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Food Research International 34 (2001) 449455


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

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 2. Pathogens of signifisanse
majority of large scale food services are also using
cook- chill technology and often produce tonnes of Traditional cook-chill foods can support growth of
product at a time. Lack of expertise by craft-based any psychrotrophic aerobic pathogen surviving
small manu- facturers and food services, economical cooking (spore-formers) or re-contaminating during
and logistical pressures to extend shelf-life, necessity chilling and storage. At 3C the lag phase of the
for chilled dis- tribution and potential temperature majority of non- spore forming psychrotrophic
abuse by consumers contribute to food safety pathogenic bacteria, such as L. monocytogenez, is
hazards. about a week with 20 h genera- tion time afterwards
There is no internationally recognised classification (Mossel & Struijk, 1991). Conse- quently, a product
concerning cook-chill foods. Project Harmony contaminated with 10 cfu]g of L. monocytogenez, for
(www.harmony.alma.ac.be), one of the initiatives of example, can accumulate 103 cfu]g within 2 weeks of
the Food Linked Agro-Industrial Research European storage, which is an infective dose for immuno-
Commission, provides an inventory of the European competent people (Sutherland & Porritt, 1997). Thus,
legislation in order to bring uniformity. The Australian hygienic practices, destruction of vegetative
codes (NSU Health Department, 1998a, b) distinguish pathogens during cooking, low storage temperature
two types of cook-chill systems traditional or open and limited shelf life are the controlling factors.
tray (5 days shelf-life) and extended shelf-life or sous Packaging protects new generation cook-chill foods
vide (28 days shelf-life). They specify heat treatment such as sous vide (cooked in a bag) from re-
equivalent to 6D reduction of Liztevia monocytogenez contamina- tion after cooking. Spores of following
for both systems. The justification for 28 days shelf- pathogens can survive mild heat treatment given to
life limit was that non-proteolytic strains of these products
1. Psychrotrophic non-proteolytic C. botulinum
(D80 C=21.6 min, z=7 C) grows at 3C (Graham,
* Tel. +61-2-4570-1339; fax +61-2-4570-1579. Mason, & Peck, 1996)
E-mail addvezz s.rodgers@uws.edu.au
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) 3
2. Bacilluz ceveuz (D100 C=2.73.1 min, z=6.1C) Nguyen-The (1999) did not detect B. ceveuz in
grows at >4C (van Netten, van de Moosdijk, van commer- cial courgette puree at 4C.
de Hoensel, Mossel, & Perales, 1990)
3. Proteolytic C. botulinum (D121.1 C=0.30.23
min, 3. Whermal preserration prinsiples
z=10C) grows at > 10C (Smelt & Haas, 1978)
4. Cloztvidium pevfvingenz The preservation principals of sous vide foods are
(D98 C=2131 min, presented in Fig. 1. Shelf stable foods are heated to
z=3.8C) grows at >15C (Snyder, 1995) 121C for 3 min or equivalent (botulinum cook), which
is similar in lethality to conventional canning. The
L. monocytogenez can grow at refrigeration examples of such products are ready-to-eat sauces
tempera- tures (Grau, 1996). However, mild heating and legume-based dishes in plastic pouches. The
such as 2 min at 70C or equivalent is suAcient to majority of meals, however, would be grossly
achieve 6D reduc- tion of this pathogen (Gaze, overcooked and taste similar to canned foods. Even
Brown, & Banks, 1989). Major breach of Good milder heating necessary to achieve 6D reduction of
Manufacturing Practices such as under- non-proteolytic C. botulinum requires 2545 min at
processing]post-process contamination is needed for L. 70C (Fernandez & Peck, 1997) and storage at <10 C
monocytogenez to survive]contaminate these pro- the growth threshold of pro- teolytic C. botulinum
ducts and gross temperature abuse during storage (Smelt et al., 1978). This tempera- ture should be
for lowered to 4C if a suAcient amount of air is left in the
C. pevfvingenz and proteolytic C. botulinum to multiply. package allowing B. ceveuz to grow (van Netten et
The growth of C. botulinum is considered the major al., 1990).
potential safety risk for refrigerated pasteurised foods It is desirable for a preservation system to be based
(Mossel et al., 1991; Notermans, Dufrenne, & Lund, on more than one controlling factor. The majority of
1990; Simunovic, Oblinger, & Adams, 1985). A number sous vide foods rely solely on temperature control.
of studies have demonstrated its ability to produce The brea- ches in the cold chain are a regular
toxin in sous vide foods (Betts & Gaze, 1995; Brown & occurrence in real life situations. Temperatures above
Gaze, 1990; Brown, Gaze, & Gaskell, 1991; Cockey & 7C were common for the refrigerated display cases of
Tatro, 1974; Simpson, Smith, Dodds, Ramaswamy, convenience stores (Hut- ton, Chehak, & Hanlin, 1991).
Blanch- field, & Simpson, 1995). Control of B. ceveuz, At 8C non-proteolytic
another pathogen of significance, also relies on
storage tem- perature. Carlin, Guinebretiere, Choma,
Schmott, and
4 S. Rybka-Rodgevz ] Yood Rezeavch Intevnational 34 (2001)
Fig. 1. Application of the Hurdle Principle to sous-vide foods.
C. botulinum produced toxin within 3 weeks (Conner, 4.1. Ivvadiation
Scott, Bernard, & Hautter, 1989). Storage
temperature had the greatest eRect on a sous vide Irradiation is an additive-free preservation method
products micro- bial load with the initial microflora and equivalent or superior to thermal processing from
and processing temperature being secondary factors a nutritional viewpoint (Shamsuzzaman, Lucht, &
(Hansen & Hno- chel, 1996). The European Chilled Chuaqui-ORermans, 1995; Thayer, Boyd, Him, Fox, &
Food Federation Botulism Uorking Party stated the Farrell, 1998). It can increase the heat sensitivity of
need for addi- tional eRective preservation factors for pathogens (Grant & Patterson, 1995) and be an addi-
sous vide foods, in which at least a 6D reduction of tional barrier for cooked and irradiated in a bag
non-proteolytic C. botulinum cannot be guaranteed products. Spore-former B. ceveuz was sensitive to
(Gould, 1999). radiation (D10=0.1260.288 kGy) in a roast beef meal
(Grant & Patterson, 1992).
FAO]IAEA]UHO recommends the use of high dose
4. Improring extended shelf-life sook-shill foods irradiation (>10 kGy) for preparation of sterilised
safety meals for hospitalised patients. Non-proteolytic
strains of C. botulinum are only slightly less resistant
An improved safety design of a product allows to irradia- tion in comparison with proteolytic types
exten- sion of its shelf-life and]or reduction of severity (Him & Foe- geding, 1992). Thus, vegetative
of its processing. First attempts to destroy spore- pathogens rather than spore-formers would be the
forming microflora were made by the modification of target for low dose irradia- tion of mildly processed
the Nacha System (Bjorkman & Delphine, 1966). The refrigerated ready-to-eat foods. The shelf-life of sous
cooked-in-a- bag product was chilled to 20C to vide chicken breasts heated to 71C was extended
initiate spore germi- nation, incubated at room from 2 to 58 weeks at 8C by irradiation levels of
temperature for four hours and then pasteurised at 18 kGy (Shamsuzzaman, Chuaqui- ORermans,
8590oC to kill sporulated vegetative cells. Such Lucht, Mcdougall, & Borsa, 1992). The inhibition of L.
double heating resulted in overcooking and a tired monocytogenez increased with the rise in irradiation
flavour. Since then a number of additional pre- level and diminished after the fourth week of storage.
servation hurdles have been applied to cook-chill Thayer et al. (1998) demonstrated that the
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 Disadvantage Reference

Additional heating ERectively sterile food Inferior quality Bjorkman and Delphine (1966)
Irradiation Possibility of treatment within Consumer resistance; capital cost; special Shamsuzzaman et al. (1995)
packaging packaging Grant et al. (1995), Thayer et al.
not excessive nutrient loss (1998)
MAP Inhibits oxidation and microbial No eRect on pathogens Shaw (1997)
Hydrostatic pressure Possibility of treatment within Spore resistance; possible eRect on Carpi et al. (1995)
packaging structure of foods

Chemical Simpson et al. (1995), Ismael et

pH, salt and spices Low cost Impact on sensory characteristics al. (1990 a, 1990b), Ultee et al.
and nutritional requirements (1999), Uard et al. (1998)

Lactate Heat stable; eRective ARects sensorial quality Meng et al. (1994), Simpson
against spore-formers Failed to inhibit B. (1994), Turner et al. (1996)
(including ceveuz
C. botulinum)

Biological Acquired resistance by pathogens; Szabo et al. (1998), Mazzotta,

Bacteriocins Many are heat stable; eRective inconsistency of the inhibitory eRect; Crandall and Montville (1997),
against spore-formers (including decomposing during storage Scott and Taylor (1981a), Uong
C. botulinum) et al. (1988), Mossel and Struijk
Cost]handling of cultures; heat Tanaka, Meske, Doyle, Traisman,
Protective cultures Responsive to temperature change; sensitivity; loss of bacteriocin producing Thayer and Johnson (1985),
eRective against spore-formers ability Crandall, Uinkowski and Montville
(including C. botulinum) (1994), Embarek et al. (1994),
Potential probiotic eRect Turner et al. (1996), Dave and Shah
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 & surface of cooked meats to control post-cooking con-
Peck, 1999). C. botulinum toxin was not produced in tamination. At the concentration of 20 000 nl]l it was
sous vide spaghetti and meat sauce during 42 days inhibitory to Ezchevichia coli O157H7, L. mono-
at 15C at pH 5 or salt concentration >1.5% cytogenez, Salmonella typhimuvium, Staphylococcuz
(Simpson et al., 1995). However, the majority of auv- euz, Sevvatia gvimezii and Lactobacilluz zake on
extended shelf-life cook-chill meals have a pH close roast beef at 12C (Uard, Delaquis, Hallay, & Mazza,
to neutrality and low salt content. The recommended 1998). Such substances can be used as tools in
sodium content of soups in hospital catering, for constructing preservation systems by the combination
example, is 390 mg]100 g or about 0.4% (NSU of gentle stresses at the concentrations below
Health Department, 1995). sensorial threshold (Alzamora, 1998).
Chemical preservatives do not enhance the fresh
image of cook-chill foods. Consumers would accept 4.4. Sodium lactate
natural antibacterial food constituents more readily.
Spice oils, for example, inhibited the growth of C. Sodium lactate is an approved additive and
botulinum (Ismael & Pierson, 1990a). Clove, eRective against spore-formers. It delays the C.
cinnamon, and origanum oils (150200 ppm) were botulinum tox- igenesis in sous vide foods. A
the most eRec- tive, garlic and onion the least (De combination of 0.25% diacetate and 1.5% lactate
Uitt, Noter- mands, Gorin, & Hampelmacher, 1979; prevented the spoilage of cooked-in-the-bag
Ismael, & Pierson, 1990b). The eRect was reversible refrigerated turkey by Clostridium species during 22
after the removal of spice oils, thus implying a weeks at 4C (Mayer, Luchanski, & Cerveny, 1995).
sporostatic nature of the eRect. Carvacrol, naturally The addition of sodium lactate at 1.8 4.8% delayed
present in oregano and thyme, inhibited vegetative toxigenesis by C. botulinum at 1216C in sous vide
cells of B. ceveuz (Ultee, Hets, & Smith, 1999). It beef, chicken and salmon (Meng & Geni- georgis,
caused the depletion of the intracellular ATP pool 1994). The lowering of storage temperature to 4C
and the reduction of the mem- brane potential. In the enhanced the inhibitory eRect.
US carvacol is added to baked goods, non-alcoholic Simpson (1994) confirmed the inhibition of C. botuli-
beverages and chewing gum. At concentrations num type E spores with sodium lactate, but to a
above 1 mM it can be applied to rice, pasta, soups lesser degree than with NaCl. Turner, Foegeding,
and other products contaminated with B. ceveuz Larich, and Murphy (1996) did not find sodium
spores. Horseradish distillate can be used on the lactate inhibitory
illnesses caused by post- processing re-contamination
for B. ceveuz growth at 10C in sous vide chicken and]or under-cooking.
breasts, which were injected with spores of B. ceveuz The eRect of bacteriocins diminishes in food
prior to heat treatment. Although it enhanced systems in comparison with an experimental
freshness, meat flavour and saltiness sensory scores microbiological medium. Uneven distribution]diRusion
of sous vide chicken breast, it also resulted in more throughout the product and partial inactivation by food
yellow colour (Turner & Larick, 1996). Sodium lactate constituents and enzymes of resistant microorganisms
aRected the sensorial quality of sous vide meals (Dr. are contribut- ing factors (Mossel et al., 1991).
ir. T. Martens, Alma Sous Vide Competence Centre, Biocontrol by protective cultures allows a tempera-
Leuven, Belgium). ture-responsive inhibitory eRect antibacterial sub-
stances are produced only when temperature abuse
4.5. Biopvezevration takes place. The examples are inhibition of L. mono-
cytogenez in sous vide beef by L. baravicuz
The term biocontrol implies a natural means of (Uinkowski, Crandall & Montville, 1993) and of a range
preservation. Bacteriocins and protective cultures are of pathogens in sous vide fish by Entevococcuz
the most common applications. The majority of faecium (Embarek, Jeppesen & Huss, 1994). The
bacter- iocins retain their activity after mild heating. In mechanism of antibiosis varies. Lactococcuz lactiz
Aus- tralia, only nisin has been approved for use in inhibited C. botulinum in chicken a la king by a
several commodities at levels between 10 mg]kg in bacteriocin production and L. delbvueckii subsp.
cream and 250 mg]kg in flour. Commercial bulgavicuz by hydrogen peroxide (Saleh & Ordal,
applications are limited due to high cost of nisin. 1955), non-bacteriocin producing L. plantavum ATCC
Scott and Taylor (1981b) demonstrated the diRerent 8014 by pH reduction of refri- gerated pea soup
sensitivities of C. botulinum strains to nisin (Skinner, Solomon, & Fingerhut, 1999). Loss of the
(56A<69A<113B+213B<Beluga E<Minnesota E), inhibitory eRect makes the application of
pH eRect (pH 6 was more eRective than pH 7 and 8) biopreservation less reliable spontaneous resistance of
and spore load (better inhibition of 10 2 than 103 or 104 B. ceveuz to nisin (Stiles, 1996); acquired resistance of L.
cfu] ml). Pediocin AcH inhibited C. botulinum type E monocytogenez to the pediocin based preparation
but not types A and B (Ray, 1994). This bacteriocin ALTA 2341 (Szabo & Cahill, 1998); and the loss of
was anti- listerial at 2400 AU]g in chicken before and bac- teriocin producing ability by old cultures of
after cook- ing (GoR, Bhunia, & Johnson, 1996), Entevococcuz
which can protect the product from food-borne
(Embarek et al., 1994). The majority of reported quality, availability of application techniques, costs,
results were obtained in microbiological media rather legislative and marketing considerations. The majority
than food systems. Food composition and structure of the described preservation methods are novel and
can aRect the rate of growth of protective cultures, only a few have been applied commercially in
rate of production of inhibitory substances and their Australia. Con- sequently, their legal status has not
biological activity. The majority of protective cultures been established.
are lactic acid bacteria derived from fermented Double heating, irradiation, addition of lactate, salt
foods. However, in Australia the addition of those and pH lowering are either aRecting the product sen-
cultures to non-fer- mented products would require a sorial]structural]nutritional quality or perceived as
new standard. The uncertainty in the eRectiveness unnatural by the consumers. MAP and hydrostatic
of inhibition, heat sensi- tivity of the cultures and their pressure are not eRective against spore-formers. The
cost are the limitations of this approach. reliance on natural antimicrobial substances is limited
to specific foods. Bacteriocins and protective cultures
do not have the above-mentioned disadvantages;
5. Conslusions however, the loss of the inhibitory eRect and lack of
practical applications require further research in this
Sous-vide foods rely heavily on temperature field.
control (refrigeration) and often do not have built in
safety margins in case of a break down in the cold Referenses
chain. Absence of visual indicators of temperature
Advisory Committee on the Microbiological Safety of Food (1995)
abuse exacerbates the hazard. Potential safety risks
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