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Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 1

Hazard Analysis and Risk-Based 

Preventive Controls for Human Food: 

Draft Guidance for Industry1

This draft guidance, when finalized, will represent the current thinking of the Food and Drug 

Administration (FDA or we) on this topic. It does not establish any rights for any person and is 

not binding on FDA or the public. You can use an alternative approach if it satisfies the 

requirements of the applicable statutes and regulations. To discuss an alternative approach, 

contact FDA’s Technical Assistance Network by submitting your question

at https://www.fda.gov/Food/GuidanceRegulation/FSMA/ucm459719.htm.

Appendix 3: Bacterial Pathogen Growth and Inactivation

This appendix contains information on the growth and inactivation of bacterial pathogens. The 

tables in this appendix derive from our guidance entitled “Fish and Fishery Products Hazards 

and Controls Guidance.” In these tables, and our discussion of these tables, we use the 

technical terms “D-value” and “z-value,” which we briefly describe immediately below. For 

additional information about what these terms mean and how you can use the information in 

these tables to determine appropriate processing conditions for your product, you should 

consult standard food processing books and technical information.

• D-value: The relationship between the duration of a thermal treatment and the percentage of 

microorganisms surviving the treatment is generally logarithmic, and the results of such studies are 

usually presented in a plot that represents the log of the percent of surviving vegetative cells or 

spores versus time at a given temperature. The time required to destroy 90 percent of the vegetative 

cells or spores at a given temperature is called the decimal reduction time, usually referred to as the 

“D-value” (Larousse and Brown, 1997). The D-value usually varies inversely with temperature.

• z-value: In general, the slope of a plot of the log of the D-value versus temperature is approximately 

linear. A “z-value” is derived from the reciprocal of the slope of the best straight line and is equal to 

the increase in the number of degrees (from a given starting temperature) that results in a 90 percent 

reduction in the D-value (Larousse and Brown, 1997). The D-value and z-value for the vegetative 

cells or spores of a microbial strain at a specified temperature characterize its thermal resistance at 

that temperature. Therefore, D-values and z-values provide a means to compare the thermal 

resistance of different microorganisms, or different strains of the same microorganism, at one or more 

temperatures. 

Table 3-A contains information on the minimum water activity (aw), minimum and maximum pH, 

and minimum and maximum temperatures that limit growth for the bacterial pathogens that are 

of greatest concern in food processing. Table 3-A also provides data on the maximum water 

 1 This guidance has been prepared by the Office of Food Safety in the Center for Food Safety and 

Applied Nutrition at the U.S. Food and Drug Administration. Underlined text in yellow highlights 

represents a correction from the draft Appendix 3 that we issued for public comment in August 2016.
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Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 2

phase salt that limits growth and the oxygen requirements for the pathogens listed. The data 

shown in Table 3-A are the extreme limits reported among the references cited. These values 

may not apply to your food or processing conditions.

Table 3-B contains information on maximum cumulative exposure time at internal product 

temperature ranges for exposure of foods that, under ordinary circumstances, will be safe for 

the bacterial pathogens that are of greatest concern in food processing. These maximum, 

cumulative exposure times are derived from published scientific information. 

Table 3-C is a Quick Reference Guide based on Table 3-B.

Because the nature of bacterial growth is logarithmic, linear interpolation using the time and 

temperature guidance may not be appropriate. Furthermore, the food matrix affects bacterial 

growth (e.g., presence of competing microorganisms, available nutrients, growth-restrictive 

agents). You should consider such attributes when using the information in Tables 3-A, 3-B, 

and 3-C.

Table 3-D contains information on the destruction of Listeria monocytogenes (L. 

monocytogenes). Lethal rate, as used in Table 3-D, is the relative lethality of 1 minute at the 

designated internal product temperature as compared with the lethality of 1 minute at the 

reference internal product temperature of 158°F (70°C) (using a z = 13.5°F (7.5°C)). For 

example, 1 minute at 145°F (63°C) is 0.117 times as lethal as 1 minute at 158°F (70°C). The 

times provided are the length of time at the designated internal product temperature necessary 

to deliver a “6D” process for L. monocytogenes (i.e., a process that will accomplish a 6 

logarithm (factor of 1,000,000) reduction in the number of L. monocytogenes). 

The length of time at a particular internal product temperature needed to accomplish a 6D 

reduction in the number of L. monocytogenes depends, in part, upon the food that is being 

heated. The values in the table are generally conservative and apply to all foods. You may be 

able to establish a shorter process time for your food by conducting scientific thermal death time 

studies. Additionally, lower degrees of destruction may be acceptable in your food if supported 

by a scientific study of the normal initial levels in the food. It is also possible that higher levels of 

destruction may be necessary in some foods, if you anticipate relatively high initial levels in the 

food you are processing.

Table 3-E contains information on the destruction of Clostridium botulinum (C. botulinum) type 

B (the most heat- resistant form of non-proteolytic C. botulinum). (The non-proteolytic strains of 

C. botulinum can grow at refrigeration temperatures and may be a hazard requiring a preventive 

control in some foods intended to be held refrigerated for extended periods of time.) Lethal rate, 

as used in this table, is the relative lethality of 1 minute at the designated internal product 

temperature as compared with the lethality of 1 minute at the reference product internal 

temperature of 194°F (90°C) (for temperatures less than 194°F (90°C), z = 12.6°F (7.0°C); for 

temperatures above 194°F (90°C), z = 18°F (10°C)). The times provided are the length of time

at the designated internal product temperature necessary to deliver a 6D process for C. 

botulinum. The values in the table are generally conservative. You may be able to establish a 

shorter process time for your food by conducting scientific thermal death time studies. 
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Table 3-A Limiting Conditions for Pathogen Growth

Pathogen

Min. aw

(using 

salt)

Min. 

pH

Max. 

pH

Max. % 

Water 

Phase 

Salt

Min. 

Temp.

Max. 

Temp.

Oxygen 

Requirement

Bacillus 

cereus

0.92 4.3 9.3 10 39.2°F 

4°C

131°F1

55°C

facultative 

anaerobe4

Campylobacter jejuni 0.987 4.9 9.5 1.7 86°F

30°C

113°F

45°C

microaerophile2

Clostridium 

botulinum, 

type A, and 

proteolytic 

types B and 

F

0.935 4.6 9 10 50°F 

10°C

118.4°F 

48°C anaerobe3

Clostridium 

botulinum, 

type E, and 

nonproteolytic 

types B and 

F

0.97 5 9 5 37.9°F 

3.3°C

113°F 

45°C anaerobe3

Clostridium 

perfringens 0.93 5 9 7 50°F 10°C

125.6°F 

52°C anaerobe3

Pathogenic 

strains of 

Escherichia 

coli

0.95 4 10 6.5 43.7°F 

6.5°C

120.9°F 

49.4°C

facultative 

anaerobe4

Listeria 

monocytogenes0.92 4.4 9.4 10 31.3°F 

-0.4°C

113°F 

45°C

facultative 

anaerobe4

Salmonella

spp. 0.94 3.7 9.5 8 41.4°F5.2°C

115.2°F 

46.2°C

facultative 

anaerobe4

Shigella spp. 0.96 4.8 9.3 5.2 43°F 

6.1°C

116.8°F

47.1°C

facultative 

anaerobe4

Staphylococcus 

aureus 

growth

0.83 4 10 20 44.6°F 

7°C

122°F 

50°C

facultative 

anaerobe4
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Pathogen

Min. aw

(using 

salt)

Min. 

pH

Max. 

pH

Max. % 

Water 

Phase 

Salt

Min. 

Temp.

Max. 

Temp.

Oxygen 

Requirement

Staphylococcus 

aureus toxin 

formation

0.85 4 9.8 10 50°F 

10°C

118°F 

48°C

facultative 

anaerobe4

Vibrio 

cholerae 0.97 5 10 6 50°F 10°C

109.4°F

43°C

facultative 

anaerobe4

Vibrio 

parahaemolyticus0.94 4.8 11 10 41°F 

5°C

113.5°F 

45.3°C

facultative 

anaerobe4

Vibrio 

vulnificus 0.96 5 10 5 46.4°F 8°C

109.4°F 

43°C

facultative 

anaerobe4

Yersinia 

enterocolitica0.945 4.2 10 7 29.7°F 

-1.3°C

107.6°F 

42°C

facultative 

anaerobe4

1

Has significantly delayed growth (>24 hours) at 131°F (55°C).

2

Requires limited levels of oxygen.

3

Requires the absence of oxygen.

4

Grows either with or without oxygen.
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Table 3-B. Time and Temperature Guidance for Controlling Pathogen Growth and Toxin 

Formation in Food Products

Potentially Hazardous Condition Product Temperature Maximum Cumulative 

Exposure Time

Growth and toxin formation by 

Bacillus cereus

39.2-43°F (4-6°C)

44-59°F (7-15°C)

60-70°F (16-21°C)

Above 70°F (21°C)

5 days

1 day

6 hours

3 hours

Growth of Campylobacter jejuni 86-93°F (30-34°C)

Above 93°F (34°C)

48 hours

12 hours

Germination, growth, and toxin 

formation by Clostridium 

botulinum type A, and proteolytic 

types B and F

50-70°F (10-21°C)

Above 70°F (21°C)

11 hours

2 hours

Germination, growth, and toxin 

formation by Clostridium 

botulinum type E, and nonproteolytic types B and F

37.9-41°F (3.3-5°C) 

42-50°F (6-10°C)

51-70°F (11-21°C)

Above 70°F (21°C)

7 days 

2 days

11 hours

6 hours

Growth of Clostridium 

perfringens

50-54°F (10-12°C) 

55-57°F (13-14 °C)

58-70°F (15-21°C)

Above 70°F (21°C)

21 days

1 day

6 hours1

2 hours

Growth of pathogenic strains of 

Escherichia coli

43.7-50°F (6.6-10°C)

51-70°F (11-21°C)

Above 70°F (21°C)

2 days 

5 hours

2 hours

Growth of Listeria 

monocytogenes

31.3-41°F (-0.4-5°C)

42-50°F (6-10°C)

51-70°F (11-21°C)

71-86°F (22-30°C)

Above 86°F (30°C)

7 days

1 day

7 hours

3 hours

1 hour

Growth of Salmonella species 41.4-50°F (5.2-10°C)

51-70°F (11-21°C)

Above 70°F (21°C)

2 days

5 hours

2 hours 

Growth of Shigella species 43-50°F (6.1-10°C)

51-70°F (11-21°C)

Above 70°F (21°C)

2 days

5 hours

2 hours

Growth and toxin formation by 

Staphylococcus aureus

50°F (7-10°C)

51-70°F (11-21°C)

Above 70°F (21°C)

14 days

12 hours1

3 hours
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Potentially Hazardous Condition Product Temperature Maximum Cumulative 

Exposure Time

Growth of Vibrio cholerae 50°F (10°C) 

51-70°F (11-21°C)

71-80°F (22-27°C) 

Above 80oF (27oC)

21 days

6 hours

2 hours

1 hour2

Growth of Vibrio 

parahaemolyticus

41-50°F (5-10°C)

51-70°F (11-21°C)

71-80°F (22-27°C) 

Above 80oF (27oC)

21 days 

6 hours

2 hours

1 hour2

Growth of Vibrio vulnificus 46.4-50°F (8-10°C) 

51-70°F (11-21°C)

71-80°F (22-27°C) 

Above 80oF (27oC)

21 days

6 hours

2 hours

1 hour2

Growth of Yersinia enterocolitica 29.7-50°F (-1.3-10°C)

51-70°F (11-21°C)

Above 70°F (21°C)

1 day

6 hours

2.5 hours

1 Additional data needed.

2

Applies to cooked, ready-to-eat foods only.

Table 3-C is a Quick Reference Guide derived from Table 3-B:

Table 3-C Quick Reference Guide for Time and Temperature Guidance for Controlling 

Pathogen Growth and Toxin Formation in Food Products (for Internal Temperatures 

above 50°F (10°C) but below 135oF (57.2oC))

If the food is a ... And the food is 

held at an internal 

temperature ...

Then you should 

limit the 

exposure time to 

...

Or, if 

Staphylococcus 

aureus (S. aureus) 

is the only 

pathogen of 

concern, then you 

should limit the 

exposure time to ...

As long as ...

Raw, RTE 

ingredient or food 

product 

Above 70°F 

(21.1°C)

2 hours 3 hours N/A

Raw, RTE 

ingredient or food 

product 

Above 70°F 

(21.1°C)

4 hours N/A No more than 2 

of those hours 

are between 70°F 

(21.1°C) and 

135oF (57.2oC)

Raw, RTE 

ingredient or food 

product

At any time above 

50°F (10°C) but 

never above 70°F 

(21.1°C)

5 hours 12 hours N/A
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If the food is a ... And the food is 

held at an internal 

temperature ...

Then you should 

limit the 

exposure time to 

...

Or, if 

Staphylococcus 

aureus (S. aureus) 

is the only 

pathogen of 

concern, then you 

should limit the 

exposure time to ...

As long as ...

Raw, RTE 

ingredient or food 

product

At internal 

temperatures (or at 

ambient air 

temperatures)

below 50°F (10°C) 

throughout 

processing

N/A N/A N/A

Cooked, RTE 

ingredient or food 

product

At any time above 

80°F (26.7°C)

1 hour 3 hours N/A

Cooked, RTE 

ingredient or food 

product

At any time above 

80°F (26.7°C)

4 hours N/A No more than 1 

of those hours is 

above 70°F 

(21.1°C)

Cooked, RTE 

ingredient or food 

product

At any time above 

70°F (21.1°C) but 

never above 80°F 

(26.7°C)

2 hours 3 hours N/A

Cooked, RTE 

ingredient or food 

product

Never held above 

80°F (26.7°C)

4 hours N/A No more than 2 

of those hours 

are above 70°F 

(21.1°C)

Cooked, RTE 

ingredient or food 

product

At any time above 

50°F (10°C) but 

never above 70°F 

(21.1°C)

5 hours 12 hours N/A

Cooked, RTE 

ingredient or food 

product

At internal 

temperatures (or 

ambient air 

temperatures) 

below 50°F (10°C) 

throughout 

processing

N/A N/A N/A

Note that the preceding recommended critical limits do not address internal product 

temperatures between 40°F (4.4°C), which is the recommended maximum storage temperature 

for refrigerated food products, and 50°F (10°C). That is because growth of foodborne 

pathogenic bacteria is very slow at these temperatures and the time necessary for significant 

growth is longer than would be reasonably likely to occur in most food processing steps. 

However, if you have processing steps that occur at these temperatures that approach the 

maximum cumulative exposure times listed in Table 3-B for the pathogenic bacteria of concern 

in your product, you should consider development of a critical limit for control at these 

temperatures. 
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It is not possible to furnish recommendations for each pathogenic bacterium, process, type of 

food product, and temperature or combination of temperatures. Programmable models to 

predict growth rates for certain pathogens associated with various foods under differing 

conditions have been developed by the U.S. Department of Agriculture’ (the Pathogen Modeling 

Program (PMP)) and by an international consortium of the Institute of Food Research (UK), the 

USDA Agricultural Research Service (USDA-ARS) and the University of Tasmania Food Safety 

Centre (CombBase database and Predictor). These programs can provide growth curves for 

selected pathogens. To use these models, you indicate the conditions, such as pH, 

temperature, and salt concentration that you are interested in and the models provide pathogen 

growth predictions (e.g., growth curve, time of doubling, time of lag phase, and generation time). 

FDA does not endorse or require the use of such modeling programs, but recognizes that the 

predictive growth information they provide may be helpful to some processors. However, you 

should be aware that significant deviations between actual microbiological data in specific 

products and the predictions may occur, including those for the lag phase of growth. Therefore, 

you should validate the time and temperature limits derived from such predictive models if 

growth of pathogens during processing requires a preventive control. 
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Table 3-D Inactivation of Listeria monocytogenes

Internal Product 

Temperature (°F)

Internal Product 

Temperature (°C)

Lethal 

Rate

Time for 6D Process 

(minutes)

145 63 0.117 17.0

147 64 0.158 12.7

149 65 0.215 9.3

151 66 0.293 6.8

153 67 0.398 5.0

154 68 0.541 3.7

156 69 0.736 2.7

158 70 1.000 2.0

160 71 1.359 1.5

162 72 1.848 1.0

163 73 2.512 0.8

165 74 3.415 0.6

167 75 4.642 0.4

169 76 6.310 0.3

171 77 8.577 0.2

172 78 11.659 0.2

174 79 15.849 0.1

176 80 21.544 0.09

178 81 29.286 0.07

180 82 39.810 0.05

182 83 54.116 0.03

183 84 73.564 0.03

185 85 100.000 0.02

Note: z = 13.5°F (7.5°C). 
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Table 3-E Inactivation of Non-Proteolytic Clostridium botulinum Type B

Internal Product 

Temperature (°F)

Internal Product 

Temperature (°C)

Lethal 

Rate*

Time for 6D Process 

(minutes)

185 85 0.193 51.8

187 86 0.270 37.0

189 87 0.370 27.0

190 88 0.520 19.2

192 89 0.720 13.9

194 90 1.000 10.0

196 91 1.260 7.9

198 92 1.600 6.3

199 93 2.000 5.0

201 94 2.510 4.0

203 95 3.160 3.2

205 96 3.980 2.5

207 97 5.010 2.0

208 98 6.310 1.6

210 99 7.940 1.3

212 100 10.000 1.0

Note: For temperatures less than 194°F (90°C), z = 12.6°F (7.0°C); for temperatures above 

194°F (90°C), z = 18°F (10°C).
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References

Abrahamsson, K., B. Gullmar, and N. Molin. 1966. "The effect of temperature on toxin formation 

and toxin stability of Clostridium botulinum type E in different environments." Can J 

Microbiol 12 (2):385-94.

Adams, M. R., C. L. Little, and M. C. Easter. 1991. "Modelling the effect of pH, acidulant and 

temperature on the growth rate of Yersinia enterocolitica." J Appl Bacteriol 71 (1):65-71.

Adesiyun, A. A. 1984. "Enterotoxigenicity of Staphylococcus aureus strains isolated from 

Nigerian ready-to-eat foods." Journal of Food Protection 47 (6):438-440.

Ajmal, M. 1968. "Growth and toxin production of Clostridium botulinum type E." J Appl Bacteriol

31 (1):120-3.

Ando, Y. 1971. "The germination requirements of spores of Clostridium botulinum type E." 

Japan J Microbiol 15 (6):515-25.

Ando, Y., and H. Iida. 1970. "Factors affecting the germination of spores of Clostridium 

botulinum type E." Jpn J Microbiol 14 (5):361-70.

Augustin, J. C., L. Rosso, and V. Carlier. 2000. "A model describing the effect of temperature 

history on lag time for Listeria monocytogenes." Int J Food Microbiol 57 (3):169-81.

Augustin, J. C., V. Zuliani, M. Cornu, and L. Guillier. 2005. "Growth rate and growth probability 

of Listeria monocytogenes in dairy, meat and seafood products in suboptimal 

conditions." J Appl Microbiol 99 (5):1019-42. doi: 10.1111/j.1365-2672.2005.02710.x.

Baird-Parker, A. C. 1971. "Symposium on microbial changes in foods: Factors affecting the 

production of bacterial food poisoning toxins." J Appl Bacteriol 34 (1):181-97.

Baird-Parker, A. C., and B. Freame. 1967. "Combined effect of water activity, pH and 

temperature on the growth of Clostridium botulinum from spore and vegetative cell 

inocula." J Appl Bacteriol 30 (3):420-9.

Baynes, N. C., J. Comrie, and J. H. Prain. 1983. "Detection of bacterial growth by the Malthus 

conductance meter." Med Lab Sci 40 (2):149-58.

Ben Embarek, P. K. 1994. "Presence, detection and growth of Listeria monocytogenes in 

seafoods: A review." Int J Food Microbiol 23 (1):17-34.

Ben Embarek, P. K., and H. H. Huss. 1993. "Heat resistance of Listeria monocytogenes in 

vacuum packaged pasteurized fish fillets." Int J Food Microbiol 20 (2):85-95.

Benedict, R. C., T. Partridge, D. Wells, and R. L. Buchanan. 1993. "Bacillus cereus: aerobic 

growth-kinetics." Journal of Food Protection 56 (3):211-214.
Contains Non-binding Recommendations

Draft-Not for Implementation

Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 12

Bergdoll, M. S. 1989. “Staphylococcus aureus.” In Foodborne Microbial Pathogens. Edited by 

Doyle, M. P., New York, NY: Marcel Dekker, Inc.

Beuchat, L. R., M. R. Clavero, and C. B. Jaquette. 1997. "Effects of nisin and temperature on 

survival, growth, and enterotoxin production characteristics of psychrotrophic Bacillus 

cereus in beef gravy." Appl Environ Microbiol 63 (5):1953-8.

Boyd, J. W., and B. A. Southcot. 1971. "Effects of sodium chloride on outgrowth and toxin 

production of Clostridium botulinum type E in cod homogenates." J Fish Res Board Can 

28 (8):1071-1075.

Brocklehurst, T. F., and B. M. Lund. 1990. "The influence of pH, temperature and organic-acids 

on the initiation of growth of Yersinia enterocolitica." J Appl Bacteriol 69 (3):390-397. 

doi: 10.1111/j.1365-2672.1990.tb01529.x.

Bryan, F. L. 1979. "Staphylococcus aureus." In Food Microbiology: Public Health and Spoilage 

Aspects. Westport, CT: The AVI Publishing Co.

Buchanan, R. L. 1991. "Using spreadsheet software for predictive microbiology applications." 

Journal of Food Safety 11 (2):123-134.

Buchanan, R. L. 1993. "Predictive food microbiology." Trends Food Sci Tech 4 (1):6-11. doi: 

10.1016/S0924-2244(05)80004-4.

Buchanan, R. L., and L. K. Bagi. 1997. "Effect of water activity and humectant identity on the 

growth kinetics of Escherichia coli O157:H7." Food Microbiol 14 (5):413-423. doi: 

10.1006/fmic.1997.0101.

Buchanan, R. L., and M. L. Cygnarowicz. 1990. "A mathematical approach toward defining and 

calculating the duration of the lag phase." Food Microbiol 7 (3):237-240. doi: 

10.1016/0740-0020(90)90029-H.

Buchanan, R. L., and L. A. Klawitter. 1992. "The effect of incubation-temperature, initial pH, and 

sodium-chloride on the growth-kinetics of Escherichia coli O157:H7." Food Microbiol 9 

(3):185-196. doi: 10.1016/0740-0020(92)80046-7.

Buchanan, R. L., and J. G. Phillips. 1990. "Response-surface model for predicting the effects of 

temperature pH, sodium-chloride content, sodium-nitrite concentration and atmosphere 

on the growth of Listeria monocytogenes." Journal of Food Protection 53 (5):370-376, 

381.

Campanini, M., A. Casolari, and S. Gola. 1977. "Bacterial-growth and pH limiting value." Ind 

Conserve 52 (4):326-331.

Carlin, F., C. Nguyen-the, and A. Abreu da Silva. 1995. "Factors affecting the growth of Listeria 

monocytogenes on minimally processed fresh endive." J Appl Bacteriol 78 (6):636-46.

Carlson, V. L., and G. H. Snoeyenbos. 1972. "Relationship of population kinetics of Salmonella 

typhimurium and cultural methodology." Am J Vet Res 33 (1):177-84.
Contains Non-binding Recommendations

Draft-Not for Implementation

Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 13

Catsaras, M., and D. Grebot. 1984. "Multiplication des Salmonella dans la viande hachee." Bull. 

Acad. Vet. France. 57:501-512.

Cole, M. B., M. V. Jones, and C. Holyoak. 1990. "The effect of pH, salt concentration and 

temperature on the survival and growth of Listeria monocytogenes." J Appl Bacteriol 69 

(1):63-72.

Colwell, R. R. 1984. Vibrios in the environment. New York, NY: John Wiley Interscience.

Conner, D. E., V. N. Scott, and D. T. Bernard. 1990. "Potential Clostridium botulinum hazards 

associated with extended shelf-life refrigerated foods: a review." Journal of Food Safety

10 (2):131-153.

Cortesi, M. L., T. Sarli, A. Santoro, N. Murru, and T. Pepe. 1997. "Distribution and behavior of 

Listeria monocytogenes in three lots of naturally-contaminated vacuum-packed smoked 

salmon stored at 2 and 10 degrees C." International Journal of Food Microbiology 37 (2-

3):209-214. doi: 10.1016/S0168-1605(97)00064-0.

Craven, S. E. 1980. "Growth and sporulation of Clostridium perfringens in foods." Food Technol 

Chicago 34 (4):80-&.

Curtis, L. M., M. Patrick, and C. D. Blackburn. 1995. "Survival of Campylobacter jejuni in foods 

and comparison with a predictive model." Lett Appl Microbiol 21 (3):194-7.

Dahl Sawyer, C. A., and J. J. Pestka. 1985. "Foodservice systems: Presence of injured bacteria 

in foods during food product flow." Annu Rev Microbiol 39:51-67. doi: 

10.1146/annurev.mi.39.100185.000411.

Dalgaard, P., and L. V. Jorgensen. 1998. "Predicted and observed growth of Listeria 

monocytogenes in seafood challenge tests and in naturally contaminated cold-smoked 

salmon." Int J Food Microbiol 40 (1-2):105-15.

Datz, M., C. Janetzki-Mittmann, S. Franke, F. Gunzer, H. Schmidt, and H. Karch. 1996. 

"Analysis of the enterohemorrhagic Escherichia coli O157 DNA region containing 

lambdoid phage gene p and shiga-like toxin structural genes." Applied and 

Environmental Microbiology 62 (3):791-797.

Deibel, K. E. 1995. Potential of Staphylococcus aureus to produce enterotoxin in fish batter at 

various temperatures. Proceedings of the IFT Annual Meeting. Minneapolis, MN: 

Medallion Lab.

Dengremont, E., and J. M. Membre. 1995. "Statistical approach for comparison of the growth 

rates of five strains of Staphylococcus aureus." Appl Environ Microbiol 61 (12):4389-95.

Dickerson, R. W., and M. R. Berry. 1976. "Heating curves during commercial cooking of blue 

crab." J Milk Food Technol 39 (4):258-262.

Dickerson, R. W., and R. B. Read. 1973. "Cooling rates of foods." J Milk Food Technol 36 

(3):167-171.
Contains Non-binding Recommendations

Draft-Not for Implementation

Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 14

Dickson, J. S., G. R. Siragusa, and J. E. Wray. 1992. "Predicting the growth of Salmonella 

typhimurium on beef by using the temperature function integration technique." Appl 

Environ Microbiol 58:3482-3487.

Doyle, M. P., and D. J. Roman. 1981. "Growth and survival of Campylobacter fetus subsp jejuni 

as a function of temperature and pH." Journal of Food Protection 44 (8):596-601.

Doyle, M. P., and D. J. Roman. 1982. "Prevalence and survival of Campylobacter jejuni in 

unpasteurized milk." Appl Environ Microbiol 44 (5):1154-8.

Eklund, M. W., G. A. Pelroy, R. Paranjpye, M. E. Peterson, and F. M. Teeny. 1982. "Inhibition of 

Clostridium botulinum type A and type E toxin production by liquid smoke and NaCl in 

hot-process smoke-flavored fish." Journal of Food Protection 45 (10):935-&.

Eklund, M. W., D. I. Wieler, and F. T. Poysky. 1967. "Outgrowth and toxin production of 

nonproteolytic type B Clostridium botulinum at 3.3 to 5.6 °C." J Bacteriol 93 (4):1461-&.

El-Shenawy, M. A., and E. H. Marth. 1988. "Inhibition and inactivation of Listeria 

monocytogenes by sorbic acid." Journal of Food Protection 51 (11):842-847.

El-Shenawy, M. A., and E. H. Marth. 1988. "Sodium benzoate inhibits growth of or inactivates 

Listeria monocytogenes." Journal of Food Protection 51 (7):525-530.

European Chilled Food Federation. 1997. Guidelines for good hygienic practice in the 

manufacture of chilled foods.

Fantasia, L. D., L. Mestrandrea, J. P. Schrade, and J. Yager. 1975. "Detection and growth of 

enteropathogenic Escherichia coli in soft ripened cheese." Appl Microbiol 29 (2):179-

185.

Fapohunda, A. O., K. W. Mcmillin, D. L. Marshall, and W. M. Waites. 1994. "Growth of selected 

cross-contaminating bacterial pathogens on beef and fish at 15 and 35 degrees C." 

Journal of Food Protection 57 (4):337-340.

Farber, J. M., and J. Z. Losos. 1988. " Listeria monocytogenes: a foodborne pathogen." Can 

Med Assoc J 138 (5):413-418.

Fernandez, P. S., S. M. George, C. C. Sills, and M. W. Peck. 1997. "Predictive model of the 

effect of CO2, pH, temperature and NaCl on the growth of Listeria monocytogenes." 

International Journal of Food Microbiology 37 (1):37-45. doi: 10.1016/S0168-

1605(97)00043-3.

Food and Drug Administration (FDA). 2012. "Bad Bug Book: Foodborne pathogenic 

microorganisms and natural toxins handbook." Accessed June 2, 

2016. http://www.fda.gov/downloads/Food/FoodSafety/FoodborneIllness/FoodborneIllne

ssFoodbornePathogensNaturalToxins/BadBugBook/UCM297627.pdf.

Fuchs, A. R., and G. J. Bonde. 1957. "The nutritional requirements of Clostridium perfringens." 

J Gen Microbiol 16 (2):317-329.
Contains Non-binding Recommendations

Draft-Not for Implementation

Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 15

Garren, D. M., M. A. Harrison, and Y. W. Huang. 1994. "Clostridium botulinum type E outgrowth 

and toxin production in vacuum-skin packaged shrimp." Food Microbiol 11 (6):467-472. 

doi: 10.1006/fmic.1994.1052.

Garren, D. M., M. A. Harrison, and Y. W. Huang. 1995. "Growth and production of toxin of 

Clostridium botulinum type E in rainbow trout under various storage conditions." J Food 

Protect 58 (8):863-866.

Garthright, W. E. 1991. "Refinements in the prediction of microbial growth curves." Food 

Microbiol 8 (3):239-248. doi: 10.1016/0740-0020(91)90056-8.

Gay, M., O. Cerf, and K. R. Davey. 1996. "Significance of pre-incubation temperature and 

inoculum concentration on subsequent growth of Listeria monocytogenes at 14 degrees 

C." J Appl Bacteriol 81 (4):433-438.

George, S. M., B. M. Lund, and T. F. Brocklehurst. 1988. "The effect of pH and temperature on 

initiation of growth of Listeria monocytogenes." Lett Appl Microbiol 6 (6):153-156. doi: 

10.1111/j.1472-765X.1988.tb01237.x.

George, S. M., L. C. C. Richardson, and M. W. Peck. 1996. "Predictive models of the effect of 

temperature, pH and acetic and lactic acids on the growth of Listeria monocytogenes." 

Int J Food Microbiol 32 (1-2):73-90. doi: 10.1016/0168-1605(96)01108-7.

Gibbs, P. A., A. R. Davies, and R. S. Fletcher. 1994. "Incidence and growth of psychrotrophic 

Clostridium botulinum in foods." Food Control 5 (1):5-7. doi: 10.1016/0956-

7135(94)90127-9.

Gibson, A. M., N. Bratchell, and T. A. Roberts. 1988. "Predicting microbial growth: Growth 

responses of Salmonellae in a laboratory medium as affected by pH, sodium chloride 

and storage temperature." Int J Food Microbiol 6 (2):155-178. doi: 10.1016/0168-

1605(88)90051-7.

Gill, C. O., and L. M. Harris. 1982. "Survival and growth of Campylobacter fetus subsp. Jejuni on 

meat and in cooked foods." Appl Environ Microbiol 44 (2):259-63.

Gould, G. W. 1999. "Sous vide foods: Conclusions of an ECFF botulinum working party." Food 

Control 10 (1):47-51. doi: 10.1016/S0956-7135(98)00133-9.

Gourama, H., W. Y. J. Tsai, and L. B. Bullerman. 1991. "Growth and production of enterotoxin A 

and enterotoxin D by Staphylococcus aureus in salad bar ingredients and clam 

chowder." J Food Protect 54 (11):844-847.

Goverde, R. L. J., J. G. Kusters, and J. H. J. Huisintveld. 1994. "Growth rate and physiology of 

Yersinia enterocolitica influence of temperature and presence of the virulence plasmid." 

J Appl Bacteriol 77 (1):96-104. doi: 10.1111/j.1365-2672.1994.tb03050.x.

Grecz, N., and L. H. Arvay. 1982. "Effect of temperature on spore germination and vegetative 

cell growth of Clostridium botulinum." Appl Environ Microbiol 43 (2):331-7.
Contains Non-binding Recommendations

Draft-Not for Implementation

Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 16

Guyer, S., and T. Jemmi. 1991. "Behavior of Listeria monocytogenes during fabrication and 

storage of experimentally contaminated smoked salmon." Appl Environ Microbiol 57 

(5):1523-7.

Halpin-Dohnalek, M. I., and E. H. Marth. 1989. "Staphylococcus aureus: production of 

extracellular compounds and behavior in foods - a review." J Food Protect 52 (4):267-

282.

Hanninen, M. L., H. Korkeala, and P. Pakkala. 1984. "Growth and survival characteristics of 

Campylobacter jejuni in liquid egg." J Hyg Cambridge 92 (1):53-58.

Hany, O. E., R. Siddiqi, and M. A. Khan. 1993. "Growth response of Listeria monocytogenes 

NCTC 7973 in two different media at four incubation temperatures." Ann. Acad. Med. 

Singapore, China 22:300-302.

Harrison, M. A., Y. W. Huang, C. H. Chao, and T. Shineman. 1991. "Fate of Listeria 

monocytogenes on packaged, refrigerated, and frozen seafood." Journal of Food 

Protection 54 (7):524-527.

Hathcox, A. K., L. R. Beuchat, and M. P. Doyle. 1995. "Death of enterohemorrhagic Escherichia 

coli O157-H7 in real mayonnaise and reduced-calorie mayonnaise dressing as 

influenced by initial population and storage temperature." Appl Environ Microbiol 61 

(12):4172-4177.

Hauschild, A. H. W. 1989. Clostridium botulinum. In Foodborne bacterial pathogens. Edited by 

Doyle, M. P., New York, NY: Marcel Dekker, Inc.

Helmy, Z. A., A. Abd-El-Bakey, and E. I. Mohamed. 1984. "Factors affecting germination and 

growth of Bacillus cereus spores in milk." Zbl Mikrobiol 139 (2):135-141.

Holler, C., D. Witthuhn, and B. Janzen-Blunck. 1998. "Effect of low temperatures on growth, 

structure, and metabolism of Campylobacter coli SP10." Appl Environ Microbiol 64 

(2):581-587.

Holley, R. A., and M. Proulx. 1986. "Use of egg washwater pH to prevent survival of Salmonella

at moderate temperatures." Poultry Sci 65 (5):922-928.

Hudson, J. A., and S. M. Avery. 1994. "Growth of Listeria monocytogenes, Aeromonas 

hydrophila and Yersinia enterocolitica on cooked mussel tissue under refrigeration and 

mild temperature abuse." J Food Safety 14 (1):41-52. doi: 10.1111/j.1745-

4565.1994.tb00582.x.

Hudson, J. A., and S. J. Mott. 1993. "Growth of Listeria monocytogenes, Aeromonas hydrophila

and Yersinia enterocolitica on cold-smoked salmon under refrigeration and mild 

temperature abuse." Food Microbiol 10 (1):61-68. doi: 10.1006/fmic.1993.1006.

Hughes, A., and A. Hurst. 1980. "The effect of NaCl on the upper temperature limit for growth of 

and enterotoxin synthesis by Staphylococcus aureus." Can J Microbiol 26 (4):507-10.
Contains Non-binding Recommendations

Draft-Not for Implementation

Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 17

Huss, H. H., I. Shaeffer, E. R. Petersen, and D. C. Cann. 1979. "Toxin production by Clostridium 

botulinum type E in fresh herring in relation to the measured oxidation potential (Eh)." 

Nord Vet Med 31 (2):81-6.

Hwang, C. A., and M. L. Tamplin. 2005. "The influence of mayonnaise pH and storage 

temperature on the growth of Listeria monocytogenes in seafood salad." Int J Food 

Microbiol 102 (3):277-85. doi: 10.1016/j.ijfoodmicro.2004.11.019.

Ingham, S. C., R. A. Alford, and A. P. McCown. 1990. "Comparative growth-rates of Salmonella 

typhimurium and Pseudomonas fragi on cooked crab meat stored under air and modified 

atmosphere." J Food Protect 53 (7):566-&.

International Commission on Microbiological Specification for Foods (ICMSF). 1996. 

Microorganisms in Foods 5: Characteristics of Microbial Pathogens. Blackie Academic & 

Professional.

Islam, M. S., M. K. Hasan, and S. I. Khan. 1993. "Growth and survival of Shigella flexneri in 

common Bangladeshi foods under various conditions of time and temperature." Appl

Environ Microbiol 59 (2):652-654.

Jemmi, T., and A. Keusch. 1992. "Behavior of Listeria monocytogenes during processing and 

storage of experimentally contaminated hot-smoked trout." Int J Food Microbiol 15 (3-

4):339-346. doi: 10.1016/0168-1605(92)90067-D.

Johnson, K. M., C. L. Nelson, and F. F. Busta. 1983. "Influence of temperature on germination 

and growth of spores of emetic and diarrheal strains of Bacillus cereus in a broth 

medium and in rice." J Food Sci 48 (1):286-287. doi: 10.1111/j.1365-

2621.1983.tb14853.x.

Jones, J. E., S. J. Walker, J. P. Sutherland, M. W. Peck, and C. L. Little. 1994. "Mathematical 

modeling of the growth, survival and death of Yersinia enterocolitica." Int J Food 

Microbiol 23 (3-4):433-447. doi: 10.1016/0168-1605(94)90168-6.

Jorgensen, L. V., and H. H. Huss. 1998. "Prevalence and growth of Listeria monocytogenes in 

naturally contaminated seafood." Int J Food Microbiol 42 (1-2):127-131. doi: 

10.1016/S0168-1605(98)00071-3.

Juneja, V. K., J. E. Call, B. S. Marmer, and A. J. Miller. 1994. "The effect of temperature abuse 

on Clostridium perfringens in cooked turkey stored under air and vacuum." Food 

Microbiol 11 (3):187-193. doi: 10.1006/fmic.1994.1022.

Juneja, V. K., and B. S. Marmer. 1996. "Growth of Clostridium perfringens from spore inocula in 

sous-vide turkey products." Int J Food Microbiol 32 (1-2):115-123. doi: 10.1016/0168-

1605(96)01111-7.

Juneja, V. K., B. S. Marmer, J. G. Phillips, and S. A. Palumbo. 1996. "Interactive effects of 

temperature, initial pH, sodium chloride, and sodium pyrophosphate on the growth 

kinetics of Clostridium perfringens." J Food Protect 59 (9):963-968.

Kaneko, T., and R. R. Colwell. 1973. "Ecology of Vibrio parahaemolyticus in Chesapeake Bay." 

J Bacteriol 113 (1):24-32.
Contains Non-binding Recommendations

Draft-Not for Implementation

Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 18

Kang, C. K., M. Woodburn, A. Pagenkopf, and R. Cheney. 1969. "Growth, sporulation, and 

germination of Clostridium perfringens in media of controlled water activity." Appl 

Microbiol 18 (5):798-805.

Kaspar, C. W., and M. L. Tamplin. 1993. "Effects of temperature and salinity on the survival of 

Vibrio vulnificus in seawater and shellfish." Appl Environ Microbiol 59 (8):2425-9.

Kauppi, K. L., S. R. Tatini, F. Harrell, and P. Feng. 1996. "Influence of substrate and low 

temperature on growth and survival of verotoxigenic Escherichia coli." Food Microbiol

13 (5):397-405. doi: 10.1006/fmic.1996.0046.

Kramer, J. M., and J. M. Gilbert. 1989. “Chapter 2: Bacillus cereus and other Bacillus species.” 

In Foodborne Bacterial Pathogens. Edited by Doyle, M. P., New York, NY: Marcel 

Dekker, Inc.

Lappi, V. R., A. Ho, K. Gall, and M. Wiedmann. 2004. "Prevalence and growth of Listeria on 

naturally contaminated smoked salmon over 28 days of storage at 4 deg C." Journal of 

Food Protection 67 (5):1022-1026.

Larousse, J., and B. Brown. 1997. “Thermobacteriology.” In Food Canning Technology. Edited 

by Larousse, J. and Brown, B., New York: Wiley-VCH.

Lin, J. S., I. S. Lee, J. Frey, J. L. Slonczewski, and J. W. Foster. 1995. "Comparative analysis of 

extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli." 

J Bacteriol 177 (14):4097-4104.

Lindberg, C. W., and E. Borch. 1994. "Predicting the aerobic growth of Y. enterocolitica O-3 at 

different pH-values, temperatures and l-lactate concentrations using conductance 

measurements." International Journal of Food Microbiology 22 (2-3):141-153.

Little, C. L., and S. Knochel. 1994. "Growth and survival of Yersinia enterocolitica, Salmonella

and Bacillus cereus in Brie stored at 4 degrees C, 8 degrees C and 20 degrees C." 

International Journal of Food Microbiology 24 (1-2):137-145. doi: 10.1016/0168-

1605(94)90113-9.

Lotter, L. P., and L. Leistner. 1978. "Minimal water activity for enterotoxin a production and 

growth of Staphylococcus aureus." Appl Environ Microbiol 36 (2):377-80.

Lund, B. M., A. F. Graham, S. M. George, and D. Brown. 1990. "The combined effect of 

incubation temperature, pH and sorbic acid on the probability of growth of nonproteolytic, type B Clostridium botulinum." J Appl Bacteriol 69 (4):481-92.

Mackey, B. M., and N. Bratchell. 1989. "The heat resistance of Listeria monocytogenes." Lett 

Appl Microbiol 9 (3):89-94. doi: 10.1111/j.1472-765X.1989.tb00298.x.

Mackey, B. M., T. A. Roberts, J. Mansfield, and G. Farkas. 1980. "Growth of Salmonella on 

chilled meat." J Hyg Cambridge 85 (1):115-124.

Matches, J. R., and J. Liston. 1968. "Low temperature growth of Salmonella." J Food Sci 33 

(6):641-645. doi: 10.1111/j.1365-2621.1968.tb09092.x.
Contains Non-binding Recommendations

Draft-Not for Implementation

Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 19

Matches, J. R., and J. Liston. 1972. "Effect of pH on low-temperature growth of Salmonella." J 

Milk Food Technol 35 (1):49-52.

Matches, J. R., J. Liston, and L. P. Daneault. 1971. "Survival of Vibrio parahaemolyticus in fish 

homogenate during storage at low temperatures." Appl Microbiol 21 (5):951-952.

Maurelli, A. T., B. Blackmon, and R. Curtiss. 1984. "Temperature-dependent expression of 

virulence genes in Shigella species." Infect Immun 43 (1):195-201.

McClure, P. J., A. L. Beaumont, J. P. Sutherland, and T. A. Roberts. 1997. "Predictive modelling 

of growth of Listeria monocytogenes - the effects on growth of NaCl, pH, storage 

temperature and NaNO2." Int J Food Microbiol 34 (3):221-232. doi: 10.1016/S0168-

1605(96)01193-2.

McElroy, D. M., L. A. Jaykus, and P. M. Foegeding. 2000. "Validation and analysis of modeled 

predictions of growth of Bacillus cereus spores in boiled rice." J Food Protect 63 

(2):268-272.

Miles, D. W., T. Ross, J. Olley, and T. A. McMeekin. 1997. "Development and evaluation of a 

predictive model for the effect of temperature and water activity on the growth rate of 

Vibrio parahaemolyticus." Int J Food Microbiol 38 (2-3):133-142. doi: 10.1016/S0168-

1605(97)00100-1.

Murphy, S. K., and J. D. Oliver. 1992. "Effects of temperature abuse on survival of Vibrio 

vulnificus in oysters." Appl Environ Microbiol 58 (9):2771-2775.

National Advisory Committee on Microbiological Criteria for Foods (NACMCF). 1991. "Listeria 

monocytogenes. Recommendations by the national advisory committee on 

microbiological criteria for foods." Int J Food Microbiol 14 (3-4):185-246.

National Advisory Committee on Microbiological Criteria for Foods (NACMCF). 1992. Vacuum 

or modified atmosphere packaging for refrigerated raw fishery products. Washington, 

DC: U.S. Department of Agriculture, Food Safety and Inspection Service.

Olmez, H. K., and N. Aran. 2005. "Modeling the growth kinetics of Bacillus cereus as a function

of temperature, pH, sodium lactate and sodium chloride concentrations." Int J Food 

Microbiol 98 (2):135-143.

Ostovar, K., and M. J. Bremier. 1975. "Effect of thawing on growth of Staphylococcus aureus in 

frozen convenience food items." J Milk Food Technol 38 (6):337-339.

Palumbo, S. A., J. E. Call, F. J. Schultz, and A. C. Williams. 1995. "Minimum and maximum 

temperatures for growth and verotoxin production by hemorrhagic strains of Escherichia 

coli." J Food Protect 58 (4):352-356.

Pelroy, G., M. Peterson, R. Paranjpye, J. Almond, and M. Eklund. 1994. "Inhibition of Listeria 

monocytogenes in cold-process (smoked) salmon by sodium nitrite and packaging 

method." J Food Protect 57 (2):114-119.
Contains Non-binding Recommendations

Draft-Not for Implementation

Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 20

Pelroy, G. A., M. W. Eklund, R. N. Paranjpye, E. M. Suzuki, and M. E. Peterson. 1982. 

"Inhibition of Clostridium botulinum type A and type E toxin formation by sodium nitrite 

and sodium chloride in hot-process (smoked) salmon." J Food Protect 45 (9):833-841.

Peters, A. C., L. Thomas, and J. W. T. Wimpenny. 1991. "Effects of salt concentration on 

bacterial growth on plates with gradients of pH and temperature." Fems Microbiol Lett

77 (2-3):309-314. doi: 10.1111/j.1574-6968.1991.tb04367.x.

Peterson, M. E., G. A. Pelroy, R. N. Paranjpye, F. T. Poysky, J. S. Almond, and M. W. Eklund. 

1993. "Parameters for control of Listeria monocytogenes in smoked fishery products: 

Sodium chloride and packaging method." J Food Protect 56 (11):938-943.

Peterson, M. E., G. A. Pelroy, F. T. Poysky, R. N. Paranjpye, F. M. Dong, G. M. Pigott, and M. 

W. Eklund. 1997. "Heat-pasteurization process for inactivation of non-proteolytic types of 

Clostridium botulinum in picked Dungeness crabmeat." J Food Protect 60 (8):928-934.

Presser, K. A., T. Ross, and D. A. Ratkowsky. 1998. "Modelling the growth limits (growth no 

growth interface) of Escherichia coli as a function of temperature, pH, lactic acid 

concentration, and water activity." Appl Environ Microbiol 64 (5):1773-1779.

Ratkowsky, D. A., R. K. Lowry, T. A. Mcmeekin, A. N. Stokes, and R. E. Chandler. 1983. "Model 

for bacterial culture growth-rate throughout the entire biokinetic temperature range." J 

Bacteriol 154 (3):1222-1226.

Ratkowsky, D. A., J. Olley, T. A. Mcmeekin, and A. Ball. 1982. "Relationship between 

temperature and growth-rate of bacterial cultures." J Bacteriol 149 (1):1-5.

Reddy, N. R., A. Paradis, M. G. Roman, H. M. Solomon, and E. J. Rhodehamel. 1996. "Toxin 

development by Clostridium botulinum in modified atmosphere-packaged fresh tilapia 

fillets during storage." J Food Sci 61 (3):632-635.

Reed, G. H. 1993. "Foodborne illness (part 2): Salmonellosis." Dairy, Food, Environ San 13:706

Reed, G. H. 1994a. "Foodborne illness (part 3): Clostridium perfringens gastroenteritis." Dairy, 

Food, Environ San 14:16-17.

Reed, G. H. 1994b. "Foodborne illness (part 4): Bacillus cereus gastroenteritis." Dairy, Food, 

Environ San 14:87

Reed, G. H. 1994c. "Foodborne illness (part 8): Escherichia coli." Dairy, Food, Environ San

14:329-330.

Reed, G. H. 1994d. "Foodborne illness (part 11): Yersinosis.” Dairy, Food, Environ San 14:536

Rey, C. R., H. W. Walker, and P. L. Rohrbaugh. 1975. "Influence of temperature on growth, 

sporulation, and heat-resistance of spores of 6 strains of Clostridium perfringens." J Milk 

Food Technol 38 (8):461-465.

Richards, J. C. S., A. C. Jason, G. Hobbs, D. M. Gibson, and R. H. Christie. 1978. "Electronic 

measurement of bacterial growth." J Phys E Sci Instrum 11 (6):560-568.
Contains Non-binding Recommendations

Draft-Not for Implementation

Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 21

Roberts, D., and R. J. Gilbert. 1979. "Survival and growth of non-cholera Vibrios in various 

foods." J Hyg-Cambridge 82 (1):123-131.

Roberts, T. A., and C. M. Derrick. 1978. "Effect of curing salts on growth of Clostridium 

perfringens (welchii) in a laboratory medium." J Food Technol 13 (4):349-353.

Roberts, T. A., and A. M. Gibson. 1986. "Chemical methods for controlling Clostridium 

botulinum in processed meats." Food Technol 40 (4):163-171, 176.

Roberts, T. A., and G. Hobbs. 1968. "Low-temperature growth characteristics of Clostridia." J 

Appl Bacteriol 31 (1):75-88. doi: 10.1111/j.1365-2672.1968.tb00343.x.

Romick, T. L., H. P. Fleming, and R. F. McFeeters. 1996. "Aerobic and anaerobic metabolism of 

Listeria monocytogenes in defined glucose medium." Appl Environ Microbiol 62 (1):304-

307.

Rorvik, L. M., and M. Yndestad. 1991. "Listeria monocytogenes in foods in Norway." Int J Food 

Microbiol 13 (2):97-104. doi: 10.1016/0168-1605(91)90052-Q.

Rorvik, L. M., M. Yndestad, and E. Skjerve. 1991. "Growth of listeria monocytogenes in vacuumpacked, smoked salmon, during storage at 4 degrees C." Int J Food Microbiol 14 

(2):111-117. doi: 10.1016/0168-1605(91)90097-9.

Schiemann, D. A. 1988. "Examination of entero-toxin production at low-temperature by Yersinia

spp in culture media and foods." J Food Protect 51 (7):571-573.

Segner, W. P., C. F. Schmidt, and J. K. Boltz. 1971. "Minimal growth temperature, sodium 

chloride tolerance, pH sensitivity, and toxin production of marine and terrestrial strains of 

Clostridium botulinum type C." Appl Microbiol 22 (6):1025-&.

Shaw, M. K., A. G. Marr, and J. L. Ingraham. 1971. "Determination of the minimal temperature 

for growth of Escherichia coli." J Bacteriol 105 (2):683-4.

Skinner, G. E., and J. W. Larkin. 1998. "Conservative prediction of time to Clostridium botulinum

toxin formation for use with time-temperature indicators to ensure the safety of foods." J 

Food Protect 61 (9):1154-1160.

Smith, G. R., and A. Turner. 1989. "The production of Clostridium botulinum toxin in 

mammalian, avian and piscine carrion." Epidemiology and Infection 102 (3):467-471.

Smith, M. G. 1985. "The generation time, lag time, and minimum temperature of growth of 

coliform organisms on meat, and the implications for codes of practice in abattoirs." J 

Hyg-Cambridge 94 (3):289-300.

Sokari, T. 1991. "Distribution of enterotoxigenic Staphylococcus aureus in ready-to-eat foods in 

eastern Nigeria." Int J Food Microbiol 12 (2-3):275-280. doi: 10.1016/0168-

1605(91)90079-5.

Stern, N. J., and A. W. Kotula. 1982. "Survival of Campylobacter jejuni inoculated into groundbeef." Appl Environ Microbiol 44 (5):1150-1153.
Contains Non-binding Recommendations

Draft-Not for Implementation

Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 22

Sutherland, A. D. 1993. "Toxin production by Bacillus cereus in dairy products." J Dairy 

Research 60 (4):569-574.

Sutherland, J. P., A. Aherne, and A. L. Beaumont. 1996. "Preparation and validation of a growth 

model for Bacillus cereus: The effects of temperature, pH, sodium chloride, and carbon 

dioxide." Int J Food Microbiol 30 (3):359-372. doi: 10.1016/0168-1605(96)00962-2.

Sutherland, J. P., and A. J. Bayliss. 1994. "Predictive modeling of growth of Yersinia 

enterocolitica: The effects of temperature, pH and sodium chloride." Int J Food Microbiol

21 (3):197-215. doi: 10.1016/0168-1605(94)90028-0.

Sutherland, J. P., A. J. Bayliss, and D. S. Braxton. 1995. "Predictive modeling of growth of 

Escherichia coli O157:H7: The effects of temperature, pH and sodium chloride." Int J 

Food Microbiol 25 (1):29-49. doi: Doi 10.1016/0168-1605(94)00082-H.

Sutherland, J. P., A. J. Bayliss, and T. A. Roberts. 1994. "Predictive modeling of growth of 

Staphylococcus aureus: The effects of temperature, pH and sodium chloride." Int J 

Food Microbiol 21 (3):217-236. doi: 10.1016/0168-1605(94)90029-9.

Taormina, P. J., G. W. Bartholomew, and W. J. Dorsa. 2003. "Incidence of Clostridium 

perfringens in commercially produced cured raw meat product mixtures and behavior in 

cooked products during chilling and refrigerated storage." J Food Protect 66 (1):72-81.

Tatini, S. R. 1973. "Influence of food environments on growth of Staphylococcus aureus and 

production of various enterotoxins." J Milk Food Technol 36 (11):559-563.

Thayer, D. W., W. S. Muller, R. L. Buchanan, and J. G. Phillips. 1987. "Effect of NaCl, pH, 

temperature, and atmosphere on growth of Salmonella typhimurium in glucose-mineral 

salts medium." Appl Environ Microbiol 53 (6):1311-1315.

Thomas, L. V., J. W. Wimpenny, and A. C. Peters. 1991. "An investigation of the effects of four 

variables on the growth of Salmonella typhimurium using two types of gradient gel 

plates." Int J Food Microbiol 14 (3-4):261-75.

Thomas, L. V., J. W. Wimpenny, and A. C. Peters. 1992. "Testing multiple variables on the 

growth of a mixed inoculum of Salmonella strains using gradient plates." Int J Food 

Microbiol 15 (1-2):165-75.

Tipparaju, S., S. Ravishankar, and P. J. Slade. 2004. "Survival of Listeria monocytogenes in 

vanilla-flavored soy and dairy products stored at 8 degrees C." J Food Prot 67 (2):378-

82.

Twedt, R. M., P. L. Spaulding, and H. E. Hall. 1969. "Morphological, cultural, biochemical, and 

serological comparison of Japanese strains of Vibrio parahemolyticus with related 

cultures isolated in the United States." J Bacteriol 98 (2):511-18.

United States Department of Agriculture (USDA)-Microbial Food Safety Research Unit. 2005. 

"Pathogen modeling program 7.0 version 1.1.1433.15425." Accessed June 1, 

2016. http://www.ars.usda.gov/Services/docs.htm?docid=6788.
Contains Non-binding Recommendations

Draft-Not for Implementation

Appendix 3 (Bacterial Pathogen Growth and Inactivation) - Page 23

Venkataramaiah, N., and A. G. Kempton. 1975. "Bacterial growth in seafood on restaurant 

premises." Can J Microbiol 21 (11):1788-1797.

Walker, S. J., P. Archer, and J. G. Banks. 1990. "Growth of Listeria monocytogenes at 

refrigeration temperatures." J Appl Bacteriol 68 (2):157-162. doi: 10.1111/j.1365-

2672.1990.tb02561.x.

Wang, C., and L. A. Shelef. 1992. "Behavior of Listeria monocytogenes and the spoilage 

microflora in fresh cod fish treated with lysozyme and EDTA." Food Microbiol 9 (3):207-

213. doi: 10.1016/0740-0020(92)80048-9.

Ward, D. R., and C. R. Hackney. 1991. Microbiology of marine food products. New York, NY: 

Van Nostrand Reinhold.

Weichart, D., J. D. Oliver, and S. Kjelleberg. 1992. "Low temperature induced non-culturability 

and killing of Vibrio vulnificus." FEMS Microbiol Lett 100 (1-3):205-10.

West, P. A. 1989. "The human pathogenic Vibrios: A public health update with environmental 

perspectives." Epidemiology and Infection 103 (1):1-34.

Whiting, R. C., and K. A. Naftulin. 1992. "Effect of headspace oxygen concentration on growth 

and toxin production by proteolytic strains of Clostridium botulinum." J Food Protect 55 

(1):23-27.

Yang, S. E., and C. C. Chou. 2000. "Growth and survival of Escherichia coli O157: H7 and 

Listeria monocytogenes in egg products held at different temperatures." J Food Protect

63 (7):907-911.

Zaika, L. L., A. H. Kim, and L. Ford. 1991. "Effect of sodium nitrite on growth of Shigella 

flexneri." J Food Protect 54 (6):424-428.

Zaika, L. L., E. Moulden, L. Weimer, J. G. Phillips, and R. L. Buchanan. 1994. "Model for the 

combined effects of temperature, initial pH, sodium chloride and sodium nitrite 

concentrations on anaerobic growth of Shigella flexneri." Int J Food Microbiol 23 (3-

4):345-358. doi: 10.1016/0168-1605(94)90162-7.

Zaika, L. L., J. G. Phillips, and R. L. Buchanan. 1992. "Model for aerobic growth of Shigella

flexneri under various conditions of temperature, pH, sodium chloride and sodium nitrite 

concentrations." J Food Protect 55 (7):509-513.

Zaika, L. L., J. G. Phillips, J. S. Fanelli, and O. J. Scullen. 1998. "Revised model for aerobic 

growth of Shigella flexneri to extend the validity of predictions at temperatures between 

10 and 19 degrees C." Int J Food Microbiol 41 (1):9-19. doi: 10.1016/S0168-

1605(98)00037-3.

Zwietering, M. H., I. Jongenburger, F. M. Rombouts, and K. Vantriet. 1990. "Modeling of the 

bacterial growth curve." Appl Environ Microbiol 56 (6):1875-1881.