Bruce Tompkin Ph.D.

Armour Swift-Eckrich

Table 1. Minimum growth temperatures for selected foodborne pathogens.

Minimum Growth
Temperatures
Salmonellae1 7C 44.6F
Pathogenic E. coli 7-8C 44.6-46.4F
L. monocytogenes -0.4C 31.3F
Y. enterocolitica -1.3C 29.7F
Campylobacter jejuni 32C 89.6F
Staphylococcus aureus 7C 44.6F
Bacillus cereus2
psychrotrophic strains 4C 39.2F
Clostridium perfringens 12C 53.6F
Clostridium botulinum
nonproteolytic 3.3C 38F
proteolytic 10C 50F

• 1One report of initial growth on bacon at 5C but then the population decreased.

• 2While growth of B. cereus occurs in milk at refrigeration temperatures (e.g., <7C), there is no
evidence for this in meat and poultry. One study reported death of vegetative cells in ground beef
at 12.5C (54.5F) and below.

• Parasites (e.g., Trichinella spiralis, Taenia spp., Toxoplasma gondii) and viruses do not
multiply in meat or poultry products.

Source: International Commission on Microbiological Specifications for Foods. 1996.

Microorganisms in Foods: Microbiological Specifications of Food Pathogens. Blackie
Academic & Professional, New York.

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 Bruce Tompkin Ph.D.
Armour Swift-Eckrich

Table 2. Estimated time (hours) for a ten fold increase at 50, 60 and 70F.

Estimated Time (hours) to increase from 10 to 100 CFU/ml

50F (10C) 60F (15.6C) 70F (21.1C)
Salmonellae 107 24 9

E. coli O157:H7
aerobic 50 21 9
anaerobic 123 38 16

L. monocytogenes
aerobic 38 16 8
anaerobic 58 27 16

Y. enterocolitica 68 31 16

Source: USDA ARS Pathogen Modeling Program Version 4.0.

Conditions: broth medium, pH 6.0, salt 0.5%, sodium nitrite 0.0%

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 Bruce Tompkin Ph.D.
Armour Swift-Eckrich

Table 3. Public health significance of meat and/or poultry held at 40-50F (4.4 to 10C) during
storage and/or distribution.

Pathogen1 Estimated No. of Estimated Foods most Impact of 40-50F on

cases of illness cost/year likely to be growth of the pathogen5
from (billion)3 involved4
meat/poultry2

T. gondii 2,056 2.7 raw pork None.

This parasite can not
multiply in meat or
poultry products.

Campylobacter 1,031,000- 0.5 - 0.8 poultry None.

1,313,000 C. jejuni/coli can not
multiply below about
90F.

S. aureus 756,000 0.6 cooked None.

meat/poultry S. aureus is a poor
competitor and would
not grow in raw meat or
poultry at 50F or below.
Most outbreaks involve
cooked products that
become contaminated
and are held at 75-100F
in the presence of air.

L. monocytogenes 808-837 0.1-0.2 ready-to-eat Little, if any.

foods Listeriosis has not been
linked to raw meat or
poultry . The potential
for growth in some
ready-to-eat foods does
exist.

C. perfringens 50,000 0.1 cooked None.

products C. perfringens can not
grow below about 54F

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 Bruce Tompkin Ph.D.
Armour Swift-Eckrich

E. coli O157:H7 6,000 - 12,000 0.1-0.2 undercooked Little, if any.

ground beef The minimum
temperature for growth is
about 45F. At 50F, from
2 to 5 days would be
needed for a 10 fold (1
log) increase depending
on available oxygen

Salmonellae 549,000- 0.3-2.6 undercooked Little, if any.

2,745,000 meat/poultry The minimum
temperature for growth is
about 45F. At 50F, about
4 days may be needed for
a 10 fold (1 log) increase.

Source: 1,2,3 Department of Agriculture, FSIS, Proposed Rule. 1995. Federal Register 60:
6881-6881. (This source was used for "the pathogens," "estimated cases", and
"estimated cost/year")

4,5 The "foods most likely to be involved" and the "impact of 40-50F" are based upon
the scientific literature.

Notes: • The Federal Register notice listed 50-75% of salmonellosis cases as being due to
meat/poultry. The 75% value was used for the above estimate of cases.

• Recent estimates from the Center for Disease Control indicates the total number of
cases of listeriosis is about 1100/year. Thus the number of cases from meat/poultry
(50% of the total) now would be estimated at about 550/year.

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 Bruce Tompkin Ph.D.
Armour Swift-Eckrich

Table 4. Estimated time (hours) for a one log increase of typical spoilage bacteria at 40, 50 and
57-59F. Applicable to raw meat and poultry.

Estimated time (hours) to increase from

10 to 100 CFU/ml
Isolate and strain # 39.2-41F (4-5C) 50F (10C) 57-59F (14-15C)
Pseudomonas (92) 39 18 8
Pseudomonas (69) 49 22 9
Ps. fluorescens 27 12 7
Ps. fluorescens (P-200) - 13 7
Ps. fluorescens 22 - -
Ps. fragi 17 9 -
Pseudomonas (21-3c) 24 11 7
Pseudomonas (1-3b) 23 9 8
Enterobacter aerogenes (Ps48) 40 14 7
Gram negative rod
aerobic 14 - -
anaerobic 32 - -
Gram negative rod 251 - -
Achromobacter (7) 18 8 5
Achromobacter (438) 20 8 4
Achromobacter (5) 24 10 5
Pseudomonas (451) 32 13 4

1 Data obtained at 6C.

Source: Adapted from Tompkin. 1973. Food Technol. 27(12):54-58.

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 Bruce Tompkin Ph.D.
Armour Swift-Eckrich

Table 5. Effect of temperature on time of spoilage for pork and poultry.

Temperature (F) Days to spoilage

A. Chicken 32 18
37 11
42 8
47 6
68 2

B. Pork 31 14
36 9
41 5

Source: A. Adapted from Shannon and Stadelman. 1957. J. Poult. Sci. 36:121-123.
B. Unpublished data from Swift and Company (before 1977).

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 Bruce Tompkin Ph.D.
Armour Swift-Eckrich

Table 6. Combined effect of temperature and bacterial content on time of spoilage of poultry and
beef.

Days to spoilage
Temperature (F) Initial level of Initial level of
100 CFU/cm² 100,000 CFU/cm²
A. Chicken 40 14 1-2
50 6 1-2

B. Beef 32 22 11
41 13 6
50 8 4
68 3 2

Source: A. Adapted from Ogilvy and Ayres. 1951. Food Technol. 5:97-102.
B. Adapted from Ayres. 1960. Food res. 25:1-18.

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 Bruce Tompkin Ph.D.
Armour Swift-Eckrich

Table 7. Factors influencing the microbial content of ready-to-eat meat and poultry products from
production through distribution/storage.

Factor Measurement (s)

Ingredients Types and levels of microorganisms in ingredients which can

multiply and/or survive during subsequent processing, distribution
and storage.

Formulating The conditions of formulating and holding that may lead to

microorganisms in finished product

Heating The conditions of heating (e.g., time, temperature, humidity).

Cooling The conditions of cooling and potential for recontamination.

Further processing The conditions of holding and further processing before packaging

Product composition Brine content / water activity

Type and amount of fermentable carbohydrate
Product pH; type and level of acidulant
Level of smoke, liquid or natural
Phosphate content
Level of residual nitrite
Hot oil dipping or flaming to brown the surface
Spices, condiments applied to the surface after heating
Sodium lactate content
Metal ion content

Packaging Product temperature during packaging and palletizing

Degree of vacuumization and leaker formation
Rate of oxygen transmission through packaging materials
Addition of oxygen scavengers
Modified atmosphere content

Contamination after heating Types and levels of microorganisms contaminating the product
between heating and packaging.

Distribution/storage Time-temperature history after packaging.

Damage to packaging permitting contamination

Source: Adapted from Tompkin, 1995. The use of HACCP for producing and distributing
processed meat and poultry products. pp. 72-108. In A.M. Pearson and T.R. Dutson
(eds.), HACCP in Meat, Poultry and Fish Processing. Blackie Academic &
Professional, New York.

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 Bruce Tompkin Ph.D.
Armour Swift-Eckrich

Options for arriving at time, temperature criteria for chilling, storage and distribution of meat and
poultry.

I. Chilling Rate
A. Carcasses, head meat, variety meats
1. Specify time and temperature requirements based upon:
a. predictive modeling and published research
b. data submitted by industry through conferences such as this and other means
c. survey of current commercial practice for rates of chilling carcasses
d. microbial sampling of carcasses before and after chilling
e. review requirements from other countries

2. Arbitrarily establish a performance standard

a. for example, <2 log increase in salmonellae and E. coli O157:H7

3. Conduct a risk assessment (This is highly recommended)

B. Cooked meat and poultry products

1. Provide time and temperature guidance such as in the current guideline (FSIS
Directive 7110.3 Rev. 1; 1-24-89)

2. Establish a performance standard

a. for example, <1.5 log increase in C. perfringens

II. Distribution/Storage
A. All perishable meat and poultry that requires refrigeration for food safety
1. a. Establish an action level in the range of 40 to 50F because a critical limit
based solely upon temperature does not exist in this range. A valid critical
limit would have to specify time and temperature.
b. A temperature of 45 or 46F (7 or 8C) is suggested.

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 Bruce Tompkin Ph.D.
Armour Swift-Eckrich

2. Establish performance standards

a. for example, <1.5 log increase in C. perfringens
b. for example, <1.5 log increase in salmonellae and E. coli O157:H7

III. If the action level or other crieria are exceeded:

A. place product on hold
B. collect information (e.g., time-temperature history)
C. review information
D. collect more information, if needed (e.g., sample and test)
E. consider the food, its intended use and consumers of the product
F. decide disposition:
options; destroy, reprocess, freeze, divert to other safe use etc.
G. implement decision
H. follow through with corrective action to prevent future occurrences

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