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Food Research International 45 (2012) 695699

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Food Research International


j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / f o o d r e s

Thermal pasteurization requirements for the inactivation of Salmonella in foods


Filipa V.M. Silva a,, Paul A. Gibbs b, c
a
b
c

University of Auckland, Department of Chemical and Materials and Engineering, Private Bag 92019, Auckland 1142, New Zealand
Leatherhead Food International, Randalls Road, Leatherhead, Surrey KT22 7RY, UK
Escola Superior de Biotecnologia - UCP, Rua Dr. Antnio Bernardino de Almeida, 4200-072 Porto, Portugal

a r t i c l e

i n f o

Article history:
Received 4 February 2011
Accepted 7 June 2011
Keywords:
Salmonella
Senftenberg
Poultry
Heat
Thermal resistance
Pasteurization
Refrigeration
Safety

a b s t r a c t
Thermal processing is still one of the most effective methods for inactivating undesirable microorganisms in
foods. Heat is used to inactivate pathogens and in developing typical avours, aromas, texture and colour of a
cooked food. Pasteurization produces safer foods with longer shelf-life. Since mild temperatures are applied
for a specied time, complementary food preservation techniques such as modied atmospheres, addition of
preservatives or the use of refrigerated storage and distribution, might be needed to control the growth of the
surviving microorganisms. This review starts by addressing food contamination by Salmonella spp., referring
to some examples of outbreaks, and the benets of pasteurization in terms of Salmonella inactivation. A
section covering the thermal resistance studies of Salmonella in poultry and other animal-based foods is
presented. Based on Salmonella thermal resistance data, minimum pasteurization times are suggested at
different heating temperatures, to meet the guidelines and recommendations of governmental food agencies
for meat products (7 log reduction). Validation of a minimum pasteurization time must be done for each
specic food-thermal process, by inserting a thermocouple into the coldest spot of the food , and ensuring
that this point is submitted to the minimum pasteurization value required. This procedure will guarantee food
safety with respect to Salmonella. Salmonella pasteurization requirements of low moisture foods such as some
nuts, chocolate and peanut butter are also reviewed.
2011 Elsevier Ltd. All rights reserved.

1. Introduction
Salmonella is one of the most common causes of food poisoning,
and low numbers of this microorganism in foods can cause illness. The
microbe is able to grow at temperatures within the range 8 C to 45 C,
in foods of pH between 4 and 9, and water activity higher than 0.94
(Guthrie, 1992). Thus, contaminated foods from animal origin such as
undercooked/raw meat or poultry, raw eggs, food products containing
raw eggs, raw or under-pasteurized milk/dairy (e.g. butter, ice cream,
cheese) and also a few vegetable based food products, can convey
Salmonella and other pathogens from animals to humans, causing
illness (FDA, 1992; WHO, 2002). Additionally, the ingestion of
contaminated water, the use of contaminated water to irrigate crops
or to wash fresh foods, can also cause human salmonellosis.
1.1. Food poisoning by Salmonella spp
The investigation of outbreaks in Australia and Canada proved that
raw, frozen chicken nuggets/strips can be the causative foods of
salmonellosis, in particular if they are breaded and partially fried
before freezing, misleading the consumers who fail to fully cook the
Corresponding author. Tel.: + 64 9 9232572; fax: + 64 9 3737463.
E-mail addresses: lipa.silva@auckland.ac.nz, lipavinagresilva@gmail.com
(F.V.M. Silva), pgibbs@leatherheadfood.com (P.A. Gibbs).
0963-9969/$ see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodres.2011.06.018

foods after thawing, by just warming in a microwave (Bucher, 2008;


Currie et al., 2005).
Although outbreaks from low moisture (and therefore low aW)
ready-to-eat foods are not very common, a Salmonella outbreak
occurred in Canada in 2001 due to contaminated raw almonds
imported from California (Federal Register/Vol. 72, No. 61/Friday,
March 30, 2007/Rules and Regulations, Pages 1502115036). Other
reports in USA in 20062007, identied Salmonella serotype Tennessee as the causative agent of peanut butter outbreaks (Nguyen, 2010).
Foods such as chocolate, powdered infant formula, toasted oats
breakfast cereal, dry seasonings, paprika-seasoned potato chips, dried
coconut, infant cereals, and children's snacks, were also associated
with Salmonella outbreaks (Chen et al., 2009). Survival of Salmonella
during 4 weeks in dry confectionery raw materials was observed,
being the most probable source of Salmonella contamination in
chocolate processing plants (Komitopoulou & Pealoza, 2009).
Refrigerated storage/distribution can promote food safety and
increase the shelf-life of raw or pasteurized foods (Silva & Gibbs,
2009; 2010), by avoiding or retarding the growth of pathogenic (e.g.
Salmonella) and spoilage microorganisms in foods. However, studies
conducted with inoculated egg yolks and albumen, reported the
growth of Salmonella Enteritidis, S. Typhimurium and S. Heidelberg
strains, during storage at 10 C, and in a few cases, growth was
observed at 4 C (Schoeni, Glass, McDermott, & Wong, 1995).
Therefore, certain strains of Salmonella can be a problem in chilled

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F.V.M. Silva, P.A. Gibbs / Food Research International 45 (2012) 695699

foods (George, 2000; Schoeni et al., 1995). Other research reported


survival of Salmonella inoculated into chicken nuggets during
16 weeks at 20 C (Risco, 2009), and concerns were expressed
regarding raw contaminated poultry frozen foods that are just heated
in a microwave after thawing.
The symptoms of food poisoning by Salmonella are common to
other gastroenteritis of bacterial origin and involve watery diarrhoea,
vomiting, abdominal pain and fever. Only by human faecal microbial
testing, can the bacterium originating the infection be identied. The
most serious forms of disease caused by Salmonella Enterica consist of
typhoid and paratyphoid fevers from serovars Typhi and Paratyphi,
respectively (Hu & Kopecko, 2003). Salmonella infections can be
transmitted between humans, and between animals and humans
(zoonoses), since although certain microbial strains infect animals or
humans, others can infect both.



Tref T
z

2

where: N number of surviving microbial cells, No initial number


of microbial cells, DT is the D-value at temperature T (min), t time
(min) and DTref D-value at reference temperature.
A review on Salmonella thermal inactivation kinetic parameters
determined in various high moisture foods of animal origin is
presented in Table 1. Thermal death time method was used to
determine the kinetic parameters. Published thermal resistances are
listed from higher to lower D- and z-values (Table 1). Most of the
experiments were carried out with a cocktail of various Salmonella
serovars isolated from contaminated foods or animal products. Those
thermal resistances are mainly affected by the Salmonella serotypes
4:1 min D55C 68 min; 0:28 min D60C 16 min;
D65C 2 min; D70C 0:25 min:

1.2. Food thermal pasteurization


Proper cooking or thermal processing of foods can eliminate most
of the vegetative microorganisms (e.g. Salmonella) causing foodborne diseases. Thermal pasteurization is a traditional physical
process of food decontamination which is still in common use
today, for being efcient, environmentally friendly, preservative-free
and inexpensive when compared with other preservation technologies. The mild temperatures applied to foods (b95 C) for a specied
time allow greater retention of the original properties of the raw food
while inactivating vegetative pathogens such as Salmonella. Being a
mild thermal treatment, possible microbial survivors (e.g. sporeformers) might be present in the food after the process. For reasons of
public safety, low-acid (pH N4.6) raw and pasteurized foods, such as
foods from animal origin, are generally stored, transported and sold
under refrigerated conditions (temperature below 7 C) and with a
limited shelf-life, to minimize the outgrowth of pathogenic microorganisms in the foods during distribution. If sterilization is applied, all
microorganisms including sporeformers, will be inactivated and food
can be stored safely at room temperature (Silva & Gibbs, 2009).
The main focus of this review is poultry and meat products which
are submitted to pasteurization and require a cold-chain for
distribution. Minimally heated chilled/frozen stored foods are
convenient for consumers since they present a longer shelf-life than
the fresh food, and can be easily cooked at home. Ready-to-eat meals
(RTE) and refrigerated processed foods of extended durability
(REPFED) are included in this type of foods. REPFED are generally
packaged under vacuum (sous-vide) or modied atmospheres to
ensure anaerobic conditions (to minimise spoilage organisms, and recontamination), and submitted to a mild thermal process, being
stored from a few days to several weeks depending on the food,
severity of the process and storage conditions.
2. Thermal resistance of Salmonella in high moisture animal foods
2.1. First order linear model (D- and z-value)
Most of the publications found in the literature on Salmonella
thermal resistance, assumed the log of survivors vs. time of exposure
to heat, as linear (Table 1). In the rst order kinetic model (Bigelow &
Esty, 1920; Teixeira, Heldman, & Lund, 1992), the Eqs. (1) and (2) are
used to estimate the microbial thermal resistance parameters D- and
z-values, respectively. D-value (or decimal reduction time) is dened
as the time required for a 1-log or one decimal reduction in the
microorganism numbers, and z-value refers to the number of Celsius
degrees required to reduce D by a factor of 10:

N
t
= 10 DT
No

DT = DTref 10

1

The use of Salmonella serotype Senftenberg 775 W (=ATCC 43845)


as a unique microbe in the inoculum (Table 1, Thomas et al., 1966;
Humphrey et al., 1990), or mixed with other serotypes in a cocktail
(Table 1, results of Murphy et al. and Osaili et al.) in the survivor
experiments, seem to be responsible for a relatively higher thermal
resistance, in comparison to the results obtained when not using
this serotype (Humphrey et al., 1990; Juneja, 2007; Mazzotta, 2000;
Schuman & Sheldon, 1997). Still supporting the same conclusion, three
studies conducted in chicken breast (same type of poultry meat),
revealed higher thermal resistance (D55C = 30 min, D60C = 5.9 min)
when using a cocktail containing Salmonella serotypes Senftenberg
(ATCC 43845), Mission and California (Murphy et al., 2000) and lower
heat resistance when those poultry related serotypes were not present
in the Salmonella inoculum: D55C = 6.1 min, D60C = 3 min (Juneja,
2007), and D60C = 0.6 min Mazzotta (2000). Humphrey et al. (1990)
determined much larger thermal resistance of Salmonella Senftenberg
775 W in homogenized whole egg (D60C = 5.6 min) than Salmonella
Enteritidis and Salmonella Typhimurium (D60C = 0.200.44 min).
Ready-to-eat fried chicken patties were the food product in which
the 6 Salmonella cocktail exhibited higher thermal resistance (Osaili
et al., 2006). Overall, the use of different animal meats (chicken, beef,
pork, turkey, duck), different body parts of chicken meat (leg, thigh,
breast), thigh/leg chicken skin versus thigh/leg chicken meat, and raw
meat vs cooked meat did not produce large differences in the thermal
resistance of the same 6 Salmonella cocktail. Variability in D-values of
different foods may be explained by different water and fat contents,
in particular at lower heating temperatures.
2.2. Deviations from linearity
There are several publications describing deviations from linearity
(Bigelow model) in the log of Salmonella survivors vs time, in foods
and solutions. In these publications, the authors opted to use other
mathematical models such as Weibull, to predict the microbial survivors more accurately.
Juneja, Eblen, and Marks (2001) worked with a cocktail of
8 Salmonella serotypes and observed downward concave survivor
curves with a lag time up to 1 min in chicken and turkey meats (58 C
to 65 C), in particular at higher fat contents (10%), and used a
model with a lag time preceding the linear inactivation phase. Downward concave survivor curves were also observed by Legurinel,
Spegagne, Couvert, Coroller, and Mafart (2007) with Salmonella
Typhimurium heated in tryptone salt broth, in particular at the higher
temperature of 59 C tested: Weibull model parameters were determined. Jordan, Gurtler, Marks, Jones, and Shaw (2011) observed initial
lag periods (3 min for 58 C to 9 s for 64 C) in 4 strains of Salmonella
Enteritidis and Oranienburg in liquid egg yolk before the rst order
inactivation, and no initial lag phase was observed at 66 C, the

F.V.M. Silva, P.A. Gibbs / Food Research International 45 (2012) 695699

697

Table 1
Thermal resistance of Salmonella in high moisture foods.
Food product

Salmonella
Inoculum

T (C)

D-value (min)

z-value (C)

Reference

Ready-to-Eat
chicken-fried beef patties

Cocktail of Senftenberg
ATCC 43845 +
5 other serotypesa

Osaili et al. (2006)

Senftenberg 775 W
(= ATCC 43845)
Senftenberg 775 W
(= ATCC 43845)
Cocktail of Senftenberg
ATCC 43845 +
5 other serotypesb

68
16
2.0
0.22
11
1.3
11
1.1
46
5.1
1.9
0.083
43
0.096
43
7.3
0.79
0.090
37
0.066
34
5.6
2.8
30
5.9
1.2
0.24
5.8
0.66
29
6.8
0.58
0.11
25
5.2
0.62
0.12
44
5.7
0.55
0.07
24
3.8
0.61
0.097
12
3.2
0.84
6.1
3.0
0.66
3.2
0.60
0.18
6.4
0.44
0.22
6.9
1.5
0.38
0.15
8.0
1.0
0.28
0.087

6.0

Skim milk

55.0
60.0
65.0
70.0
60.0
65.6
60.0
65.6
55.0
60.0
65.0
70.0
55.0
70.0
55.0
60.0
65.0
70.0
55.0
70.0
55.0
60.0
64.0
55.0
60.0
65.0
70.0
60.0
65.6
55.0
60.0
65.0
70.0
55.0
60.0
65.0
70.0
55.0
60.0
65.0
70.0
55.0
60.0
65.0
70.0
55.0
60.0
62.5
55.0
60.0
62.5
56.0
60.0
63.0
55.0
60.0
64.0
55.0
58.0
60.0
62.0
55.1
58.3
60.0
62.2

6.1

Thomas et al. (1966)

5.7

Thomas et al. (1966)

5.9

Murphy, Beard, et al. (2004)

5.5

Murphy, Martin, et al. (2004)

5.6

Murphy, Osaili, et al. (2004)

5.7

Murphy, Martin, et al. (2004)

8.2

Humphrey et al. (1990)

6.5

Murphy et al. (2000)

5.9

Thomas et al. (1966)

5.8

Murphy et al. (2003)

6.2

Murphy et al. (2003)

5.3

Murphy, Osaili, et al. (2004)

6.3

Murphy et al. (2003)

6.9

Juneja (2007)

8.1

Juneja (2007)

5.7

Mazzotta (2000)

6.0

Humphrey et al. (1990)

4.1

Bucher (2008)

3.5

Schuman and Sheldon (1997)

4.3

Schuman and Sheldon (1997)

Green pea soup


Ground pork

Ground turkey
Ground chicken thigh/leg skin

Ground beef
Homogenized whole egg

Cocktail of Senftenberg ATCC 43845 +


5 other serotypesb
Cocktail of Senftenberg ATCC 43845 +
5 other serotypesb

Cocktail of Senftenberg ATCC 43845 +


5 other serotypesb
Senftenberg 775 W

Chicken breast meat

Cocktail of Senftenberg ATCC 43845 +


5 other serotypesb

Beef bouillon

Senftenberg 775 W
(= ATCC 43845)
Cocktail of Senftenberg ATCC 43845 +
5 other serotypesb

Fully cooked duck muscle meat

Fully cooked turkey breast meat

Cocktail of Senftenberg ATCC 43845 +


5 other serotypesb

Ground chicken thigh/leg meat

Cocktail of Senftenberg ATCC 43845 +


5 other serotypesb

Fully cooked chicken breast

Cocktail of Senftenberg ATCC 43845 +


5 other serotypesb

Chicken thigh meat

Cocktail of 4 serotypesc

Chicken breast meat

Cocktail of 4 serotypesc

Ground chicken breast meat

Cocktail of 7 serotypesd

Homogenized whole egg

Enteritidis PT4

Chicken nugget/strip meat

Enteritidis
(pelleted feed isolate)

Liquid egg white

Cocktail of 5 strainse

Liquid egg yolk

Cocktail of 5 strainse

Senftenberg (ATCC 43845 = 775 W), Typhimurium, Heidelberg (ATCC 8326), Mission, Montevideo (ATCC 8387), California (ATCC 23201).
Senftenberg (ATCC 43845), Typhimurium, Heidelberg, Mission, Montevideo, California.
Typhimurium, Heidelberg, Montevideo, Mbandaka.
d
Typhimurium (ATCC 13311), Heidelberg, Montevideo, Mbandaka, Enteritidis, Thompson.
e
Typhimurium (ATCC 14028, type strain), Typhimurium (25642, egg layer house isolate), Enteritidis (ME-15, shell egg isolate), Enteritidis (ME-18, live poultry isolate),
Enteritidis (ATCC 4931, clinical isolate).
b
c

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F.V.M. Silva, P.A. Gibbs / Food Research International 45 (2012) 695699

highest temperature tested. A new model was developed by the


authors.
Tailing with an upward concavity was registered by Buzrul and
Alpas (2007) at 60 C in Salmonella Typhimurium and S. Enteritidis
suspended in 1% peptone solution. Weibull distribution tted the
survival data better than the rst-order model. In this work, the 1st
order model overestimates the number of survivors, and poses no
problem in terms of safety and process design.
One possibility to overcome deviations from the Bigelow model
and in particular underestimation of survivor numbers, is the application of a P-value which delivers an additional 1 or 2D inactivation
in Salmonella numbers.

Table 2
Minimum process time for meat and poultry food products at various temperatures for
7D Salmonella inactivation in the food's coldest pointa.

3. Pasteurization requirements (P-value) for Salmonella spp.


inactivation in foods

PT-value pasteurization value at temperature T, DT decimal reduction time at


temperature T, CUTT come up time at temperature T, nr not reported.
a
The food coldest point might be different from the geometric centre and should be
determined.
b
D55C, D60C, D65C, D70C were directly extracted from Osaili et al. (2006), whereas
D75C, D80C, and D85C were estimated using z-value = 6 C published by Osaili et al.
(2006).

In general a minimum process of 6 decimal reductions in the


numbers of target microorganism (6D) is recommended for pasteurized foods (Betts & Gaze, 1992; FDA, 2001; ICMSF, 2005). For foods
containing poultry, a minimum process of 7D aiming at Salmonella is
suggested by Canadian Food Inspection Agency (CFIA, 2010).
3.1. Validation of pasteurization processes in meat and poultry products
Regarding the manufacturing process for cooked ready-to-eat
(RTE) meat products, the Canadian Food Inspection Agency requires a
PT-value (pasteurization value, minimum time of food exposure to a
specic temperature T) of 6.5 decimal reductions (6.5D) in Salmonella
spp. in the slowest heating point (usually the geometric centre) of
foods not containing poultry, whereas a minimum pasteurization
causing 7D is needed if food contains poultry (CFIA, 2010). The United
States Department of Agriculture (USDA) rule for minimum lethality
in RTE foods is a 6.5 log reduction of Salmonella in meat for all
categories (cooked, fermented, salt-cured, dried) (FSIS, 2005).
The pasteurization should be applied to the food's coldest point,
and the validation of the pasteurization process requires the experimental determination of the come up time in this spot (CUT, time
to reach the set process temperature) and subsequent conrmation
of the desired pasteurization value in this point. The CUT can be
determined for any temperature by inserting a thermocouple in the
meat's coldest point (needs to be determined although is expected to
be close to the geometric centre). The CUT is dependent on the heat
transfer properties of food, package (if any) and heating medium,
being directly related with the thermal technology applied and the
heating medium (steam, water, air) used, and how the food is exposed
to the heat. Based on the pasteurization requirements (P-value = 7D)
(CFIA, 2010), and on the higher D-values published with Salmonella by
Osaili et al., 2006 (Table 1) for RTE meat products, P-values that will
reduce by 7D the most thermally resistant Salmonella spp. (Senftenberg ATCC 43845) are suggested and listed in Table 2. The CUT must
be added to ensure the centre of food is properly pasteurized by
receiving a 7D process. The USDA recommended values for pasteurising meat and poultry products (FSIS, 1999) are considerably lower
(Table 2).
Processes at 70 C, 75 C, 80 C or 85 C of 91 s + CUT70C, 21 s +
CUT75C, 3.2 s + CUT80C, and CUT85C, respectively, will assure a safe
process in case the food is contaminated with the most thermally
resistant serovar of Salmonella. Given the long processing times
needed at lower temperatures, processing temperatures 70 C are
more realistic for food industry applications.

Pasteurization
temperature,
T (C)

Suggested total process time


(PT-value = 7DT)
DT

55
60
65
70
75
80
85

68 min
16 min
2.0 min
13 s
3.0 s
0.45 s
0

USDA guidelines (FSIS, 1999)


(PT-value=7DT)

PT-value + CUTT

PT-value + CUTT

476 min + CUT55C


112 min + CUT60C
14 min + CUT65C
91 s + CUT70C
21 s + CUT75C
3.2 s + CUT80C
CUT85C

97 min + CUT55C
12 min + CUT60C
95 s + CUT65C
CUT70C
nr
nr
nr

almonds to oil at 126.7 C for 1.6 min is sufcient, although commercially 2.0 min is applied (this treatment achieves 5D in Salmonella
numbers) (TERP, 2007). These temperature/time conditions are much
more severe than normal pasteurization processes because of higher
thermal resistance in nuts and similar commodities such as cocoa
beans and peanut butter, which are very low in water content (low
aW). It is known that microorganisms including Salmonella are much
more resistant to heat in low water-activity foods: D71C in chocolate
decreased from 20 h to 4 h after adding 2% water (Barrile & Cone,
1970); Salmonella spp. survivors were registered after roasting cocoa
beans at 130 C for 5 min (Pealoza-Izurieta, Krapf, Diep, Benz, &
Gantenbein-Demarchi, 2008); Ma et al. (2009) reported that 90 C for
less than 30 min was not sufcient for reducing by 5 log CFU/g of
Salmonella in peanut butter; 26 min at 90 C only reduced Salmonella
by 1D in dark chocolate (Krapf & Gantenbein-Demarchi, 2010). To
overcome this problem, the use of moist air (5 to 90% RH) convection
heating was successfully applied to raw almonds for their pasteurization by Jeong, Marks, and Orta-Ramirez (2009). The surface
moisture status of the almonds rather than RH of the air, was the
most important factor in ensuring effective pasteurization.
4. Final considerations
Pasteurized meat and liquid egg food products must be stored
under refrigerated conditions, to avoid growth of surviving sporeformers.
Regarding liquid egg products, an alternate process must be
devised since too high temperatures (60 C) coagulate the egg,
negatively affecting the texture/quality.
Within high moisture foods, larger D-values were observed with
a cocktail of 6 Salmonella including Senftenberg serovar, in ready-toeat chicken fried beef patties: D55C = 68 min, D60C = 16 min, D65C =
2 min, D70C = 0.22 min, z = 6.0 C.
Some authors found the use of alternative non-linear models more
effective for predicting Salmonella survivors in pasteurized foods.
The conclusions and recommendations for thermal pasteurizations
can be extended to non-thermal pasteurization processes, it being necessary to determine microbial D- and z-values, or non-thermal resistance
parameters of other models, with respect to the new technologies.

3.2. Low moisture foods

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recommended for almond producers in California: a process exposing

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