Food Research International 34 (2001) 449455

www.elsevier.com]locate]foodres

Improvement of food safety

design of cook-chill foods
S. Rybka-Rodgers *
Centve fov Adranced Yood Rezeavch, Jnirevzity of Eeztevn Sydney,
Kawkezbuvy Locked Bag 1797 PENRIZK SOJZK DC, NSE 1797, Auztvalia

Accepted 6 December 2000

Abstrast
Preservation principles of cook-chill technology are analysed. There is a need to improve safety design of foods relying
solely on refrigeration to control pathogens. The preservation hurdles, which can be applied to such foods, are double heating,
irradiation, hydrostatic pressure, modified atmosphere packaging, low pH, salt, spices, lactate, bacteriocins, protective
cultures and their com- bination. Theoretical, practical and legislative considerations of these methods are reviewed. g 2001
Elsevier Science Ltd. All rights reserved.
Keywovdz Cook-chill; Sous vide; Food safety; Preservation hurdles

botulinum can produce toxin within 31 days at 3.3 C

1. Introdustion (Schmidt, Lechowich, & Folinazzo, 1961).

Retail refrigerated ready-to-eat meals are gaining

popularity for their convenience and freshness. The
majority of large scale food services are also using
cook- chill technology and often produce tonnes of
product at a time. Lack of expertise by craft-based
small manu- facturers and food services, economical
and logistical pressures to extend shelf-life, necessity
for chilled dis- tribution and potential temperature
abuse by consumers contribute to food safety
hazards.
There is no internationally recognised classification
concerning cook-chill foods. Project Harmony
(www.harmony.alma.ac.be), one of the initiatives of
the Food Linked Agro-Industrial Research European
Commission, provides an inventory of the European
legislation in order to bring uniformity. The Australian
codes (NSU Health Department, 1998a, b) distinguish
two types of cook-chill systems traditional or open
tray (5 days shelf-life) and extended shelf-life or sous
vide (28 days shelf-life). They specify heat treatment
equivalent to 6D reduction of Liztevia monocytogenez
for both systems. The justification for 28 days shelf-
life limit was that non-proteolytic strains of
Cloztvidium
* Tel. +61-2-4570-1339; fax +61-2-4570-1579.
E-mail addvezz s.rodgers@uws.edu.au
2. Pathogens of signifisanse
Traditional cook-chill foods can support growth of
any psychrotrophic aerobic pathogen surviving
cooking (spore-formers) or re-contaminating during
chilling and storage. At 3C the lag phase of the
majority of non- spore forming psychrotrophic
pathogenic bacteria, such as L. monocytogenez, is
about a week with 20 h genera- tion time afterwards
(Mossel & Struijk, 1991). Conse- quently, a product
contaminated with 10 cfu]g of L. monocytogenez, for
example, can accumulate 103 cfu]g within 2 weeks of
storage, which is an infective dose for immuno-
competent people (Sutherland & Porritt, 1997). Thus,
hygienic practices, destruction of vegetative
pathogens during cooking, low storage temperature
and limited shelf life are the controlling factors.
Packaging protects new generation cook-chill foods
such as sous vide (cooked in a bag) from re-
contamina- tion after cooking. Spores of following
pathogens can survive mild heat treatment given to
these products
1. Psychrotrophic non-proteolytic C. botulinum
(D80 C=21.6 min, z=7 C) grows at 3C (Graham,
Mason, & Peck, 1996)
0963-9969]01]$ - see front matter g 2001 Elsevier Science Ltd. All rights
reserved. PII S 0963 -9969 (0 1) 00 06 2 -X
 S. Rybka-Rodgevz ] Yood Rezeavch Intevnational 34 (2001)
449455
2. Bacilluz ceveuz (D100 C=2.73.1 min, z=6.1C)
grows at >4C (van Netten, van de Moosdijk, van
de Hoensel, Mossel, & Perales, 1990)
3. Proteolytic C. botulinum (D121.1 C=0.30.23
min,
z=10C) grows at > 10C (Smelt & Haas, 1978)
4. Cloztvidium pevfvingenz
(D98 C=2131 min,
z=3.8C) grows at >15C (Snyder, 1995)
L. monocytogenez can grow at refrigeration
tempera- tures (Grau, 1996). However, mild heating
such as 2 min at 70C or equivalent is suAcient to
achieve 6D reduc- tion of this pathogen (Gaze,
Brown, & Banks, 1989). Major breach of Good
Manufacturing Practices such as under-
processing]post-process contamination is needed for L.
monocytogenez to survive]contaminate these pro-
ducts and gross temperature abuse during storage
for
C. pevfvingenz and proteolytic C. botulinum to multiply.
The growth of C. botulinum is considered the major
potential safety risk for refrigerated pasteurised foods
(Mossel et al., 1991; Notermans, Dufrenne, & Lund,
1990; Simunovic, Oblinger, & Adams, 1985). A number
of studies have demonstrated its ability to produce
toxin in sous vide foods (Betts & Gaze, 1995; Brown &
Gaze, 1990; Brown, Gaze, & Gaskell, 1991; Cockey &
Tatro, 1974; Simpson, Smith, Dodds, Ramaswamy,
Blanch- field, & Simpson, 1995). Control of B. ceveuz,
another pathogen of significance, also relies on
storage tem- perature. Carlin, Guinebretiere, Choma,
Schmott, and
3
Nguyen-The (1999) did not detect B. ceveuz in
commer- cial courgette puree at 4C.
3. Whermal preserration prinsiples
The preservation principals of sous vide foods are
presented in Fig. 1. Shelf stable foods are heated to
121C for 3 min or equivalent (botulinum cook), which
is similar in lethality to conventional canning. The
examples of such products are ready-to-eat sauces
and legume-based dishes in plastic pouches. The
majority of meals, however, would be grossly
overcooked and taste similar to canned foods. Even
milder heating necessary to achieve 6D reduction of
non-proteolytic C. botulinum requires 2545 min at
70C (Fernandez & Peck, 1997) and storage at <10 C
the growth threshold of pro- teolytic C. botulinum
(Smelt et al., 1978). This tempera- ture should be
lowered to 4C if a suAcient amount of air is left in the
package allowing B. ceveuz to grow (van Netten et
al., 1990).
It is desirable for a preservation system to be based
on more than one controlling factor. The majority of
sous vide foods rely solely on temperature control.
The brea- ches in the cold chain are a regular
occurrence in real life situations. Temperatures above
7C were common for the refrigerated display cases of
convenience stores (Hut- ton, Chehak, & Hanlin, 1991).
At 8C non-proteolytic
4 S. Rybka-Rodgevz ] Yood Rezeavch Intevnational 34 (2001)
449455
Fig. 1. Application of the Hurdle Principle to sous-vide foods.
C. botulinum produced toxin within 3 weeks (Conner,
Scott, Bernard, & Hautter, 1989). Storage
temperature had the greatest eRect on a sous vide
products micro- bial load with the initial microflora
and processing temperature being secondary factors
(Hansen & Hno- chel, 1996). The European Chilled
Food Federation Botulism Uorking Party stated the
need for addi- tional eRective preservation factors for
sous vide foods, in which at least a 6D reduction of
non-proteolytic C. botulinum cannot be guaranteed
(Gould, 1999).
4. Improring extended shelf-life sook-shill foods
safety
An improved safety design of a product allows
exten- sion of its shelf-life and]or reduction of severity
of its processing. First attempts to destroy spore-
forming microflora were made by the modification of
the Nacha System (Bjorkman & Delphine, 1966). The
cooked-in-a- bag product was chilled to 20C to
initiate spore germi- nation, incubated at room
temperature for four hours and then pasteurised at
8590oC to kill sporulated vegetative cells. Such
double heating resulted in overcooking and a tired
flavour. Since then a number of additional pre-
servation hurdles have been applied to cook-chill
foods (Table 1). They are physical, chemical and
biological in nature.
Table 1
Additional hurdles for preservation of extended shelf-life cook-chill meals
Hurdle Advantage
Phyzical
Additional heating ERectively sterile food
Irradiation Possibility of treatment within
packaging
not excessive nutrient loss
MAP Inhibits oxidation and microbial
spoilage
Hydrostatic pressure Possibility of treatment within
packaging
Chemical
pH, salt and spices Low cost
Lactate Heat stable; eRective
against spore-formers
(including
C. botulinum)
Biological
Bacteriocins Many are heat stable; eRective
against spore-formers (including
C. botulinum)
Protective cultures Responsive to temperature change;
eRective against spore-formers
(including C. botulinum)
Potential probiotic eRect
4.1. Ivvadiation
Irradiation is an additive-free preservation method
and equivalent or superior to thermal processing from
a nutritional viewpoint (Shamsuzzaman, Lucht, &
Chuaqui-ORermans, 1995; Thayer, Boyd, Him, Fox, &
Farrell, 1998). It can increase the heat sensitivity of
pathogens (Grant & Patterson, 1995) and be an addi-
tional barrier for cooked and irradiated in a bag
products. Spore-former B. ceveuz was sensitive to
radiation (D10=0.1260.288 kGy) in a roast beef meal
(Grant & Patterson, 1992).
FAO]IAEA]UHO recommends the use of high dose
irradiation (>10 kGy) for preparation of sterilised
meals for hospitalised patients. Non-proteolytic
strains of C. botulinum are only slightly less resistant
to irradia- tion in comparison with proteolytic types
(Him & Foe- geding, 1992). Thus, vegetative
pathogens rather than spore-formers would be the
target for low dose irradia- tion of mildly processed
refrigerated ready-to-eat foods. The shelf-life of sous
vide chicken breasts heated to 71C was extended
from 2 to 58 weeks at 8C by irradiation levels of
18 kGy (Shamsuzzaman, Chuaqui- ORermans,
Lucht, Mcdougall, & Borsa, 1992). The inhibition of L.
monocytogenez increased with the rise in irradiation
level and diminished after the fourth week of storage.
Thayer et al. (1998) demonstrated that the
Disadvantage Reference
Inferior quality Bjorkman and Delphine (1966)
Consumer resistance; capital cost; special Shamsuzzaman et al. (1995)
packaging Grant et al. (1995), Thayer et al.
(1998)
No eRect on pathogens Shaw (1997)
Spore resistance; possible eRect on Carpi et al. (1995)
structure of foods
Simpson et al. (1995), Ismael et
Impact on sensory characteristics al. (1990 a, 1990b), Ultee et al.
and nutritional requirements (1999), Uard et al. (1998)
ARects sensorial quality Meng et al. (1994), Simpson
Failed to inhibit B. (1994), Turner et al. (1996)
ceveuz
Acquired resistance by pathogens; Szabo et al. (1998), Mazzotta,
inconsistency of the inhibitory eRect; Crandall and Montville (1997),
decomposing during storage Scott and Taylor (1981a), Uong
et al. (1988), Mossel and Struijk
(1991)
Cost]handling of cultures; heat Tanaka, Meske, Doyle, Traisman,
sensitivity; loss of bacteriocin producing Thayer and Johnson (1985),
ability Crandall, Uinkowski and Montville
(1994), Embarek et al. (1994),
Turner et al. (1996), Dave and Shah
(1997)
resistance to irradiation of L. monocytogenez on air- acetate. Acetic and lactic acid were less eRective than
packed refrigerated turkey breast meat depended on citric acid and sorbate
its state cooked versus raw and nuggets versus
mince. Irradiation at 23 kGy prevented spoilage of
cook-chill ready meals (roast beef and gravy,
cauliflower and white sauce, roast and mashed
potatoes) stored for 15 days at 23C, but aRected
the colour, appearance and textural attributes of
vegetable components (McAteer, Grant, Patterson,
Stevenson, & Ueatherup, 1995).
The eRect on sensorial quality, need for an
irradiation plant and specially designed packaging
material are the limiting factors. However, the major
obstacle for the adoption of this technology is
consumer resistance to food irradiation and legislative
restrictions. In Aus- tralian Standard AS17 Irradiation
of Food Products, food irradiation is prohibited
unless approved for a specific application and no
upper limits for irradiation doses are specified.
Permission is given on a case-by- case basis
(Stanley, 2000).

4.2. Wodified atmozpheve packaging and

hydvoztatic pvezzuve

MAP can be applied to the ready-to-eat products

after being cooked, chilled and portioned or sliced.
MAP extends shelf-life by delaying microbial spoilage
and oxidative chemical deterioration. Shaw (1997)
reviewed opportunities of MAP for cook-chill meals.
The UH governments Advisory Committee on the
Microbiological Safety of Foods (1995) identified the
risk of botulism from chilled vacuum and modified
atmosphere packaged foods.
Hydrostatic pressure can be applied to packaged
ready- to-eat refrigerated foods. The shelf-life of
smoked sal- mon cream inoculated with pathogens was
extended from 60 to 180 days at 3 or 8C by treatment
for 3 minutes at 700 MPa (Carpi, Gola, Maggi,
Rovere, & Buzzoni, 1995). The authors emphasised the
necessity to store the product at <8C to prevent
growth of spores of pro- teolytic C. botulinum.
Resistance of spores to high pres- sure (up to 1000
Mpa) can be overcome by a combination with other
preservation methods, such as mild heat treatment or
irradiation (Gould & Jones, 1989). To keep the
pressure moderate in order to preserve food quality,
Halchayanand, Sikes, Dunne, and Ray (1998)
suggested a combination of hydrostatic pressure,
pasteurisation and the addition of bacteriocins (nisin
A, pediocin AcH).

4.3. Acidz, zalt and zpicez

The ingredients of cook-chill foods with preservation

qualities can be a part of their safety design. Uong
and Chen (1988) graded salts of organic acids in
terms of eRectiveness to inhibit B. ceveuz spore
germination in the following order formate, lactate,
in inhibiting non-proteolytic C. botulinum (Stringer &
Peck, 1999). C. botulinum toxin was not produced in
sous vide spaghetti and meat sauce during 42 days
at 15C at pH 5 or salt concentration >1.5%
(Simpson et al., 1995). However, the majority of
extended shelf-life cook-chill meals have a pH close
to neutrality and low salt content. The recommended
sodium content of soups in hospital catering, for
example, is 390 mg]100 g or about 0.4% (NSU
Health Department, 1995).
Chemical preservatives do not enhance the fresh
image of cook-chill foods. Consumers would accept
natural antibacterial food constituents more readily.
Spice oils, for example, inhibited the growth of C.
botulinum (Ismael & Pierson, 1990a). Clove,
cinnamon, and origanum oils (150200 ppm) were
the most eRec- tive, garlic and onion the least (De
Uitt, Noter- mands, Gorin, & Hampelmacher, 1979;
Ismael, & Pierson, 1990b). The eRect was reversible
after the removal of spice oils, thus implying a
sporostatic nature of the eRect. Carvacrol, naturally
present in oregano and thyme, inhibited vegetative
cells of B. ceveuz (Ultee, Hets, & Smith, 1999). It
caused the depletion of the intracellular ATP pool
and the reduction of the mem- brane potential. In the
US carvacol is added to baked goods, non-alcoholic
beverages and chewing gum. At concentrations
above 1 mM it can be applied to rice, pasta, soups
and other products contaminated with B. ceveuz
spores. Horseradish distillate can be used on the
for B. ceveuz growth at 10C in sous vide chicken
breasts, which were injected with spores of B. ceveuz
prior to heat treatment. Although it enhanced
freshness, meat flavour and saltiness sensory scores
of sous vide chicken breast, it also resulted in more
yellow colour (Turner & Larick, 1996). Sodium lactate
aRected the sensorial quality of sous vide meals (Dr.
ir. T. Martens, Alma Sous Vide Competence Centre,
Leuven, Belgium).
4.5. Biopvezevration
The term biocontrol implies a natural means of
preservation. Bacteriocins and protective cultures are
the most common applications. The majority of
bacter- iocins retain their activity after mild heating. In
Aus- tralia, only nisin has been approved for use in
several commodities at levels between 10 mg]kg in
cream and 250 mg]kg in flour. Commercial
applications are limited due to high cost of nisin.
Scott and Taylor (1981b) demonstrated the diRerent
sensitivities of C. botulinum strains to nisin
(56A<69A<113B+213B<Beluga E<Minnesota E),
pH eRect (pH 6 was more eRective than pH 7 and 8)
and spore load (better inhibition of 10 2 than 103 or 104
cfu] ml). Pediocin AcH inhibited C. botulinum type E
but not types A and B (Ray, 1994). This bacteriocin
was anti- listerial at 2400 AU]g in chicken before and
after cook- ing (GoR, Bhunia, & Johnson, 1996),
which can protect the product from food-borne
surface of cooked meats to control post-cooking con-
tamination. At the concentration of 20 000 nl]l it was
inhibitory to Ezchevichia coli O157H7, L. mono-
cytogenez, Salmonella typhimuvium, Staphylococcuz
auv- euz, Sevvatia gvimezii and Lactobacilluz zake on
roast beef at 12C (Uard, Delaquis, Hallay, & Mazza,
1998). Such substances can be used as tools in
constructing preservation systems by the combination
of gentle stresses at the concentrations below
sensorial threshold (Alzamora, 1998).
4.4. Sodium lactate
Sodium lactate is an approved additive and
eRective against spore-formers. It delays the C.
botulinum tox- igenesis in sous vide foods. A
combination of 0.25% diacetate and 1.5% lactate
prevented the spoilage of cooked-in-the-bag
refrigerated turkey by Clostridium species during 22
weeks at 4C (Mayer, Luchanski, & Cerveny, 1995).
The addition of sodium lactate at 1.8 4.8% delayed
toxigenesis by C. botulinum at 1216C in sous vide
beef, chicken and salmon (Meng & Geni- georgis,
1994). The lowering of storage temperature to 4C
enhanced the inhibitory eRect.
Simpson (1994) confirmed the inhibition of C. botuli-
num type E spores with sodium lactate, but to a
lesser degree than with NaCl. Turner, Foegeding,
Larich, and Murphy (1996) did not find sodium
lactate inhibitory
illnesses caused by post- processing re-contamination
and]or under-cooking.
The eRect of bacteriocins diminishes in food
systems in comparison with an experimental
microbiological medium. Uneven distribution]diRusion
throughout the product and partial inactivation by food
constituents and enzymes of resistant microorganisms
are contribut- ing factors (Mossel et al., 1991).
Biocontrol by protective cultures allows a tempera-
ture-responsive inhibitory eRect antibacterial sub-
stances are produced only when temperature abuse
takes place. The examples are inhibition of L. mono-
cytogenez in sous vide beef by L. baravicuz
(Uinkowski, Crandall & Montville, 1993) and of a range
of pathogens in sous vide fish by Entevococcuz
faecium (Embarek, Jeppesen & Huss, 1994). The
mechanism of antibiosis varies. Lactococcuz lactiz
inhibited C. botulinum in chicken a la king by a
bacteriocin production and L. delbvueckii subsp.
bulgavicuz by hydrogen peroxide (Saleh & Ordal,
1955), non-bacteriocin producing L. plantavum ATCC
8014 by pH reduction of refri- gerated pea soup
(Skinner, Solomon, & Fingerhut, 1999). Loss of the
inhibitory eRect makes the application of
biopreservation less reliable spontaneous resistance of
B. ceveuz to nisin (Stiles, 1996); acquired resistance of L.
monocytogenez to the pediocin based preparation
ALTA 2341 (Szabo & Cahill, 1998); and the loss of
bac- teriocin producing ability by old cultures of
Entevococcuz
(Embarek et al., 1994). The majority of reported
results were obtained in microbiological media rather
than food systems. Food composition and structure
can aRect the rate of growth of protective cultures,
rate of production of inhibitory substances and their
biological activity. The majority of protective cultures
are lactic acid bacteria derived from fermented
foods. However, in Australia the addition of those
cultures to non-fer- mented products would require a
new standard. The uncertainty in the eRectiveness
of inhibition, heat sensi- tivity of the cultures and their
cost are the limitations of this approach.
5. Conslusions
Sous-vide foods rely heavily on temperature
control (refrigeration) and often do not have built in
safety margins in case of a break down in the cold
chain. Absence of visual indicators of temperature
abuse exacerbates the hazard. Potential safety risks
remain a restraining factor for wider acceptance of
the cook-chill technology. Furthermore,
manufactures are often faced with a dilemma
between applying suAcient heat treat- ment and
preserving quality of heat sensitive ingre- dients,
such as eggs, cheese, poultry, etc. A combination of
subtle inhibitory factors can be a potential solution.
The choice of an approach depends on suAcient
sci- entific information, eRect on the products
quality, availability of application techniques, costs,
legislative and marketing considerations. The majority
of the described preservation methods are novel and
only a few have been applied commercially in
Australia. Con- sequently, their legal status has not
been established.
Double heating, irradiation, addition of lactate, salt
and pH lowering are either aRecting the product sen-
sorial]structural]nutritional quality or perceived as
unnatural by the consumers. MAP and hydrostatic
pressure are not eRective against spore-formers. The
reliance on natural antimicrobial substances is limited
to specific foods. Bacteriocins and protective cultures
do not have the above-mentioned disadvantages;
however, the loss of the inhibitory eRect and lack of
practical applications require further research in this
field.
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