk. J. Dairy Science. 49(2):202-203.
33. Denny, C.B. 1971. Effect of toxin concentration on the inactivation of Staphylococcal enterotoxin A in beef bouillion and in phosphate buffer. Appl. Microbiol. 21:1064-1066
34. van Netten, P., van de Moosdijk, A., van Hoensel, P., Mossel, D.A.A., and Perales, I. 1990. Psychrotrophic strains of Bacillus cereus producing enterotoxin. J. Appl. Microbiol. 69:73-79.
35. Johnson, K. M., Nelson, C.L., and Busta, F.F. 1983. Influence of temperature on germination and growth of spores of emetic and diarrheal strains of Bacillus cereus in a growth medium and in rice. J. Food Sci. 48:286.
36. Kramer, J.M., and Gilbert, R.J. 1989. Bacillus cereus and other Bacillus species. In Foodborne Bacterial Pathogens. Doyle, M.P., ed. Marcel Dekker, Inc. New York, NY.
37. Johnson, K. M. 1986. Personal communication.
38. Labbe, R. 1989. Clostridium perfringens. In Foodborne Bacterial Pathogens. Doyle, M.P., ed. Marcel Dekker, Inc. New York, NY.
39. Shoemaker, S.P. and Pierson, M.D. 1976. "Phoenix Phenomenon" in the growth of Clostridium perfringens. Appl. Microbiol. 32(6):803-807.
40. Fuchs, A and Bonde, G.J. 1957. The nutritional requirements of Clostridium perfringens. J. Gen. Microbiol. 34:280-284.
41. Willardsen, R.R., Busta, F.F. Allen, C.E., and Smith, L.B. 1977. Growth and survival of Clostridium perfringens during constantly rising temperatures. J. Food Sci. 43:470.
42. Roy, R.J., Busta, F.F., and Thompson, D.R. 1981. Thermal inactivation Clostridium perfringens after growth at several constant and linearly rising temperatures. J. Food Sci. 46:1586-1591.
43. Bradshaw, J.G., Peeler, J.T., and Twedt, R.M. 1977. Thermal inactivation of ileal loop-reactive Clostridium perfringens type A strains in phosphate buffer and beef gravy. Appl. Environ. Microbiol. 34:280-284.
 

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