Maximum Growth Temperatures
of Foodbourne Pathogens and
appropriate Temperatures for Hot
Holding
MPI Technical Paper No: 2016/06
Prepared for the Ministry for Primary Industries
by Dr J. Andrew Hudson (ESR), Lisa Olsen
(MPI) and Dr Roger Cook (MPI)
ISBN No: 978-1-77665-193-1 (online)
ISSN No: 2253-3923 (online)
January 2011
Disclaimer
While every effort has been made to ensure the information in this publication is accurate, the
Ministry for Primary Industries does not accept any responsibility or liability for error of fact,
omission, interpretation or opinion that may be present, nor for the consequences of any decisions
based on this information.
Requests for further copies should be directed to:
Publications Logistics Officer
Ministry for Primary Industries
PO Box 2526
WELLINGTON 6140
Email: [email protected]
Telephone: 0800 00 83 33
Facsimile: 04-894 0300
This publication is also available on the Ministry for Primary Industries website at
http://www.mpi.govt.nz/news-and-resources/publications/
© Crown Copyright - Ministry for Primary Industries
Scientific Interpretative Summary
This SIS is prepared by MPI risk assessors to provide context to the following report
for MPI risk managers and external readers.
Standardisation of parameters for pathogen control in food:
Maximum growth temperatures of foodborne pathogens and
appropriate temperatures for hot-holding
ESR FW10047
This report reviews maximum growth data for the foodborne pathogens Campylobacter
jejuni, Campylobacter coli, Staphylococcus aureus, Salmonella, STECs, Clostridium
perfringens, Listeria monocytogenes, Yersinia entercolitica and Bacillus cereus.
The report notes that there limited data available for studies of growth in a food matrix and
thus data on growth in broth has had to be used. This impacts on the ability to make
recommendations on hot-holding temperatures. There is also limited data on temperatures
that allow toxin production. In particular the absence of data relating to the two most heattolerant of the pathogens studied (Bacillus cereus and Clostridium perfringens) both with
regards to growth and toxin production, is a major data gap. Within this limitation, maximum
growth temperatures have been arrived at. These data have allowed the limits cited by
ICMSF in 1996 to be refined.
The report concludes that the current hot-holding temperature recommendation of 60˚C is
appropriate but suggests that this temperature could possibly be lowered to 55˚C with a
maximum holding period. This is a complex topic as both bacterial strain variation and food
matrices need to be considered. More data for the growth and conditions for toxin production
for Bacillus cereus and Clostridium perfringens would assist greatly with such decision
making.
The report contains a detailed discussion on what needs to be considered in arriving at
maximum times for hot-holding.
MAXIMUM GROWTH TEMPERATURES
OF FOODBORNE PATHOGENS
AND APPROPRIATE TEMPERATURES FOR HOT
HOLDING
Prepared for New Zealand Food Safety Authority under project MFS/07/07 –
Standardisation of parameters for pathogen control in foods, as part of overall contract
for scientific services
by
Dr. J. A. Hudson
January 2011
Client Report
FW10047
MAXIMUM GROWTH TEMPERATURES
OF FOODBORNE PATHOGENS
AND APPROPRIATE TEMPERATURES FOR HOT
HOLDING
Dr. Stephen On
Food Programme Leader
Dr. Andrew Hudson
Project Leader
Dr. Tecklok Wong
Peer Reviewer
DISCLAIMER
This report or document ("the Report") is given by the Institute of Environmental
Science and Research Limited ("ESR") solely for the benefit of MAF Food Safety,
Public Health Services Providers and other Third Party Beneficiaries as defined in
the Contract between ESR and the MAF Food Safety, and is strictly subject to the
conditions laid out in that Contract.
Neither ESR nor any of its employees makes any warranty, express or implied, or
assumes any legal liability or responsibility for use of the Report or its contents by
any other person or organisation.
Maximum growth temperatures for
foodborne pathogens
i
January 2011
ACKNOWLEDGMENTS
The author would like to thank Prof. Dr. Monika Ehling-Schulz, University of Veterinary
Medicine, Vienna, Austria for advice concerning the ability of B. cereus to produce emetic
toxin at high temperatures.
Maximum growth temperatures for
foodborne pathogens
ii
January 2011
TABLE OF CONTENTS
1
SUMMARY .................................................................................................................... v
2
INTRODUCTION ......................................................................................................... 1
3
METHODS ..................................................................................................................... 1
4
RESULTS ....................................................................................................................... 2
4.1
4.2
4.2.1
4.2.2
4.2.3
4.2.4
4.2.6
4.2.7
4.2.8
4.3
4.4
Summary of data ...................................................................................................... 2
Summary of data for each pathogen ........................................................................ 3
Campylobacter spp. .............................................................................................. 3
Staphylococcus aureus .......................................................................................... 4
Salmonella............................................................................................................. 5
Shiga toxigenic Escherichia coli (STEC) ............................................................. 6
Listeria monocytogenes ........................................................................................ 8
Yersinia enterocolitica .......................................................................................... 9
Bacillus cereus .................................................................................................... 10
Summary data for all pathogens............................................................................. 12
Existing recommendations by regulators ............................................................... 12
5
DISCUSSION ............................................................................................................... 15
6
PRELIMINARY RECOMMENDATIONS .............................................................. 18
7
APPENDIX 1. FDA FOOD CODE RLEVANT TO HOT HOLDING ................... 20
8
REFERENCES ............................................................................................................ 23
Maximum growth temperatures for
foodborne pathogens
iii
January 2011
LIST OF TABLES
Table 1.
Table 2.
Table 3.
Table 4.
Table 5.
Growth maxima of the specified pathogens according to ICMSF (1996b) ............ 2
Data defining the maximum temperature of growth for Campylobacter spp. ........ 3
Data defining the maximum temperature of growth for Staphylococcus aureus ... 4
Data defining the maximum temperature of growth for Salmonella ...................... 5
Data defining the maximum temperature of growth for E. coli O157 and other
STEC ....................................................................................................................... 6
Table 6.
Data defining the maximum temperature of growth for Clostridium
perfringens .............................................................................................................. 7
Table 7.
Data defining the maximum temperature of growth for Listeria
monocytogenes ........................................................................................................ 8
Table 8.
Data defining the maximum temperature of growth for Yersinia enterocolitica.... 9
Table 9.
Data defining the maximum temperature of growth for Bacillus cereus.............. 10
Table 10. Growth rates and maximum population densities for B. cereus and C. perfringens
at temperatures ≥50°C .......................................................................................... 11
Table 11. Advised/Mandated Hot Holding Temperatures .................................................... 14
LIST OF FIGURES
Figure 1. Graphical representation of the maximum growth temperatures of a range of
foodborne pathogens. ............................................................................................ 12
Maximum growth temperatures for
foodborne pathogens
iv
January 2011
1
SUMMARY
This report is one of a series of four commissioned by MAF Food Safety to address an
identified lack of conformity with respect to temperature advice given by regulators.
This report presents a review of the scientific literature to determine the upper growth
temperatures of foodborne pathogens of relevance to food safety in foods held at high
temperatures. Temperatures recommended for hot holding of foods are discussed in light
of these findings of this review to determine whether they are appropriate.
It was concluded that Bacillus cereus and Clostridium perfringens are the species that
grow at the highest temperatures. The upper limits for growth of both of these organisms
are greater than 50°C, with growth of B. cereus reported in two studies at 55°C. Growth
rate and maximum population density data in this range are limited as are data concerning
the capacity of B. cereus to produce toxins at high temperatures, although the maximum
temperature for emetic toxin production is reported to be 40°C in isolates with maximum
growth temperatures <50°C.
Competent Authorities in New Zealand, Canada and Australia recommend 60°C as an
appropriate hot holding temperature, England and Wales use 63°C and the United States
Food Code uses 57°C (with some exceptions). Maintaining the existing 60°C
recommendation in New Zealand may be prudent as it provides a 5°C buffer over the
maximum temperature observed to permit the growth of B. cereus to account for nonuniform heat distribution in hot holding units and the potential for evaporative cooling at
food surfaces.
This report presents information suggesting that a hot holding temperature of 55°C,
possibly in combination with a maximum holding period, may be sufficient to prevent
significant growth of all pathogens examined, including B. cereus and C. perfringens,
although some significant data gaps remain. Further work may allow a downward revision
of this “safe” limit by taking the growth rate, maximum population density, capacity to
produce toxin at temperatures close to the upper limit for growth and likely holding periods
into consideration. In particular, further studies on the growth/toxin production of B.
cereus and C. perfringens in foods over the 50-55°C temperature range may provide the
required data to allow the formulation of alternative time/temperature hot-holding
combinations.
Maximum growth temperatures for
foodborne pathogens
v
January 2011
2
INTRODUCTION
MAF Food Safety has identified that there is a lack of conformity with respect to
temperature advice given by regulators and food industry organisations to the
consumer and food service industry. This applies across thermal treatment times and
temperatures, chilled storage temperatures and hot holding temperatures.
This report is one of four; the other three being a discussion document considering the
factors affecting thermal death of pathogens (“Background Document on Factors
Influencing the Heat Inactivation of Bacteria in Foods”), a consideration of chilled
storage temperatures (“Minimum Growth Temperatures of Foodborne Pathogens and
Recommended Chiller Temperatures”), and an analysis of time/temperature
combinations required to inactivate a range of pathogens in meat products (“Analysis
of D- and z-Values of Selected Foodborne Pathogens in Meat and Seafood”).
This report presents a review of the scientific literature to determine the upper growth
temperatures of foodborne pathogens of relevance to food safety in foods stored at
high temperatures. Temperatures recommended for hot-holding of foods are discussed
in light of the findings of this review to determine whether they are appropriate.
Some preliminary recommendations are also made.
3
METHODS
The pathogens considered were:
Campylobacter jejuni and coli
Staphylococcus aureus
Salmonella
E. coli O157 and others (The five European Union specified Group A strains)
Clostridium perfringens
Listeria monocytogenes
Yersinia enterocolitica
A discussion document available through the United States Department of Agriculture
Food Safety Inspection Service (2002) indicated that Bacillus cereus also needs to be
considered and so relevant data are presented below. This is because B. cereus and C.
perfringens are those pathogens with the highest maximum growth temperatures and
so most relevant when considering hot holding conditions.
The tables of data published by the International Commission on Microbiological
Specifications for Foods (ICMSF 1996b) were used as an initial source of
information. The data were supplemented by searching the scientific literature using
Infotrieve (http://www4.infotrieve.com/search/databases/newsearch.asp ) to increase
the coverage and to attempt to identify variability or consensus in the maximum
growth temperatures reported. The data used were from papers which described
growth in foods held at temperatures above the optimum for the organism.
Temperatures at which growth was and was not recorded were used where possible,
but in several papers only one of these values was given.
Maximum growth temperatures for
foodborne pathogens
1
January 2011
Data from papers describing attempts to measure growth at considerably higher and
lower temperatures were excluded from assessment of the maximum growth
temperature as they did not assist in defining the growth boundary. Also excluded
were data for foods or media in which the pathogens cannot grow.
4
RESULTS
4.1
Summary of data
There is a lack of maximum growth temperature data for bacteria, especially for
growth in foods rather than microbiological media. It was necessary, therefore, to use
data from all sources to define the upper limits for growth. The maxima extracted
from the ICMSF (1996b) are given in Table 1 and provide initial estimates for these
parameters. However, this book is 15 years old and so additional data are now
available
Table 1.
(1996b)
Growth maxima of the specified pathogens according to ICMSF
Pathogen
Bacillus cereus
Campylobacter jejuni
Clostridium perfringens
Escherichia coli
Listeria monocytogenes
Salmonella
Staphylococcus aureus
Yersinia enterocolitica
Maximum growth temperature (°C)
55
45
50
44-46
45
46.2
48
42
It should be noted that at temperatures above the optimum for growth of any
organism, small changes in temperature bring with them large reductions in specific
growth rates, as an example see the Arrhenius plot illustrating the change in growth
rate over the normal growth range of L. monocytogenes shown in Nichols et al.
(2002).
Factors affecting bacterial growth in food include inter-strain variability, competing
microbiota, and the physicochemical characteristics of the food. These factors will
apply to foods held at any temperature, but the data presented do not allow for their
further analysis for temperatures close to the maximum. It might be possible,
therefore, to have different recommended hot-holding temperatures for different kinds
of foods, but this is not the approach that has generally been taken and it may be
overly complex.
There are some considerations that need to be made when assessing the data in the
tables below. Firstly, the papers cited generally only use a few temperatures and so
this can lead to quite large gaps between temperatures at which growth did or did not
occur.
Maximum growth temperatures for
foodborne pathogens
2
January 2011
Secondly, the incubation periods are different between studies. Therefore a given
pathogen may be reported to grow and not to grow on the same food if the incubation
period was longer in the first instance than the second.
For the purposes of this study, growth was defined as a sustained period of increasing
cell concentration shown in the data presented, irrespective of the amount of growth.
The data below in Tables 2 to 9 give information on growth obtained at temperatures
close to the maximum growth temperature of the organism. It is apparent that the
pathogens with the highest maximum growth temperatures are C. perfringens and B.
cereus. Both of these can grow at temperatures in excess of 50°C, with reports of B.
cereus growing at 55°C in bacteriological media although there are no specific
corresponding data for growth in a food. Both organisms are associated with
foodborne disease outbreaks caused by temperature abused meat and rice dishes. The
other pathogens investigated have maxima approximately 5°C lower than this.
4.2
Summary of data for each pathogen
4.2.1 Campylobacter spp.
Table 2.
spp.
Data defining the maximum temperature of growth for Campylobacter
Food/substrate
Brucella broth
Temperature not
allowing growth
(°C)
47
Egg yolk, yolk and
albumen mixed
Chicken and pork
skins
Skim milk
Autoclaved
minced chicken
Raw liver1
ND
Meat pie
Campylobacter
Agar
Temperature
Reference
allowing growth
(°C)
45
Doyle and Roman
1981
42
Clark and Bueschkens
1986
42
Solow et al. 2003
ND
50
43
ND
37
37
ND
43
ND
ND
44-45
Christopher et al. 1982
Blankenship and
Craven 1982
Moore and Madden
2001
Gill and Harris 1982
1
Data for C. coli.
ND = No Data
Maximum growth temperatures for
foodborne pathogens
3
January 2011
4.2.2 Staphylococcus aureus
Table 3.
aureus
Data defining the maximum temperature of growth for Staphylococcus
Food/substrate
Phosphate buffer
Skim milk
Brain heart infusion
broth
Various media
Temperature not
allowing growth
(°C)
48.9
ND
50
Temperature
allowing growth
(°C)
ND
48.91
452
50
45
ND
43.3
44.4
45.6
46.7
ND
ND
35
44.4
45.6
45.6
44.0
Angelotti et al. 1961
46.6
45.5
55
50
ND
ND
Brown and Twedt
1972
Yang et al. 2001
Kennedy et al. 2005
Minced turkey,
pork and beef
Ham salad
Chicken a la king
Custard
Raw pastry
Steak and kidney
pie filling
Roast beef
Steamed egg
Trypticase soy
broth
Reference
Stiles and Witter
1965
Scheusner et al. 1973
Vandenbosch et al.
1973
Ingham et al. 2007
ICMSF 1996a
1
Condition described as “not lethal”.
Toxin detected.
ND = No Data
2
Maximum growth temperatures for
foodborne pathogens
4
January 2011
4.2.3 Salmonella
Data are for a variety of serovars.
Table 4.
Data defining the maximum temperature of growth for Salmonella
Food/substrate
Temperature not
allowing growth (°C)
Ham salad
Chicken a la king
Custard
Minced
turkey,
pork and beef
Cooked beef
44.4
46.7
46.7
ND
Temperature
allowing growth
(°C)
35.0
45.61
45.61
43.3
48.81
ND
10% milk solids
Minced beef
51.4
51.6
ND
ND
Scald tank water
Steamed egg
Trypticase
soy
broth+2%
yeast
extract
52.5
55
55
ND
ND
ND
Reference
Angelotti et al. 1961
Ingham et al. 2007
Brown and Twedt
1972
Dega et al. 1972
Goodfellow and
Brown 1978
Humphrey 1981
Yang et al. 2001
Ng et al. 1969
1
Maximum population density was reduced.
ND = No Data
Maximum growth temperatures for
foodborne pathogens
5
January 2011
4.2.4
Shiga toxigenic Escherichia coli (STEC)
Table 5. Data defining the maximum temperature of growth for E. coli O157
and other STEC
Food/substrate
Temperature not
allowing growth (°C)
Nutrient Broth
Brain Heart Infusion
Broth
Trypticase Soy Broth
Sterile raw minced
beef
EC broth
Cow and buffalo
milk
Chicken, turkey, beef
and pork sausage
Minced beef
Steamed eggs
ND
ND
ND
45.5
Temperature
allowing growth
(°C)
43.6-47.41
451
49.41
452
Reference
46
45
ND
41
50
ND1
50
ND
Raghubeer and
Matches 1990
Singh and
Ranganathan 1980
Ahmed et al. 1995
54.4
55
ND
ND
Wiegand et al. 2009
Yang and Chou 2000
Salter et al. 1998
Palumbo et al. 1995
Doyle and Schoeni
1984
Tamplin et al. 2005
1
Various serotypes
Very small increase in concentration measured between 44 and 45°C.
ND = No Data
2
Maximum growth temperatures for
foodborne pathogens
6
January 2011
4.2.5 Clostridium perfringens
Table 6. Data defining the maximum temperature of growth for Clostridium
perfringens
Food
Temperature not
allowing growth
(°C)
ND
Temperature
allowing growth
(°C)
541
52
51.72
ND
53
53.3
51.13
Cooked beef
Cooked meat broth
Cooked beef
Cooked chilli
ND
53
51
ND
51
50
50
48.9
Chicken thigh meat
Meat loaf
ND
ND
45
45
Various meat
products
Raw minced beef
ND
45
55
53
Fluid thioglycollate
medium
Cooked meat
medium
Reduced cooked
meat medium
Roast beef
Reference
Li and McClane
(2006)
Shoemaker
and
Pierson 1976
Brown and Twedt
1972
Juneja et al. 2008
Collee et al. 1961
Huang 2003
Blankenship et al.
1988
Craven et al. 1981
Schroder and Busta
1971
Willardsen et al.
1979
1
Maximum temperature recorded for 15 isolates tested.
Growth occurred in one of three isolates tested, the maximum population attained being 3.5 x 10 5
CFU/g.
3
Maximum concentration reached was only ten fold higher than the inoculum. “Normal” growth
occurred at 48.8°C; at higher temperatures a reduction in maximum population density was measured.
ND = No Data
2
Maximum growth temperatures for
foodborne pathogens
7
January 2011
4.2.6 Listeria monocytogenes
Table 7. Data defining the maximum temperature of growth for Listeria
monocytogenes
Food
Temperature not
Temperature
Reference
allowing growth (°C) allowing growth
(°C)
Various turkey and
ND
45
Busta and Schroder
beef products
1971
Trypticase soy
ND
45
Petran and Zottola
broth
1989
Steamed eggs
55
ND
Yang and Chou
2000
Clarified cabbage
50
ND
Beuchat et al. 1986
juice
Beef
50
ND
Mackey et al. 1990
Reconstituted
50
ND
El-Shenawy et al.
nonfat dried milk
1989
Infant formula
50
ND
Linton et al. 1996
Liquid whole egg
50
ND
Knight et al. 1999
Minced beef
50
ND
Doherty et al. 1998
products and potato
slices
Fermented beaker
48.9
ND
Schoeni et al. 1991
sausage
ND = No Data
Maximum growth temperatures for
foodborne pathogens
8
January 2011
4.2.7 Yersinia enterocolitica
Table 8. Data defining the maximum temperature of growth for Yersinia
enterocolitica
Food
Nutrient broth
Milk
Temperature not
allowing growth
(°C)
43
51.7
Temperature allowing
growth (°C)
50
ND
50
ND
Minced beef
products and
potato slices
Skim milk
42
ND
Reference
ICMSF (1996)
Lovett et al.
1982
Doherty et al.
1998
Hanna et al.
1977
ND = No Data
Maximum growth temperatures for
foodborne pathogens
9
January 2011
4.2.8 Bacillus cereus
Table 9.
cereus.
Data defining the maximum temperature of growth for Bacillus
Food/substrate
Trypticase soy
broth
Rice/beef extract
Trypticase soy
agar
Boiled rice
Reconstituted
dehydrated
mashed potato
Nutrient agar and
trypticase soy agar
Brain heart
infusion broth
Skim milk medium
Brain heart
infusion broth +
0.1% glucose
Temperature not
allowing growth
(°C)
ND
Temperature
Reference
allowing growth
(°C)
551
Johnson et al. 1983
55
ND
45
55
55
ND
43
50
ND
50
ND
502
Larkin and Stokes
1966
Borge et al. 2001
50
50
46
46
Finlay et al. 2000
Fermanian et al. 1994
Rusul and Yaacob
1995
Gilbert et al. 1974
Turner et al. 2006
1
Despite growth being recorded for some isolates in Trypticase Soy Broth the maximum population
reached was < 106 CFU/ml.
2
One of eleven isolates tested grew at this temperature
None of these studies reported on toxin production.
ND = No Data
Maximum growth temperatures for
foodborne pathogens
10
January 2011
Table 10 shows measured growth kinetic data for B. cereus and C. perfringens
obtained for experiments conducted between 50 and 55°C. This was done to provide
information which might be used to allow flexibility in hot holding recommendations.
Table 10. Growth rates and maximum population densities for B. cereus and C.
perfringens at temperatures ≥50°C
Food/substrate
Temperature
(°C)
Generation
time (h)
Lag
time
(h)
Maximum
population
density
(log10 cfu/g
or ml)
Reference
B. cereus
Rice
Trypticase soy
broth
501
50
55
6.2
2.2
6.22
ND
ND
ND
2 x 105
5 x 105
105-106
Reconstituted
dehydrated
mashed potato
Brain heart
infusion broth
50
0.2
4
ND
Turner et al.
2006
50
ND
72
ND
Borge et al.
2001
Li
and
McClane
2006
Shoemaker
and Pierson,
19763
Johnson
al. 1983
et
C. perfringens
Fluid
thioglycollate
medium
Cooked meat
medium
Roast beef
Cooked beef
Cooked meat
broth
Cooked beef
50
1.7-1.8
ND
ND
51.7
52.3
52.5
53.0
0.3
0.3
13
13
1
6
6
6
107
106
ND
ND
50
51.1
51
0.9
1.8
0.3
0
0
1
106
5 x 105
106
50
0.2
4
106
50
0.3
2.5
107.5
Brown and
Twedt, 1972
Juneja et al.
2008
Collee et al.
1961
Huang 2003
Data were read from graphs and in some cases interpolations between data points
1
Interpolated from graph presented; there were no datapoints at this temperature.
2
For some isolates
3
This paper describes the “phoenix phenomenon” and although definitive data are not provided it
seems likely that no significant growth above the initial concentration would occur at the highest two
temperatures, since there is a 1 log10 cfu/ml reduction in final concentration when comparing data for
51.7°C and 52.3°C. There is a several log10 reduction in concentration at the higher temperatures prior
to the resumption of growth (hence the phoenix phenomenon).
ND = No data
Maximum growth temperatures for
foodborne pathogens
11
January 2011
4.3
Summary data for all pathogens
The data from this review have been plotted to show the ranges of temperatures found
in the literature (Figure 1).
Figure 1. Graphical representation of the maximum growth temperatures of a
range of foodborne pathogens.
Bacillus cereus
Campylobacter
Clostridium
perfringens
STEC
Salmonella
Staphylococcus
Listeria
Yersinia
40
45
50
55
60
Temperature (°C)
Squares show data datapoints where growth occurred, and circles where it did not.
These data need to be considered in relation to the upper end of the datapoints
representing growth and the lower end of the datapoints representing no growth.
Particular consideration needs to be given to the overlap between the two as this
represents the area of uncertainty. This uncertainty is a result, inter alia, of strain
variation, physiochemical parameters of different foods and the length of time over
which the experiments were conducted.
4.4
Existing recommendations by regulators
The information presented in Table 11 reflects diversity in the way in which hot
holding controls are communicated. Australia, New Zealand, England and Wales, and
Canada have a single temperature. In the USA there was a recommendation for
consideration of prior treatment of the food and the time for which it is to be held, but
this is not contained in the FDA Food Code. The USFDA Food Code hot holding
requirements are is shown below in Appendix 1. Essentially the recommended
Maximum growth temperatures for
foodborne pathogens
12
January 2011
minimum holding temperature is 57°C except for roasts undergoing specified cooking
or reheating regimes may be held at 54°C or above.
Maximum growth temperatures for
foodborne pathogens
13
January 2011
Table 11. Advised/Mandated Hot Holding Temperatures
Country
Australia
Canada
England and
Wales
New Zealand
United States
United States
Holding temperature
60°C or above
Not less than 60°C
At or above 63°C
Link
www.foodstandards.gov.au/_srcfiles/Standard_3_2_2_FS_Practices_&_Gen_Requirements_v106.pdf
www.foodsafe.ca/downloadfiles/FSFoodservices02-FoodPremReg.pdf
http://www.legislation.gov.uk/uksi/1995/2200/regulation/8/made
At 60°C or hotter
57°C or 54°C
51.7°C for a
maximum of 2 h,
54.4°C for a
maximum of 4h,
57.2°C for a
maximum of 8h,
60°C indefinitely
www.MAF Food Safety.govt.nz
http://www.fda.gov/Food/FoodSafety/RetailFoodProtection/FoodCode/FoodCode2001/ucm089117.htm
http://www.fsis.usda.gov/OPHS/NACMCF/2002/rep_hothold1.htm#att2
http://www.fsis.usda.gov/OPHS/NACMCF/2002/hotholdcharge.pdf
(these guidelines were given as part of input into the FDA Food Code amendments given in the row
above, but were not adopted)
Maximum growth temperatures for
foodborne pathogens
14
January 2010
5
DISCUSSION
A summary table of the maximum growth temperatures reported above is given in Table
12.
Growth maxima of the specified pathogens according to data analysed
Table 12.
in this report
Pathogen
Bacillus cereus
Campylobacter jejuni
Clostridium perfringens
STEC O157
Listeria monocytogenes
Salmonella
Staphylococcus aureus
Yersinia enterocolitica
Maximum growth temperature (°C)
55
45
54
49.4
45
45.6
48.9
42
The data show that the bacteria which grow at the highest temperatures in foods are B.
cereus and C. perfringens. These were the only organisms where growth at 50°C or above
was reported, and in the case of B. cereus growth at 55°C has been described in
bacteriological media.
For B. cereus, consideration needs to be made of the potential for emetic toxin to be
produced in situ and for cell concentrations to increase significantly. High concentrations
of cells are typically required, in the order of > 105 CFU/g (although reports vary widely,
Granum 2007), for either emetic or diarrhoeal disease to result. Little information could be
located about toxin production at high temperatures, but production of emetic toxin at 42°C
has been described as minimal at <0.1 µg/g wet weight of cells grown on tryptic soy agar
(Häggblom et al. 2002). However the isolates tested had low maximum growth
temperatures of 42-47°C, which is below most of the reports included in Table 9 and it
may be the case that strains capable of growth at higher temperatures also produce toxin at
higher temperatures. Similar results, but differing in detail with respect to the optimum
temperature for emetic toxin production, have been reported elsewhere (Finlay et al. 2000).
By their assay no toxin was produced by seven isolates, five of which were associated with
food poisoning outbreaks, when incubated at 43°C, with the highest temperature allowing
toxin production being 37°C. The maximum growth temperature of these isolates is not
stated except that they grew at 46°C and not 50°C. The restriction of toxin production to
below 40°C under laboratory conditions has been stated in a review (Ehling-Schulz et al.
2004) and confirmed by the lead author (Ehling-Schulz, Pers. Comm.). While the details
remain unclear as toxin might be produced at higher temperatures in strains with higher
maximum growth temperatures, a difference between conditions allowing growth and
toxin production are suggested by these data.
No information on diarrhoeal toxin production at higher temperatures could be located
although it is considered that food poisoning caused by consumption of pre-formed
diarrhoeal toxin is “unlikely” (Andersson et al. 1995). This is because it is heat labile and
degraded by trypsin.
Maximum growth temperatures for
foodborne pathogens
15
January 2011
In Brain Heart Infusion (BHI) broth plus glucose, growth of B. cereus was considerably
slower at 46°C that at 42°C and the final concentration reached was approximately 0.5
log10 cfu/ml less than at 42°C, but still in the order of 5 x 108/ml (Fermanian et al. 1994).
Differences have been described between the ability to grow in rice compared to broth,
with the organism seemingly able to grow at higher temperatures (55°C) in broth (Table 9).
However, increasing temperature from 30°C to 55°C resulted in increased generation time
and reduced maximum population densities (Johnson et al. 1983). At 45°C some isolates
were able to reach high concnetrations (108/ml) but at 55°C there was no growth in rice. At
50°C growth has been recorded in reconstituted dehydrated mashed potato (Turner et al.
2006), although the incubation period was not continued long enough to allow the
maximum population density to be measured. One of 11 isolates tested was able to grow in
BHI broth at 50°C (Borge et al. 2001) and also in Trypticase Soy Broth (TSB) (Larkin and
Stokes 1966). Growth at 55°C was recorded on Trypticase Soy Agar (TSA), although the
time for growth to become visible was generally days longer than when plates were
incubated at 45°C, and not all isolates were able to grow at 55°C (Rusul and Yaacob
1995).
Growth of B. cereus does occur in the 45-50°C range and it is likely that high
concentrations could be reached given sufficient time. There is a data gap in respect to
growth kinetics in foods in the 50-55°C range, which is crucial for defining a safe hot
holding temperature/set of conditions. A maximum growth temperature of 55°C has been
recorded for a subset of isolates in TSB, but all other data in this temperature range report
growth at 50°C. No data for lag times were found for this temperature range. There is some
evidence for a maximum for emetic toxin production of 40°C, as reported above. One
paper reports the absence of spore germination on reconstituted dehydrated mashed
potatoes held at 52°C with a mean surface temperature of 56°C (Snyder et al. 1983).
Clostridium perfringens does not commonly form toxin in the food but in the intestine
during multiplication and sporulation following ingestion (McClane 2007). The number of
the pathogen required to provide a dose likely to result in food poisoning is at least 107
CFU (Brynestad and Granum, 2002). Rapid growth to high concentrations at 50°C has
been reported in fluid thioglycollate medium (Park and Mikolajcik 1979), roast beef
(Brown and Twedt 1972) and cooked meat medium (Collee et al. 1961, Shoemaker and
Pierson 1976). Cooked meat supported rapid growth to a high concentration when
incubated at 51°C (Juneja et al. 2008). Similar observations have been made at
temperatures up to 51.7°C, and at temperatures at and above 52.3°C. Although the
maximum concentration reached was around 106 CFU/ml at 51.7°C the experiment was not
continued long enough to establish this value when the temperature was 52.5°C and 53°C
(Shoemaker and Pierson 1976). When the data at 51.7°C and 52.3°C are considered it is
unlikely that the final concentration would have exceeded the initial inoculum at the two
higher temperatures as the lag time increased at temperatures above 50°C and, in fact, cell
concentrations decreased markedly for several hours before growth resumed, termed the
“phoenix phenomenon”. In various meat products exposed to increasing temperatures the
point at which growth ceased was between 50 and 55°C (Smith et al. 1980, Willardsen et
al. 1979). It can be concluded that significant growth of C. perfringens at 50°C and slightly
above (at least 51°C) can occur in food.
The data in table 10 reflect the incompleteness of the information regarding the kinetics of
growth for both B. cereus and C. perfringens at temperature at or below 55°C. For B.
cereus there are only two sets of data with respect to growth in foods and both are at 50°C.
Maximum growth temperatures for
foodborne pathogens
16
January 2011
More data are available for C. perfringens but, again, the data are concentrated at the lower
end of the range. One study (Shoemaker and Pierson, 1976) designed to investigate the
“phoenix phenomenon” provides data for slightly higher temperatures. However, the data
suggest that recovered cells may not re-grow to a concentration exceeding that of the
inoculum; the experiment was not continued long enough for this to be established. There
remain many datagaps with respect to growth of these two organisms over the 50-55°C
range.
Compared with B. cereus and C. perfringens the maximum growth temperatures of the
other bacteria considered were markedly lower and so not important in the setting of hot
holding temperatures. For Campylobacter and L. monocytogenes the maximum recorded
growth temperature was 44-45°C for both organisms. Members of the genus Yersinia were
not able to grow in food at 50°C while, in Nutrient Broth, the ICMSF (1996b) report a
maximum growth temperature of 42°C with 76 of 79 isolates growing, but none grew at
43°C. STEC, Salmonella and staphylococci have similar characteristics and none of these
organisms was reported to grow at a temperature above 50°C.
Most authorities recommend a single temperature for hot holding. Australia and Canada
use the same values as New Zealand, i.e. 60°C, while England used a higher temperature
of 63°C. For the data presented above, all of these are adequate to control the pathogens
considered.
The USFDA has some lower temperature limits of 57°C and 54.4°C, in the case of the
latter only for roasts that have been cooked/reheated to specific time/temperature
combinations. The higher of these two temperatures is likely to be effective. The 54.4°C
temperature is in the range where the data are poor but is applied in tandem with other
thermal treatment requirements. The temperatures were derived on an understanding the
the maximum recorded growth temperature for C. perfringens was 52°C. A meeting in
2002 provided input into the hot holding recommendations, and The National Advisory
Committee on Microbiological Criteria for Foods (NACMCF) provided various opinions
during the formulation of the Food Code (link provided in Table 11). The specific question
posed by the FDA and the NACMCF response was;
“Question 4: What minimum time/temperature parameters for hot holding would ensure
food safety?
Response: A product temperature of 130 degrees Fahrenheit (54.4°C) will control growth
of foodborne pathogens during hot holding, with a margin of safety. However, FDA
surveys have shown food temperatures to be highly variable. When 130 degrees
Fahrenheit is used as a minimum hot holding temperature, it is essential that data exist to
demonstrate that 130 degrees Fahrenheit is the minimum temperature in the coldest part of
the food at all times to account for such things as evaporative cooling, equipment
capability, and food matrix dynamics. When data do not exist to verify that 130 degrees
Fahrenheit is the minimum temperature in the coldest part of the food at all times, the
margin of safety should be increased through the use of both time and temperature control.
For non-continuous temperature and time monitoring, a minimum hot holding temperature
of 130 degrees Fahrenheit for a maximum time of 4 hours, based on information provided
by FDA regarding the limitation of growth of Clostridium perfringens to no more than 1
log10 in food, would be adequate to ensure food safety. In addition, the Committee
concluded that a minimum temperature of 135 degrees for a maximum of 8 hours, or a
Maximum growth temperatures for
foodborne pathogens
17
January 2011
minimum temperature of 140 degrees Fahrenheit indefinitely also would be adequate to
ensure food safety. Finally, the Committee concluded that any food that requires
temperature and time control for safety that is maintained during hot holding at a lower
temperature or for a longer time than recommended by the Committee is unsafe for
purposes of food service and retail establishment use.”
A temperature of 130°F is equivalent to 54.4°C, 135°F 57.2°C and 140°F 60°C.
One of the NACMCF time temperature combinations produced in their background
document (Table 11) can be assessed, i.e. holding at 51.7°C for a maximum of 2 h. For C.
perfringens only the lag time at this temperature was 1 h and the generation time 0.3 h
(Table 11) and so a 10-fold allowable increase in concentration would approximate that
which would actually occur. However, the data are from one study and the datapoints read
from a graph. The data that allowed the recommendations in Table 11 to be made are not
provided.
Since the Food Code does not include multiple time/temperature combinations then it can
be concluded that the opinion of the NACMCF was not wholly adopted, but a general hot
holding temperature of 57°C (with exceptions outlined above) adopted in place of the
previous 60°C.
6
PRELIMINARY RECOMMENDATIONS
Of the organisms considered in this report Bacillus cereus and Clostridium perfringens are
those most likely to grow at hot holding temperatures and so are the most important to
consider when establishing hot-holding temperature guidelines.
Both can grow up to 50°C with some studies reporting little effect on growth rate or
maximum population density, but at temperatures above the optimum both the growth rate
and maximum population density decline. Both B. cereus and C. perfringens may be able
to grow in foods at temperatures between 50 and 55°C. Explicit data showing growth in
this temperature range in food are limited, but growth in microbiological media in this
range has also been reported. For both organisms there is scant information on growth
rates, differences between strains, and maximum population densities that might be
achieved in this temperature range. Neither are there data in the 55-60°C range available
that would help to define the maximum growth temperature; all that can be said is that B.
cereus has been reported to grow at 55°C in two studies. Further experimentation would be
required to provide more precise information on these topics.
The recommendations in this report are based on the literature describing the growth of B.
cereus and C. perfringens at high temperatures. However, in the case of B. cereus, illness
is caused by the consumption of toxin in food and there are reports indicating a maximum
of 40°C for emetic toxin production. It is possible that these reports are for isolates with
low growth temperature maxima, but confirmation of the observation has been supplied by
an expert in the field (Ehling-Schulz, Pers. comm.). Similar data for diarrhoeal toxin
production were not located although it is considered that food poisoning caused by
consumption of pre-formed diarrhoeal toxin is “unlikely” because the toxin is temperature
and trypsin sensitive (Andersson et al. 1995).
Maximum growth temperatures for
foodborne pathogens
18
January 2011
A hot holding temperature of 60°C is more conservative than one of 55°C and, if correctly
applied, would ensure that food poisoning events resulting from hot holding are extremely
unlikely. New Zealand, Canada and Australia currently recommend a hot holding
temperature of 60°C. Such a recommendation would build in a safety margin of 5°C above
the identified upper temperature at which growth has been measured and would be
consistent with current recommendations. This would be to accommodate any lack of
uniformity of heating in equipment used for hot holding, and the possibility of evaporative
cooling at the surface of food. Risk managers may wish to weigh this option against
potential energy and organoleptic impacts.
The use of 55°C, possibly with a maximum holding time, could be an option but, given the
available data, the following would need to be considered:
55°C is the maximum temperature at which growth of B. cereus has been recorded,
but this was in only two studies.
The actual maximum growth temperature of B. cereus has not been defined (other
than it is >55°C) and this is a significant data gap
Emetic toxin may not produced at temperatures ≥ 40°C, an observation that could
be confirmed with isolates with higher growth temperature maxima. No equivalent
data were located for diarrhoeal toxins but these are probably not relevant
The fastest generation time at 55°C (estimated from a graph) in medium was 6.2 h,
so the following changes in concentration would be expected:
o 1 log10 increase in concentration would occur in 20.7 h
o 2 log10 increase in concentration would occur in 41.4 h
o 3 log10 increase in concentration would occur in 62.1 h
If growth were to occur at 55°C the rate of growth would be slower than that under
optimum growth conditions and the maximum population density lower, so reducing the
risk. Date presented as graphs by Johnson et al. (1983) show that in rice the maximum
population density reached was around 109 CFU/g at 30-35°C reducing to 108 – 5 x 105
CFU/g at 45°C, and no growth measured at 55°C. In TSB, the maximum concentration
achieved was lower, at 108 CFU/g at 30-35°C, reducing twenty fold and two hundred fold
at 50°C and 55°C respectively. A similar effect occurred with respect to the generation
time, being 10-20 min in rice under optimum conditions and increasing to 20-100 min at
45°C (strain-dependent) in rice. A similar optimum was found in TSB, increasing to 30250 min at 45°C, 150-200 min at 50°C and >200 min at 55°C.
Other time/temperature combinations may be acceptable but could be more complicated to
apply as they would require recording and monitoring of the time for which the food had
been hot held to ensure that the relevant time limit was not exceeded. An example of such
time/temperature recommendations is shown in Table 11 although these were not finally
adopted into the USFDA Food Code. These values were based on a maximum 1 log10
increase in the concentration of C. perfringens but the actual data that led to their
formulation are not provided. A very limited evaluation of one of these criteria (storage at
51.7°C for a maximum of 2 h) suggests that they would result in the stated goal. However,
the data available to inform risk managers are very limited, and further studies on the
growth and toxin production of B. cereus and C. perfringens in foods over the 50-55°C
temperature range would provide the required data to allow the formulation of alternative
time/temperature hot-holding combinations and to provide a greater degree of certainty
around the minimum temperature recommended above.
Maximum growth temperatures for
foodborne pathogens
19
January 2011
7
APPENDIX 1. FDA FOOD CODE RLEVANT TO HOT HOLDING
Source: FDA Food Code 2009
http://www.fda.gov/Food/FoodSafety/RetailFoodProtection/FoodCode/FoodCode2009/uc
m186451.htm#part3-5
3-501.16 Potentially Hazardous Food (Time/Temperature Control for Safety Food),
Hot and Cold Holding.
(A) “Except during preparation, cooking, or cooling, or when time is used as the public
health control as specified under §3-501.19, and except as specified under ¶ (B) and in
¶ (C ) of this section, POTENTIALLY HAZARDOUS FOOD (TIME/TEMPERATURE CONTROL FOR
SAFETY FOOD) shall be maintained:
1. (1) At 57oC (135oF) or above, except that roasts cooked to a temperature
and for a time specified in ¶ 3-401.11(B) or reheated as specified in ¶ 3403.11(E) may be held at a temperature of 54oC (130oF) or above; P or
Sections B and C of this section read:
1. (B) EGGS that have not been treated to destroy all viable Salmonellae shall be
stored in refrigerated EQUIPMENT that maintains an ambient air temperature of 7°C
(45°F) or less. P
2. (C) POTENTIALLY HAZARDOUS FOOD (TIME/TEMPERATURE CONTROL FOR SAFETY
FOOD) in a homogenous liquid form may be maintained outside of the temperature
control requirements, as specified under ¶ (A) of this section, while contained
within specially designed EQUIPMENT that complies with the design and
construction requirements as specified under ¶ 4-204.13(E).
Paragraph 3-501.19 reads:
3-501.19 Time as a Public Health Control.
1. (A) Except as specified under ¶ (D) of this section, if time without temperature
control is used as the public health control for a working supply of POTENTIALLY
HAZARDOUS FOOD (TIME/TEMPERATURE CONTROL FOR SAFETY FOOD) before
cooking, or for READY-TO-EAT POTENTIALLY HAZARDOUS FOOD
(TIME/TEMPERATURE CONTROL FOR SAFETY FOOD) that is displayed or held for sale
or service:
1. (1) Written procedures shall be prepared in advance, maintained in the FOOD
ESTABLISHMENT and made available to the REGULATORY AUTHORITY upon
request that specify: Pf
1. (a) Methods of compliance with Subparagraphs (B)(1) -(3) or C)(1)(5) of this section; Pf and
2. (b) Methods of compliance with § 3-501.14 for FOOD that is
prepared, cooked, and refrigerated before time is used as a public
health control. Pf
2. Time – maximum up to 4 hours
Maximum growth temperatures for
foodborne pathogens
20
January 2011
(B) If time temperature control is used as the public health control up to a
maximum of 4 hours:
1. (1) The FOOD shall have an initial temperature of 5ºC (41ºF) or less when
removed from cold holding temperature control, or 57°C (135°F) or greater
when removed from hot holding temperature control; P
2. (2) The FOOD shall be marked or otherwise identified to indicate the time
that is 4 hours past the point in time when the FOOD is removed from
temperature control; Pf
3. (3) The FOOD shall be cooked and served, served at any temperature if
READY-TO-EAT, or discarded, within 4 hours from the point in time when the
P
FOOD is removed from temperature control; and
4. (4) The FOOD in unmarked containers or PACKAGES, or marked to exceed a
4-hour limit shall be discarded. P
3. (C) If time without temperature control is used as the public health control up to a
maximum of 6 hours:
1. (1) The FOOD shall have an initial temperature of 5ºC (41ºF) or less when
removed from temperature control and the FOOD temperature may not
exceed 21ºC (70ºF) within a maximum time period of 6 hours; P
2. (2) The FOOD shall be monitored to ensure the warmest portion of the FOOD
does not exceed 21ºC (70ºF) during the 6-hour period, unless an ambient air
temperature is maintained that ensures the FOOD does not exceed 21ºC
(70ºF) during the 6-hour holding period; Pf
3. (3) The FOOD shall be marked or otherwise identified to indicate: Pf
1. (a) The time when the FOOD is removed from 5ºC (41ºF) or less cold
holding temperature control, Pf and
2. (b) The time that is 6 hours past the point in time when the FOOD is
removed from cold holding temperature control; Pf
4. (4) The FOOD shall be:
1. (a) Discarded if the temperature of the FOOD exceeds 21°C (70°F), P
or
2. (b) Cooked and served, served at any temperature if READY-TO-EAT,
or discarded within a maximum of 6 hours from the point in time
when the FOOD is removed from 5ºC (41ºF) or less cold holding
temperature control; P and
5. (5) The FOOD in unmarked containers or PACKAGES, or marked with a time
that exceeds the 6-hour limit shall be discarded. P
4. (D) A FOOD ESTABLISHMENT that serves a HIGHLY SUSCEPTIBLE POPULATION may
not use time as specified under ¶¶ (A), (B) or (C) of this section as the public health
control for raw EGGS.
1.
Paragraph 3-401.11(B) reads:
1. B) Whole MEAT roasts including beef, corned beef, lamb, pork, and cured pork
roasts such as ham shall be cooked:
1. (1) In an oven that is preheated to the temperature specified for the roast's
weight in the following chart and that is held at that temperature: Pf
Maximum growth temperatures for
foodborne pathogens
21
January 2011
Oven Type
Oven Temperature Based on Roast Weight
Less than 4.5 kg (10
lbs)
4.5 kg (10 lbs) or More
Still Dry
177oC (350oF) or more
121oC (250oF) or more
Convection
163oC (325oF) or more
121oC (250oF) or more
High Humidity1
121oC (250oF) or less
121oC (250oF) or less
1
Relative humidity greater than 90% for at least 1 hour as measured in the
cooking chamber or exit of the oven; or in a moisture-impermeable bag that
provides 100% humidity.
2. ;and
3. (2) As specified in the following chart, to heat all parts of the FOOD to a
temperature and for the holding time that corresponds to that temperature: P
1
Temperature
°C (°F)
Time1 in
Minutes
Temperature
°C (°F)
Time1 in
Seconds
54.4 (130)
112
63.9 (147)
134
55.0 (131)
89
65.0 (149)
85
56.1 (133)
56
66.1 (151)
54
57.2 (135)
36
67.2 (153)
34
57.8 (136)
28
68.3 (155)
22
58.9 (138)
18
69.4 (157)
14
60.0 (140)
12
70.0 (158)
0
61.1 (142)
8
62.2 (144)
5
62.8 (145)
4
Holding time may include postoven heat rise.
Paragraph 3-403.11(E) reads:
(E) Remaining unsliced portions of MEAT roasts that are cooked as specified under ¶ 3401.11(B) may be reheated for hot holding using the oven parameters and minimum time
and temperature conditions specified under ¶ 3-401.11(B).
Maximum growth temperatures for
foodborne pathogens
22
January 2011
8
REFERENCES
Ahmed N M, Conner D E and Huffman D L (1995) Heat-resistance of Escherichia coli
O157:H7 in meat and poultry as affected by product composition. Journal of Food
Science; 60:606-610.
Andersson A, Ronner U and Granum P E (1995) What problems does the food industry
have with the spore-forming pathogens Bacillus cereus and Clostridium
perfringens ? International Journal of Food Microbiology; 28:145-155.
Angelotti R, Foter M J and Lewis K H (1961) Time temperature effects on salmonellae and
staphylococci in foods II. Behavior at warm holding temperatures. American
Journal of Public Health; 51:83-88.
Beuchat L R, Brackett R E, Hao Y-Y and Conner D E (1986) Growth and thermal
inactivation of Listeria monocytogenes in cabbage and cabbage juice. Canadian
Journal of Microbiology; 32:791-795.
Blankenship L C and Craven S E (1982) Campylobacter jejuni survival in chicken meat as
a function of temperature. Applied and Environmental Microbiology; 44:88-92.
Blankenship L C, Craven S E, Leffler R G and Custer C (1988) Growth of Clostridium
perfringens in cooked chilli during cooling. Applied and Environmental
Microbiology; 54:1104-1108.
Borge G I A, Skeie M, Sorhaug T, Langsrud T and Granum P E (2001) Growth and toxin
profiles of Bacillus cereus isolated from different food sources. International
Journal of Food Microbiology; 69:237-246.
Brown D F and Twedt R M (1972) Assessment of the sanitary effectiveness of holding
temperatures on beef cooked at low temperature. Applied Microbiology; 24:599603.
Brynestad S and Granum PE (2002) Clostridium perfringens and foodborne infections.
International Journal of Food Microbiology; 74:195-202.
Busta F F and Schroder D J (1971) Effect of soy protein on the growth of Clostridium
perfringens. Applied Microbiology; 22:177-183.
Christopher F M, Smith G C and Vanderzandt C (1982) Effect of temperature and pH on
the survival of Campylobacter fetus. Journal of Food Protection; 45:
Clark A G and Bueschkens D H (1986) Survival and growth of Campylobacter jejuni in
egg yolk and albumen. Journal of Food Protection; 49:135-141.
Collee J G, Knowlden J A and Hobbs B C (1961) Studies on the growth, sporulation and
carriage of Clostridium welchii with special reference to food poisoning strains.
Journal of Applied Bacteriology; 24:326-339.
Craven S E, Blankenship L C and McDonel J L (1981) Relationship of sporulation,
enterotoxin formation, and spoilage during growth of Clostridium perfringens type
A in cooked chicken. Applied and Environmental Microbiology; 41:1184-1191.
Dega C A, Goepfert J M and Amundson C H (1972) Heat resistance of salmonellae in
concentrated milk. Applied Microbiology; 23:415-420.
Doherty A M, McMahon C M M, Sheridan J J, Blair I S, McDowell D A and Hegarty T
(1998) Thermal resistance of Yersinia enterocolitica and Listeria monocytogenes in
meat and potato substrates. Journal of Food Safety; 18:
Doyle M P and Roman D J (1981) Growth and survival of Campylobacter fetus subsp.
jejuni as a function of temperature and pH. Journal of Food Protection; 44:596-601.
Doyle M P and Schoeni J L (1984) Survival and growth of Escherichia coli associated
with hemorrhagic colitis. Applied and Environmental Microbiology; 48:855-856.
Maximum growth temperatures for
foodborne pathogens
23
January 2011
El-Shenawy M A, Yousef A E and Marth E H (1989) Thermal inactivation and injury of
Listeria monocytogenes in reconstituted nonfat dry milk. Milchwissenschaft;
44:739-806.
Fermanian C, Fremy J M and Claisse M (1994) Effect of temperature on the vegetative
growth of type and field strains of Bacillus cereus. Letters in Applied
Microbiology; 19:414-418.
Finlay W J J, Logan N A and Sutherland A D (2000) Bacillus cereus produces most emetic
toxin at lower temperatures. Letters in Applied Microbiology; 31:385-389.
Gilbert R J, Sringer M F and Peace T C (1974) The survival and growth of Bacillus cereus
in boiled ad fried rice in relation to outbreaks of food poisoning. Journal of
Hygeine, Cambridge, 73:433-444.
Gill C O and Harris L M (1982) Survival and growth of Campylobacter fetus subsp. jejuni
on meat and in cooked foods. Applied and Environmental Microbiology; 44:259263.
Goodfellow D J and Brown W L (1978) Fate of Salmonella inoculated into beef for
cooking. Journal of Food Protection; 41:598-605.
Granum P E (2007) Bacillus cereus In: Food microbiology fundamentals and frontiers, Ed:
Doyle, M.P. and Beuchat, L.R., 445-455. ASM Press, Washington, DC, USA.
Häggblom M M, Apetroaie C, Andersson M A and Salkinoja-Salonen M S (2002)
Quantitative analysis of cereulide, the emetic toxin of Bacillus cereus, produced
under various conditions. Applied and Environmental Microbiology; 68:24792483.
Hanna M O, Stewart J C, Carpenter Z L and Vanderzant C (1977) Heat resistance of
Yersinia enterocolitica in skim milk. Journal of Food Science; 42:1134-1135.
Huang L (2003) Growth kinetics of Clostridium perfringens in cooked beef. Journal of
Food Safety; 23:91-105.
Humphrey T J (1981) The effects of pH and levels of organic matter on the death rates of
salmonellas in chicken scald-tank water. Journal of Applied Bacteriology; 51:2739.
Ingham S C, Fanslau M A, Burnham G M, Ingham B H, Norback J P and Schaffner D W
(2007) Predicting pathogen growth during short-term temperature abuse of raw
pork, beef and poultry products: Use of an isothermal-based predictive tool Journal
of Food Protection; 70:1445-1456.
International Commission on Microbiological Specifications for Foods (1996a)
Staphylococcus aureus. In: Microorganisms in foods: Microbiological
specifications of food pathogens, Ed: T. A. Roberts, A. C. Baird-Parker and R. B.
Tompkin, 299-333. Blackie Academic: London.
International Commission on Microbiological Specifications for Foods (1996b) Microorganisms in foods 5. Microbiological specifications of food pathogens. Blackie
Academic. London.
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 broth
medium and rice. Journal of Food Science; 48:286-287.
Juneja V K, Marks H and Thippareddi H (2008) Predictive model for growth of
Clostridium perfringens during cooling of cooked uncured beef. Food
Microbiology; 25:42-55.
Kennedy J, Blair I S, McDowell D A and Bolton D J (2005) An investigation of the
thermal inactivation of Staphylococcus aureus and the potential for increased
thermotolerance as a result of chilled storage. Journal of Applied Microbiology;
99:1229-1235.
Maximum growth temperatures for
foodborne pathogens
24
January 2011
Knight K P, Bartlett F M, McKellar R C and Harris L J (1999) Nisin reduces the thermal
resistance of Listeria monocytogenes Scott A in liquid whole egg. Journal of Food
Protection; 62:999-1003.
Larkin J M and Stokes J L (1966) Isolation of psychrophilic species of Bacillus. Journal of
Bacteriology; 91:1667-1671.
Li J and McClane BA (2006) Further comparison of temperature effects on growth and
survival of Clostridium perfringens type A isolates carrying a chromosomal or
plasmid-borne enterotoxin gene. Applied and Environmental Microbiology; 72:
4651-4658.
Linton R H, Carter W H, Pierson M D, Hackney C R and Eifert J D (1996) Use of a
modified Gompertz equation to predict the effects of temperature, pH, and NaCl on
the inactivation of Listeria monocytogenes in infant formula. Journal of Food
Protection; 59:16-23.
Lovett J, Bradshaw J G and Peeler J T (1982) Thermal inactivation of Yersinia
enterocolititca in milk. Applied and Environmental Microbiology; 44:517-519.
Mackey B M, Pritchet C, Norris A and Mead G C (1990) Heat resistance of Listeria: strain
differences and effects of meat type and curing salts. Letters in Applied
Microbiology; 10:251-255.
McClane B A (2007) Clostridium perfringens. In: Food microbiology fundamentals and
frontiers, Ed: M. P. Doyle and L. R. Beuchat, ASM Press: Washington, DC, USA.
Moore J E and Madden R H (2001) Survival of Campylobacter coli in porcine liver. Food
Microbiology; 18:1-10.
Ng H, Bayne H G and Garibaldi J A (1969) Heat resistance of Salmonella: the uniqueness
of Salmonella senftenberg 775W. Applied Microbiology; 17:78-82.
Nichols D S, Presser K A, Olley J, Ross T and McMeekin T A (2002) Variation of
branched-chain fatty acids marks the normal physiological range for growth in
Listeria monocytogenes. Applied and Environmental Microbiology; 68:2809-2813.
Palumbo S A, Call J E, Schultz F J and Williams A C (1995) Minimum and maximum
temperatures for growth and verotoxin production by hemorrhagic strains of
Escherichia coli. Journal of Food Protection; 58:352-256.
Park Y and Mikolajcik E M (1979) Effect of temperature on growth and alpha toxin
production by Clostridium perfringens. Journal of Food Protection; 42:848-851.
Petran R L and Zottola E A (1989) A study of factors affecting the growth and recovery of
Listeria monocytogenes Scott A Journal of Food Science; 54:458-460.
Raghubeer E V and Matches J R (1990) Temperature range for growth of Escherichia coli
serotype O157:H7 and selected coliforms in E. coli medium. Journal of Clinical
Microbiology; 28:803-805.
Rusul G and Yaacob N Y (1995) Prevalence of Bacillus cereus in selected foods and
detection of enterotoxin using TECRA-VIA and BCET-RPLA. International
Journal of Food Microbiology; 25:131-139.
Salter M A, Ross T and McMeekin T A (1998) Applicability of a model for nonpathogenic Escherichia coli for predicting the growth of pathogenic Escherichia
coli. Journal of Applied Microbiology; 85:357-364.
Scheusner D L, Hood L L and Harmon L G (1973) Effect of temperature and pH on
growth and enterotoxin production by Staphylococcus aureus. Journal of Milk and
Food Technology; 36:249-252.
Schoeni J L, Brunner K and Doyle M P (1991) Rates of thermal inactivation of Listeria
monocytogenes in beef and fermented beaker sausage. Journal of Food Protection;
54:334-337.
Maximum growth temperatures for
foodborne pathogens
25
January 2011
Schroder D J and Busta F F (1971) Growth of Clostridium perfringens in meat loaf with
and without added soybean protein. Journal of Milk and Food Technology; 34:215217.
Shoemaker S P and Pierson M D (1976) "Phoenix phenomenon" in the growth of
Clostridium perfringens. Applied and Environmental Microbiology; 32:803-807.
Singh R S and Ranganathan R (1980) Heat resistance of Escherichia coli incow and
buffalo milk. Journal of Food Protection; 43:376-380.
Smith L B, Busta F F and Allen C E (1980) Effect of rising temperatures on growth and
survival of Clostridium perfringens indigenous to raw beef. Journal of Food
Protection; 43:520-524.
Snyder O P, Matthews M E and Marth E H (1983) Fate of Bacillus cereus in whipped
potatoes during pre-service holding as could occur in a conventional foodservice
system. Journal of Food Protection; 46:408-411.
Solow B T, Cloak O M and Fratamico P M (2003) Effect of temperature on viability of
Campylobacter jejuni and Campylobacter coli on raw chicken or pork skin. Journal
of Food Protection; 66:2023-2031.
Stiles M E and Witter L D (1965) Thermal inactivation, heat injury, and recovery of
Staphylococcus aureus. Journal of Dairy Science; 48:677-681.
Tamplin M L, Paoli G, Marmer B S and Phillips J (2005) Models of the behavior of
Escherichia coli O157:H7 in raw sterile ground beef stored at 5 to 46°C.
International Journal of Food Microbiology; 100:335-344.
Turner N J, Whyte R, Hudson J A and Kaltovei S L (2006) Presence and growth of
Bacillus cereus in dehydrated potato flakes and hot-held, ready-to-eat potato
products in New Zealand. Journal of Food Protection; 69:1173-1177.
USDA
FSIS
(2002)
Hot
holding
temperatures.
http://www.fsis.usda.gov/OPHS/nacmcf/2002/rep_hothold1.htm.
Vandenbosch L L, Fung D Y C and Widomski M (1973) Optimum temperature for
enterotoxin production by Staphylococcus aureus S-6 and 137 in liquid medium.
Applied and Environmental Microbiology; 25:498-500.
Warriner K and Namvar A (2009) What is the hysteria with Listeria. Trends in Food
Science and Technology; 20:245-254.
Wiegand K M, Ingham S C and Ingham B H (2009) Survival of Escherichia coli O157 in
ground beef after sublethal heat shock and subsequent isothermal cooking. Journal
of Food Protection; 72:1727-1731.
Willardsen R B, Busta F F and Allen C E (1979) Growth of Clostridium perfringens in
three different beef media and fluid thioglycollate medium at static and constantly
rising temperatures. Journal of Food Protection; 42:144-148.
Yang S-E and Chou C-C (2000) Growth and survival of Escherichia coli O157:H7 and
Listeria monocytogenes in egg products held at different temperatures. Journal of
Food Protection; 63:907-911.
Yang S-E, Yu R-C and Chou C-C (2001) Influence of holding temperature on the growth
and survival of Salmonella spp. and Staphylococcus aureus and the production of
staphylococcal toxin in egg products. International Journal of Food Microbiology;
63:99-107.
Maximum growth temperatures for
foodborne pathogens
26
January 2011