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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
696
Tref T
z
2
N
t
= 10 DT
No
DT = DTref 10
1
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
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
5.7
5.9
5.5
5.6
5.7
8.2
6.5
5.9
5.8
6.2
5.3
6.3
6.9
Juneja (2007)
8.1
Juneja (2007)
5.7
Mazzotta (2000)
6.0
4.1
Bucher (2008)
3.5
4.3
Ground turkey
Ground chicken thigh/leg skin
Ground beef
Homogenized whole egg
Beef bouillon
Senftenberg 775 W
(= ATCC 43845)
Cocktail of Senftenberg ATCC 43845 +
5 other serotypesb
Cocktail of 4 serotypesc
Cocktail of 4 serotypesc
Cocktail of 7 serotypesd
Enteritidis PT4
Enteritidis
(pelleted feed isolate)
Cocktail of 5 strainse
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
698
Table 2
Minimum process time for meat and poultry food products at various temperatures for
7D Salmonella inactivation in the food's coldest pointa.
Pasteurization
temperature,
T (C)
55
60
65
70
75
80
85
68 min
16 min
2.0 min
13 s
3.0 s
0.45 s
0
PT-value + CUTT
PT-value + CUTT
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.
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