16
Modified atmosphere packaging (MAP)
F. Devlieghere, Ghent University; M. I. Gil, CEBAS-CSIC,
Spain; and J. Debevere, Ghent University
16.1 Introduction
Modified atmosphere packaging (MAP) may be defined as ‘the enclosure of food
products in gas-barrier materials, in which the gaseous environment has been
changed’ (Young et al, 1988). Because of its substantial shelf-life extending
effect, MAP has been one of the most significant and innovative growth areas in
retail food packaging over the past two decades. The potential advantages and
disadvantages of MAP have been presented by both Farber (1991) and Parry
(1993), and summarised by Davies (1995) in Table 16.1.
There is considerable information available regarding suitable gas mixtures
for different food products. However, there is still a lack of scientific detail
regarding many aspects relating to MAP. These include:
? Mechanism of action of carbon dioxide (CO
2)
on microorganisms.
? Safety of MAP packaged food products.
? Interactive effects of MAP and other preservation methods.
? The influence of CO
2
on the microbial ecology of a food product.
? The effect of MAP on the nutrional quality of packaged food products.
16.2 Principles of MAP
16.2.1 General principles
Modified atmosphere packaging can be defined as packaging a product in an
atmosphere that is different from air. This atmosphere can be altered in four
different ways:
1. Vacuum packaging.
2. Passive MAP.
3. Introduction of a gas at the moment of packaging.
4. Active packaging. In passive MAP, the modified atmosphere is created
by the packaged commodity that continues its respiration after packaging.
Active packaging systems alter the atmosphere using packaging materials
or inserts absorbing and/or generating gases. Typical examples are oxygen
absorbers and CO
2
emitting films or sachets.
The gases that are applied in MAP today are basically O
2
, CO
2
and N
2
. The
last has no specific preservative effect but functions mainly as a filler gas to avoid
the collapse that takes place when CO
2
dissolves in the food product. The func-
tions of CO
2
and O
2
will be discussed in more detail.
16.2.2 Carbon dioxide as anti-microbial gas
CO
2
, because of its antimicrobial activity, is the most important component in
applied gas mixtures. When CO
2
is introduced into the package, it is partly dis-
solved in the water phase and the fat phase of the food. This results, after equi-
librium, in a certain concentration of dissolved CO
2
([CO
2
]
diss
) in the water phase
of the product. Devlieghere et al (1998) have demonstrated that the growth
Modified atmosphere packaging (MAP) 343
Table 16.1 The potential positive and negative effects MAP has on the food industry
Benefits Disadvantages
1. Product A centralised packaging system Increased package volume, adds to
packaging incorporating portion control the transport costs and affects
Clear, all-round visibility of the area required for retail display
product, improving its Benefits are lost when the
presentation characteristics package leaks or is opened
2. Product Overall product quality is high Product safety has not yet been
quality Sliced products are much easier fully established
to separate
Shelf life increases by 50–400%
3. Special Use of chemical preservatives Temperature control is essential
features can be reduced or Different products require their
discontinued own specific gas formulation
Speciality equipment and
associated training is required
4. Economics Improved shelf life decreases Increased costs
financial losses
Distribution costs are reduced
due to fewer deliveries being
necessary over long distances
after Davies, 1995.
inhibition of microorganisms in modified atmospheres is determined by the con-
centration of dissolved CO
2
in the water phase.
The effect of the gaseous environment on microorganisms in foods is not as
well understood by microbiologists and food technologists as are other external
factors, such as pH and a
w
. Despite numerous reports of the effects of CO
2
on microbial growth and metabolism, the ‘mechanism’ of CO
2
inhibition still
remains unclear (Dixon and Kell, 1989; Day, 2000). The question of whether any
specific metabolic pathway or cellular activity is critically sensitive to CO
2
inhi-
bition has been examined by several workers. The different proposed mechanisms
of action are:
1. Lowering the pH of the food.
2. Cellular penetration followed by a decrease in the cytoplasmic pH of the cell.
3. Specific actions on cytoplasmic enzymes.
4. Specific actions on biological membranes.
When gaseous CO
2
is applied to a biological tissue, it first dissolves in the
liquid phase, where hydration and dissociation lead to a rapid pH decrease in the
tissue. This drop in pH, which depends on the buffering capacity of the medium
(Dixon and Kell, 1989), is not large in food products. In fact, the pH drop in
cooked meat products only amounted to 0.3 pH units when 80% of CO
2
was
applied in the gas phase with a gas/product volume ratio of 4 :1 (Devlieghere et
al, 2000b). Several studies have proved that the observed inhibitory effects of
CO
2
could not solely be explained by the acidification of the substrate (Becker,
1933; Coyne, 1933).
Many researchers have documented the rapidity with which CO
2
in solution
penetrates into the cell. Krogh (1919) discovered that this rate is 30 times faster
than for oxygen (O
2
), under most circumstances. Wolfe (1980) suggested the
inhibitory effects of CO
2
are the result of internal acidification of the cytoplasm.
Eklund (1984) supported this idea by pointing out that the growth inhibition of
four bacteria obtained with CO
2
had the same general form as that obtained with
weak organic acids (chemical preservatives), such as sorbic and benzoic acid. Tan
and Gill (1982) also found that the intracellular pH of Pseudomonas fluorescens
fell by approximately 0.03 units for each 1 mM rise in extracellular CO
2
concentration.
CO
2
may also exert its influence upon a cell by affecting the rate at which
particular enzymatic reactions proceed. One way this may be brought about is to
cause an alteration in the production of a specific enzyme, or enzymes, via induc-
tion or repression of enzyme synthesis (Dixon, 1988; Dixon and Kell, 1989;
Jones, 1989). It was also suggested (Jones and Greenfield, 1982; Dixon and Kell,
1989) that the primary sites where CO
2
exerts its effects are the enzymatic car-
boxylation and decarboxylation reactions, although inhibition of other enzymes
has also been reported (Jones and Greenfield, 1982).
Another possible factor contributing to the growth-inhibitory effect of CO
2
could be an alteration of the membrane properties (Daniels et al, 1985; Dixon
and Kell, 1989). It was suggested that CO
2
interacts with lipids in the cell mem-
344 The nutrition handbook for food processors
brane, decreasing the ability of the cell wall to uptake various ions. Moreover,
perturbations in membrane fluidity, caused by the disordering of the lipid bilayer,
are postulated to alter the function of membrane proteins (Chin et al, 1976; Roth,
1980).
Studies examining the effect of a CO
2
enriched atmosphere on the growth of
microorganisms are often difficult to compare because of the lack of information
regarding the packaging configurations applied. The gas/product volume ratio and
the permeability of the applied film for O
2
and CO
2
will influence the amount
of dissolved CO
2
and thus the microbial inhibition of the atmosphere. For this
reason, the concentration of dissolved CO
2
in the aqueous phase of the food
should always be measured and mentioned in publications concerning MAP
(Devlieghere et al, 1998).
Only a few publications deal with the effect of MAP on specific spoilage
microorganisms. Gill and Tan (1980) compared the effect of CO
2
on the growth
of some fresh meat spoilage bacteria at 30 °C. Molin (1983) determined the resis-
tance to CO
2
of several food spoilage bacteria. Boskou and Debevere (1997;1998)
investigated the effect of CO
2
on the growth and trimethylamine production
of Shewanella putrifaciens in marine fish, and Devlieghere and Debevere (2000)
compared the sensitivity for dissolved CO
2
of different spoilage bacteria at 7 °C.
In general, Gram-negative microorganisms such as Pseudomonas, Shewanella
and Aeromonas are very sensitive to CO
2
. Gram-positive bacteria show less sen-
sitivity and lactic acid bacteria are the most resistant. Most yeasts and moulds
are also sensitive to CO
2
. The effect of CO
2
on psychrotrophic food pathogens is
discussed in section 16.5.
16.3 The use of oxygen in MAP
16.3.1 Colour retention in fresh meat products
The colour of fresh meat is determined by the condition of myoglobin in the meat.
When an anaerobic atmosphere is applied, myoglobin (purplish-red) will be trans-
formed to metmyoglobin, producing a brown colour, which is an undesirable trait
for European consumers. It is therefore essential that O
2
is included (e.g. 40%)
into the applied gas atmosphere when fresh meat, destined for the consumer, is
packaged. This will ensure the myoglobin is oxygenated, resulting in an attrac-
tive bright red colour. However, by doing this, the microbial shelf life of the pack-
aged meat is decreased compared with meat that is packaged in an O
2
free
atmosphere.
16.3.2 Inhibition of the reduction of trimethylamineoxide (TMAO)
in marine fish
Marine fish contain TMAO, which is an osmo-regulator. In O
2
poor conditions
(e.g. when stored in ice), TMAO is used by spoilage organisms (e.g. Shewanella
putrifaciens) as a terminal electron-acceptor, and is reduced to trimethylamine
Modified atmosphere packaging (MAP) 345
(TMA). TMA is the main active component responsible for the unpleasant ‘fishy’
odour. However, by introducing high levels of O
2
in the gas atmosphere, the
TMAO-reduction can be retarded, and consequently the shelf-life of the fish is
increased . This was clearly demonstrated by Boskou and Debevere (1997, 1998).
Therefore, packaging atmospheres for lean marine fish should contain oxygen
levels of at least 30%.
16.3.3 Avoiding anaerobic respiration of fresh produce
When fresh produce is packaged in a closed packaging system, it continues to
respire. It is of great importance to avoid anaerobic conditions in the package of
fresh produce because anaerobic respiration of the plant tissue will result in the
production of off-odour compounds such as ethanol and acetaldehyde. The tech-
niques applied to maintain an aerobic atmosphere in the packaging of fresh
produce are discussed in detail in section 16.4.2.
16.4 Applications of MAP in the food industry
16.4.1 Non-respiring products
Non-respiring food products do not consume any oxygen during further storage.
When such food products are packaged in a modified atmosphere, the aim is
to retain the introduced atmosphere during the storage period. Therefore, high
barrier films are used which are most often composed out of different layers
of materials. Typical O
2
and CO
2
barrier materials are PA (polyamide), PVDC
(polyvinylidenechloride) and EVOH (ethylenevinyl alcohol). Depending on the
intended storage time, the O
2
-permeability of the applied films should be <2ml
O
2
/m
2
.24h.atm determined at 75% relative humidity at 23 °C for products with a
long shelf life and <10 ml O
2
/m
2
.24h.atm determined at the same conditions for
products with a limited shelf life (<1 week).
One of the bottlenecks in modified atmosphere packaging lies in defining the
optimal gas atmosphere for a food product in a specific packaging design. This
optimal atmosphere depends on the intrinsic parameters of the food product (pH,
water activity, fat content, type of fat) and the gas/product volume ratio in the
chosen package type. The intrinsic parameters determine the sensitivity of the
product for specific microbial, chemical and enzymatic degradation reactions.
Products that are susceptible to microbial spoilage due to the development of
Gram-negative bacteria (e.g. fresh meat and fish) and yeasts (salads) should
be packaged in a CO
2
enriched atmosphere because the growth of those micro-
organisms is significantly retarded by CO
2
. In general, oxygen is excluded from
the gas mixture. For prolonging the shelf life of products which are spoiled by
mould growth (e.g. hard cheeses) or by oxidation, it is essential to package in O
2
free atmospheres. In some cases, O
2
will be included for the reasons previously
mentioned in section 16.3.
The use of CO
2
is however limited due to its solubility in water and fat. This
346 The nutrition handbook for food processors
high solubility can cause collapsing of the package when the concentrations of
CO
2
are too high. This will especially be the case for food products containing
high amounts of unsaturated fat such as smoked salmon and salads that contain
mayonnaise. The influence of pH, temperature, fat content, water activity and
gas/product ratio on the CO
2
solubility has been quantified by Devlieghere et al
(1998). Moreover, too high CO
2
concentrations in the atmosphere can lead to an
increased drip loss during storage. This can be explained by the pH drop induced
by CO
2
dissolving in the water phase of the product, causing a decrease in the
water binding capacity of the proteins. Table 16.2 gives an overview of the rec-
ommended gas regimes for different non-respiring food products and the specific
purpose of the gas mixture.
16.4.2 Respiring products (Equilibrium Modified Atmosphere Packaging)
In contrast to other types of food, fruits and vegetables continue to respire actively
after harvesting. A packaging technology, used for prolonging the shelf life of
respiring products, is Equilibrium Modified Atmosphere Packaging (EMAP).
The air around the commodity is replaced by a gas combination of 1–5% O
2
and
3–10% CO
2
with the balance made up of N
2
. Inside the package, an equilibrium
becomes established, when the O
2
transmission rate (OTR) of the packaging film
is matched by the O
2
consumption rate of the packaged commodity. The respira-
tion of the living plant tissue also results in the production of CO
2
, which dif-
fuses through the packaging film, depending on the film’s CO
2
transmission rate
Modified atmosphere packaging (MAP) 347
Table 16.2 Recommended gas regimes for MAP of various non-respiring foods
Food type
Gas composition (%)
Purpose
CO
2
N
2
O
2
Fresh meat
retail 15–40 0 60–85 ′ Gram
-
organisms (CO
2
) &
20 10 70 Colour (O
2
)
industrial packages 50–100 0–50 0 ′ Gram
-
organisms
Poultry 70 20 10 ′ Gram
-
, colour
Fish
lean, marine 50–60 0–20 30–40 ′ Gram
-
, ′ TMA production
fatty or fresh water 40–65 35–60 0 ′ Gram
-
, ′ oxidation
Meat and fish products
a
w
> 0.94 50–70 30–50 0 ′ Gram
+
a
w
< 0.94 10–20 80–90 0 ′ Yeasts and moulds
Shrimps 35 65 ′ Gram
-
& Gram
+
Cheese
hard 0–70 0–30 0
0 100 0 ′ Moulds, ′ oxidation
soft 0 100 0
Bakery products 20–70 30–80 0 ′ Yeasts & moulds
Dry products (a
w
< 0.60) 0 100 0 ′ Oxidation
(CO
2
TR). The type of packaging film selected is based on the film OTR and
CO
2
TR, which is required to obtain a desirable equilibrium modified atmosphere.
For packaging fruits, the film also needs to have a certain permeability for
ethylene (C
2
H
4
), which prevents an accumulation of the ripening hormone and
prolongs fruit shelf life (Kader et al, 1989).
The modified atmosphere not only reduces the respiration rate and the ripen-
ing behaviour of fruit, but it also maintains the general structure and turgidity of
the plant tissue for a much longer period, which results in better protection against
microbial invasion. This atmosphere is also thought to inhibit the growth of
spoilage microorganisms (Farber, 1991), which is mostly due to the low O
2
con-
centration, because the elevated CO
2
concentration (<10%) inside the package is
not sufficiently high enough to act as an antimicrobial (Bennik et al, 1998). The
shelf life is also prolonged by the suppression of the enzymatic browning reac-
tions on cut surfaces (Kader et al, 1989, Jacxsens et al, 1999a).
Regarding the relatively short shelf life of fruits, raw vegetables, and fresh-
cut vegetables, an active modification of the atmosphere is preferred, compared
to a passive modification, which is caused by the produce respiring. Form-Fill-
Seal (FFS) machines are used with a flushing system to obtain the optimal mod-
ified atmosphere for packaging this type of product.
The attained EMAs are influenced by produce respiration (which in turn is
affected by product type, temperature, variety, size, maturity, and processing
method), packaging film permeability (OTR, CO
2
TR, and C
2
H
4
TR), package
dimensions, and fill weight. Consequently, it is a very complex procedure
to establish an optimal EMA for different items of produce. The current knowl-
edge of EMAP of fruits and vegetables is mainly empirical, but a systematic ap-
proach for designing optimal EMA packages for minimally processed fruits and
vegetables is proposed by a number of different authors (Exama et al, 1993;
Peppelenbos, 1996; Jacxsens et al, 1999b; Jacxsens et al, 2000). Several mathe-
matical models have been published that predict the OTR and CO
2
TR of the pack-
aging film, which is necessary to obtain the desired equilibrium gas atmosphere
(Mannaperuma and Singh, 1994; Solomos, 1994; and Talasila et al, 1995).
However, in these models an unrealistic constant storage temperature is assumed.
Two important parameters in EMAP of fresh-cut produce, respiration rate and
permeability of the packaging film are temperature dependent. The respiration
rate is less affected by the temperature change (Q
10
R
= 2–3) than is the perme-
ability of the packaging film (Q
10
P
= 1–2) (Exama et al, 1993; Jacxsens et al,
2000), as is illustrated in Fig. 16.1.
When temperature increases, a larger volume of O
2
will be consumed by the
fresh-cut produce than is diffused through the packaging film, resulting in a shift
of the EMA towards an anaerobic atmosphere (<1% O
2
and >10% CO
2
). Anaer-
obic atmospheres must be avoided in EMAP of respiring products because the
shift towards anaerobic respiration will cause the formation of ethanol, acetal-
dehyde, off-flavours, and off-odours. At lower temperatures, the O
2
level will
increase (>5%) in the EMA package and the benefits of EMA are lost. Changing
temperatures during the transport, distribution, or storage of EMA packages will
348 The nutrition handbook for food processors
result in an equilibrium O
2
level inside the packages that differs from the optimal
3%. A lack of OTR and CO
2
TR of commercial films adapted to the needs of
middle and high respiring products can result in undesirable anaerobic atmos-
pheres. When both gas fluxes cannot be matched, the O
2
flux should take prior-
ity because it is the limiting factor in EMA packaging. A decreased O
2
content is
more effective in inhibiting respiration rate and decay than is a decreased CO
2
concentration (Kader et al, 1989; Bennik et al, 1995). New types of packaging
films, with an OTR that is adaptable to the needs of fresh cut packaged produce,
offer new possibilities in replacing OPP (oriented polypropylene), BOPP (biaxi-
ally oriented polypropylene), or LDPE (low density polyethylene) that are cur-
rently used in the industry and from which the OTR is not high enough for
packaging products with medium or high respiration rates (Exama et al, 1993).
Jacxsens et al (2000) proposed an integrated model in which the design of an
optimal EMA package for fresh-cut produce and fruits is possible, taking into
consideration the changing temperatures and O
2
/CO
2
concentrations inside the
package. A prediction of the equilibrium O
2
concentration inside the packages,
designed to obtain 3% O
2
at 7 °C, could be conducted between a temperature
range of 2 to 15 °C. These packages (3% O
2
at 7 °C) had acceptable O
2
concen-
trations between 2 and 10 °C. However, above 10 °C an increase in the growth
of spoilage microorganisms and a sharp decrease in sensorial quality were
noticed.
The application of high O
2
concentrations (i.e. >70% O
2
) could overcome the
disadvantages of low O
2
modified atmosphere packaging (EMA) for some ready-
to-eat vegetables. High O
2
was found to be particularly effective in inhibit-
ing enzymatic discolouration, preventing anaerobic fermentation reactions and
inhibiting microbial growth (Day, 1996; Day, 2000; Day, 2001). Amanatidou et
Modified atmosphere packaging (MAP) 349
Film permeability
0
5
10
15
20
25
30
2 4 7 10 12 15
0
500
1000
1500
2000
2500
3000
3500
4000
4500
5000
Temperature (°C)
Respiration rate (ml O2/kg.h)
Film permeability (ml O2/m.24h.atm)
Respiration rate
Fig. 16.1 Temperature dependence of the oxygen permeability and the respiration rate
of shredded chicory. (Devlieghere et al, 2000c)
al (1999) screened microorganisms associated with the spoilage and safety of
minimally processed vegetables. In general, exposure to high oxygen alone (80
to 90% O
2
, balance N
2
) did not inhibit microbial growth strongly and was highly
variable. A prolongation of the lag phase was more pronounced at higher O
2
con-
centrations. Amanatidou et al, (1999) as well as Kader and Ben-Yehoshua (2000)
suggested that these high O
2
-levels could lead to intracellular generation of reac-
tive oxygen species (ROS, O
2
-
, H
2
O
2
, OH*), damaging vital cell components and
thereby reducing cell viability when oxidative stresses overwhelm cellular pro-
tection systems. Combined with an increased CO
2
concentration (10 to 20%), a
more effective inhibitory effect on the growth of all microorganisms was noticed
in comparison with the individual gases alone (Gonzalez Roncero and Day, 1998;
Amanatidou et al, 1999; Amanatidou et al, 2000). Wszelaki and Mitcham (1999)
found that 80–100% O
2
inhibited the in vivo growth of Botrytis cinerea on straw-
berries. Based on practical trials (best benefits on sensory quality and anti-
microbial effects), the recommended gas levels immediately after packaging
are 80–95% O
2
and 5–20% N
2
. Carbon dioxide level increases naturally due to
product respiration (Day, 2001; Jacxsens et al, 2001a). Exposure to high O
2
levels
may stimulate, have no effect on or reduce rates of respiration of produce depend-
ing on the commodity, maturity and ripeness stage, concentrations of O
2
, CO
2
and C
2
H
4
and time and temperature of storage (Kader and Ben-Yehoshua, 2000).
Respiration intensity is directly correlated to the shelf life of produce (Kader et
al, 1989). Therefore, the quantification of the effect of high O
2
levels on the res-
piratory activity is necessary (Jacxsens et al, 2001a). To maximise the benefits of
a high O
2
atmosphere, it is desirable to maintain levels of >40% O
2
in the head-
space and to build up CO
2
levels to 10–25%, depending on the type of packaged
produce. These conditions can be obtained by altering packaging parameters such
as storage temperature, selected permeability for O
2
and CO
2
of the packaging
film and reducing or increasing gas/product ratio (Day, 2001).
High O
2
MAP of vegetables is only commercialised in some specific cases,
probably because of the lack of understanding of the basic biological mechanisms
involved in inhibiting microbial growth, enzymatic browning and concerns about
possible safety implications. Concentrations higher than 25% O
2
are consid-
ered to be explosive and special precautions have to be taken on the work floor
(BCGA, 1998). In order to keep the high oxygen inside the package, it is advised
to apply barrier films or low permeable OPP films (Day, 2001). However, for high
respiring products, such as strawberries or raspberries, it is better to combine high
O
2
atmospheres with a permeable film for O
2
and CO
2
, as applied in EMA pack-
aging, in order to prevent a too high accumulation of CO
2
(Jacxsens et al, 2001b).
16.5 The microbial safety of MAP
Modified atmospheres containing CO
2
are effective in extending the shelf life
of many food products. However, one major concern is the inhibition of nor-
mal aerobic spoilage bacteria and the possible growth of psychrotrophic food
350 The nutrition handbook for food processors
pathogens, which may result in the food becoming unsafe for consumption before
it appears to be organoleptically unacceptable. Most of the pathogenic bacteria
can be inhibited by low temperatures (<7 °C). At these conditions, only psy-
chrotrophic pathogens can proliferate. The effect of CO
2
on the different
psychrotrophic foodborne pathogens is described below.
16.5.1 Clostridium botulinum
One major concern is the suitability of MAP in the food industry. This is mainly
due to the possibility that psychrotrophic, non-proteolytic strains of C. botulinum
types B, E, and F are able to grow and produce toxins under MAP conditions.
Little is known about the effects of modified atmosphere storage conditions on
toxin production by C. botulinum. The possibility of inhibiting C. botulinum by
incorporating low levels of O
2
in the package does not appear to be feasible.
Miller (1988, cited by Connor et al, 1989) reported that psychrotrophic strains of
C. botulinum are able to produce toxins in an environment with up to 10% O
2
.
Toxin production by C. botulinum type E, prior to spoilage, has been described
in 3 types of fish, at O
2
levels of 2% and 4% (O’Connor-Shaw and Reyes, 2000).
Dufresne et al (2000) also proposed that additional barriers, other than headspace
O
2
and film, need to be considered to ensure the safety of MAP trout fillets, par-
ticularly at moderate temperature abuse conditions.
The probability of one spore of non-proteolytic C. botulinum (types B, E,
and F) being toxicogenic in rock fish was outlined in a report by Ikawa and
Genigeorgis (1987). The results showed that the toxigenicity was significantly
affected (P < 0.005) by temperature and storage time, but not by the used modi-
fied atmosphere (vacuum, 100% CO
2
, or 70% CO
2
/30% air). In Tilapia fillets, a
modified atmosphere (75% CO
2
/25% N
2
), at 8 °C, delayed toxin formation by C.
botulinum type E, from 17 to 40 days, when compared to vacuum packaged fillets
(Reddy et al, 1996). Similar inhibiting effects were recorded for salmon fillets
and catfish fillets, at 4°C (Reddy et al, 1997a and 1997b). Toxin production from
non-proteolytic C. botulinum type B spores was also retarded by a CO
2
enriched
atmosphere (30% CO
2
/70% N
2
) in cooked turkey at 4 °C but not at 10 °C nor at
15 °C (Lawlor et al, 2000). Recent results in a study by Gibson et al (2000) also
indicated that 100% CO
2
slows the growth rate of C. botulinum, and that this
inhibitory effect is further enhanced with appropriate NaCl concentrations and
chilled temperatures.
16.5.2 Listeria monocytogenes
Listeria monocytogenes is considered a psychrotrophic foodborne pathogen.
Growth is possible at 1 °C (Varnam and Evans, 1991) and has even been reported
at temperatures as low as -1.5 °C (Hudson et al, 1994). The growth of L. mono-
cytogenes in food products, packaged under modified atmospheres, has been the
focus of several, although in some cases contradicting, studies (Garcia de
Fernando et al, 1995). In general, L. monocytogenes is not greatly inhibited by
Modified atmosphere packaging (MAP) 351
CO
2
enriched atmospheres (Zhao et al, 1992) although when combined with other
factors such as low temperature, decreased water activity and the addition of Na
lactate the inhibiting effect of CO
2
is significant (Devlieghere et al, 2001). Liste-
ria growth in anaerobic CO
2
enriched atmospheres has been demonstrated in lamb
in an atmosphere of 50:50 CO
2
/N
2
, at 5 °C (Nychas, 1994); in frankfurter type
sausages in atmospheres of distinct proportions of CO
2
/N
2
, at 4, 7, and 10°C
(Kr?mer and Baumgart, 1992) and in pork in an atmosphere of 40:60 CO
2
/N
2
, at
4 °C (Manu-Tawiah et al, 1993). However, other authors have not detected growth
in chicken anaerobically packaged in 30:70 CO
2
/N
2
, at 6 °C (Hart et al, 1991); in
75:25 CO
2
/N
2
at 4 °C (Wimpfheimer et al, 1990) and at 4 °C in 100% CO
2
in raw
minced meat (Franco-Abuin et al, 1997) or in buffered tryptose broth (Szabo and
Cahill, 1998). Several investigations demonstrated possible growth of L. mono-
cytogenes on modified atmosphere packaged fresh-cut vegetables, although the
results depended very much on the type of vegetables and the storage tempera-
ture (Berrang et al, 1989a; Beuchat and Brackett, 1990; Omary et al, 1993; Carlin
et al, 1995; Carlin et al, 1996a and 1996b; Zhang and Farber, 1996; Juneja et al,
1998; Bennik et al, 1999; Jacxsens et al, 1999a; Liao and Sapers, 1999; Thomas
et al, 1999; Castillejo-Rodriguez et al, 2000).
There is no agreement about the effect of incorporating O
2
in the atmosphere
on the antimicrobial activity of CO
2
on L. monocytogenes (Garcia de Fernando
et al, 1995). However, this effect could be very important in practice, as the exis-
tence of residual O
2
levels after packaging, and the diffusion of O
2
through the
packaging film, can result in substantial O
2
levels during the storage of industri-
ally ‘anaerobically’ modified atmosphere packaged food products. Most publica-
tions suggest there is a decrease in the inhibitory effect of CO
2
on L.
monocytogenes when O
2
is incorporated into the atmosphere. Experiments on raw
chicken showed L. monocytogenes failed to grow at 4, 10, and 27 °C, in an anaer-
obic atmosphere containing 75% CO
2
and 25% N
2
(Wimpfheimer et al, 1990).
However, an aerobic atmosphere containing 72.5% CO
2
, 22.5% N
2
, and 5% O
2
did not inhibit the growth of L. monocytogenes, even at 4 °C. L. monocytogenes
was also only minimally inhibited on chicken legs, in an atmosphere containing
10% O
2
and 90% CO
2
(Zeitoun and Debevere, 1991). There was no significant
difference in the inhibitory effect of CO
2,
between the range of 0% and 50%,
when 1.5% O
2
, or 21% O
2
was present in the atmosphere of gas packaged brain
heart infusion agar plates (Bennik et al, 1995). When L. monocytogenes was cul-
tured in buffered nutrient broth, at 7.5 °C, in atmospheres containing 30% CO
2
,
with four different O
2
concentrations (0, 10, 20, and 40%), the results showed
that bacterial growth increased with the increasing O
2
concentrations (Hendricks
and Hotchkiss, 1997).
16.5.3 Yersinia enterocolitica
Yersinia enterocolitica is generally regarded as one of the most psychrotrophic
foodborne pathogens. Growth of Y. enterocolitica was reported in vacuum pack-
aged lamb at 0 °C (Doherty et al, 1995; Sheridan and Doherty, 1994; Sheridan
352 The nutrition handbook for food processors
et al, 1992), beef at -2 °C (Gill and Reichel, 1989), pork at 4 °C (Bodnaruk and
Draughon, 1998; Manu-Tawiah et al, 1993), fresh chicken breasts (?zbas et al,
1997) and roast beef at 3 °C but not at -1.5 °C (Hudson et al, 1994).
CO
2
retards the growth of Y. enterocolitica at refrigerated temperatures. The
effect of CO
2
on the growth of Y. enterocolitica has been described by several
authors. Some of the results are shown in Table 16.3. Oxygen also seems to play
an inhibiting role on the growth of Y. enterocolitica (Garcia de Fernando et al,
1995). To ensure total inhibition of Y. enterocolitica in O
2
poor atmospheres and
at realistic temperatures throughout the cooling chain, high CO
2
concentrations
in the headspace are necessary.
Modified atmosphere packaging (MAP) 353
Table 16.3 Growth of Yersina enterocolitica in different atmospheres
Product Temp.
Storage
Atmosphere Increase Reference
type
pH
(°C)
time
(%O
2
/CO
2
/N
2
) (log cfu/g)
(days)
Beef >6.0 -2 126 0/100/0 0 Gill and Reichel
63 vacuum 2.4 (1989)
0 98 0/100/0 0
49 vacuum 4.1
2 42 0/100/0 0
35 vacuum 5.1
5 35 0/100/0 1.9
17 vacuum 5.5
10 10 0/100/0 3.4
5 vacuum 4.0
Sliced 6.1 -1.5 112 0/100/0 0 Hudson et al
roast 56 vacuum 4.2 (1994)
beef 3 70 0/100/0 3.8
21 vacuum 4.7
Pork 5.57 30 0/100/0 0 Bodnaruk and
(normal) 4 25 vacuum 1.7 Draughon (1998)
6.21 30 0/100/0 1.7
(high) 25 vacuum 2.6
Pork 6.0 35 0/20/80 4.1 Manu-Tawiah et al
chops 4 35 0/40/60 4.0 (1993)
35 10/40/50 4.0
35 vacuum 4.1
Lamb 5.4–5.8 0 28 80/20/0 1.2 Doherty et al
28 0/50/50 3.9 (1995)
28 0/100/0 1.6
28 vacuum 5.9
5 28 80/20/0 6.8
28 0/50/50 8.5
28 0/100/0 5.6
28 vacuum 8.1
16.5.4 Aeromonas spp.
Aeromonas species are able to multiply in food products stored in refrigerated
conditions. Growth of A. hydrophila has been detected at low temperatures in a
variety of vacuum packaged fresh products, such as chicken breasts at 3°C
(?zbas et al, 1996), lamb at 0 °C under high pH conditions (Doherty et al, 1996),
and at -2 °C (Gill and Reichel, 1989), and in sliced roast beef at -1.5°C (Hudson
et al, 1994). Devlieghere et al (2000a) developed a model, predicting the influ-
ence of temperature and CO
2
on the growth of A. hydrophila. Proliferation of A.
hydrophila is greatly affected by CO
2
enriched atmospheres. Some reports regard-
ing the effect of CO
2
on the growth of A. hydrophila on meat are summarised in
Table 16.4.
In a study by Berrang et al (1989b), regarding controlled atmosphere storage
of broccoli, cauliflower and asparagus stored at 4 °C and 15 °C, fast proliferation
of A. hydrophila was observed at both temperatures, but growth was not signifi-
cantly affected by gas atmosphere. Garcia-Gimeno et al (1996) published the sur-
vival of A. hydrophila on mixed vegetable salads (lettuce, red cabbage and
carrots) packaged under MA (initial 10% of O
2
–10% CO
2
, after 48h 0% O
2
–18%
CO
2
) and stored at 4 °C while at 15 °C a fast growth was noticed (5 log units
in 24 h). The combination of high CO
2
concentration and low temperature were
revealed as responsible for the inhibition of growth. Bennik et al (1995) con-
cluded from their solid-surface model that at MA-conditions, generally applied
for minimally processed vegetables (1–5% O
2
and 5–10% CO
2
), growth of A.
hydrophila is possible. Growth was virtually the same under 1.5% and 21% O
2
.
The behaviour of a cocktail of A. caviae (HG4) and A. bestiarum (HG2) in air or
in low O
2
–low CO
2
atmosphere was investigated in fresh-cut vegetables: no dif-
ference between both atmospheres was observed on grated carrots, a decreased
growth on shredded Belgian endive and Brussels sprouts in MA but an increased
growth on shredded iceberg lettuce in MA storage (Jacxsens et al, 1999a).
16.6 The effect of MAP on the nutritional quality of
non-respiring food products
Because by using modified atmosphere packaging, the shelf-life of the packaged
products can be extended by 50–200% questions could arise regarding the nutri-
tional consequences of MAP on the packaged food products. This section will
discuss the effect of MAP on the nutritional quality of non-respiring food prod-
ucts while the effect of MAP on the nutritional value of respiring products, such
as fresh fruits and vegetables, will be discussed in detail in section 16.7.
Very little information is available about the influence of MAP on the nutri-
tional quality of non-respiring food products. In most cases, for packaging non-
respiring food products, oxygen is excluded from the atmosphere and therefore
one should expect a retardation of oxidative degradation reactions. Moreover,
modified atmosphere packaged food products should be stored under refrigera-
354 The nutrition handbook for food processors
tion to allow CO
2
to dissolve and perform its antimicrobial action. At these chilled
conditions, chemical degradation reactions have only a limited importance.
No information is available regarding the nutritional consequences of enriched
oxygen concentrations in modified atmospheres which can be applied for pack-
aging fresh meat and marine fish. Some oxidative reactions can occur with nutri-
tionally important compounds such as vitamins and polyunsaturated fatty acids.
However, no quantitative information is available about these degradation reac-
tions in products packaged in O
2
enriched atmospheres.
Modified atmosphere packaging (MAP) 355
Table 16.4 Growth of Aeromonas hydrophila in different atmospheres
Product pH Temp Storage Atmosphere Increase Reference
type (°C) time (%O
2
/CO
2
/N
2
) (log cfu/g)
(days)
Beef >6.0 -2 126 0/100/0 0 Gill and
63 vacuum 1.0 Reichel
0 98 0/100/0 0 (1989)
49 vacuum 3.1
2 42 0/100/0 0
35 vacuum 3.0
5 35 0/100/0 0
17 vacuum 3.0
10 10 0/100/0 3.8
5 vacuum 5.8
Sliced roast 6.1 -1.5 112 0/100/0 0 Hudson et al
beef 56 vacuum 4.3 (1994)
3 70 0/100/0 3.1
21 vacuum 4.6
Lamb 5.4–5.8 0 45 80/20/0 0 Doherty et al
45 0/50/50 0 (1996)
45 0/100/0 0
45 vacuum 0
5 45 80/20/0 0
45 0/50/50 0
45 0/100/0 0
45 vacuum 0
Lamb >6.0 0 42 80/20/0 0 Doherty et al
42 0/50/50 0 (1996)
42 0/100/0 0
42 vacuum 4.1
5 42 80/20/0 4.2
42 0/50/50 1.7
42 0/100/0 0
42 vacuum 4.0
16.7 The effect of MAP on the nutritional quality of
fresh fruits and vegetables
During the last few years many studies have demonstrated that fruit and veget-
ables are rich sources of micronutrients and dietary fibre. They also contain an
immense variety of biologically active secondary metabolites that provide the
plant with colour, flavour and sometimes antinutritional or toxic properties
(Johnson et al, 1994). Among the most important classes of such substances
are vitamin C, carotenoids, folates, flavonoids and more complex phenolics,
saponins, phytosterols, glycoalkaloids and the glucosinolates.
The nutrient content of fruit and vegetables can be influenced by various
factors such as genetic and agronomic factors, maturity and harvesting methods,
and postharvest handling procedures. There are some postharvest treatments
which undoubtedly improve food quality by inhibiting the action of oxidative
enzymes and slowing down deleterious processes. Storage of fresh fruits and
vegetables within the optimum range of low O
2
and/or elevated CO
2
atmospheres
for each commodity reduces their respiration and C
2
H
4
production rates (Kader,
1986; Kader, 1997). Optimum CA retards loss of chlorophyll, biosynthesis of
carotenoids and anthocyanins, and biosynthesis and oxidation of phenolic com-
pounds. In general, CA influences flavour quality by reducing loss of acidity,
starch to sugar conversion, and biosynthesis of aroma volatiles, especially esters.
Retention of ascorbic acid and other vitamins results in better nutritional quality,
including antioxidant activity, of fruits and vegetables when kept in their optimum
CA (Kader, 2001). However, little information is available on the effectiveness
of controlled atmospheres or modified atmosphere packaging (CA/MAP) on the
nutrient retention during storage. The influence of CA/MAP on the antioxidant
constituents related to nutritional quality of fruits and vegetables, including
vitamin C, carotenoids, phenolic compounds, as well as glucosinolates will be
reviewed here.
16.7.1 Vitamin C
Vitamin C is one of the most important vitamins in fruits and vegetables for
human nutrition. More than 90% of the vitamin C in human diets is supplied by
the intake of fresh fruits and vegetables. Vitamin C is required for the prevention
of scurvy and maintenance of healthy skin, gums and blood vessels. Vitamin C,
as an antioxidant, reduces the risk of arteriosclerosis, cardiovascular diseases and
some forms of cancer (Simon, 1992). Ascorbate oxidase has been proposed as
the major enzyme responsible for enzymatic degradation of l-ascorbic acid (AA).
The oxidation of AA, the active form of vitamin C, to dehydroascorbic acid
(DHA) does not result in loss of biological activity since DHA is readily re-
converted to l-AA in vivo. However, DHA is less stable than AA and may be
hydrolysed to 2,3-diketogulonic acid, which does not have physiological activity
(Klein, 1987) and it has therefore been suggested that measurements of vitamin
C in fruits and vegetables in relation to their nutritional value should include both
AA and DHA.
356 The nutrition handbook for food processors
The vulnerability of different fruits and vegetables to oxidative loss of AA
varies greatly, as indeed do general quality changes. Low pH fruits (citrus fruits)
are relatively stable, whereas soft fruits (strawberries, raspberries) undergo more
rapid changes. Leafy vegetables (e.g. spinach) are very vulnerable to spoilage and
AA loss, whereas root vegetables (e.g. potatoes) retain quality and AA for many
months (Davey et al, 2000). Fruits and vegetables undergo changes from the
moment of harvest and since l-AA is one of the more reactive compounds it is
particularly vulnerable to treatment and storage conditions. In broad terms, the
milder the treatment and the lower the temperature the better the retention of
vitamin C, but there are several interacting factors which affect AA retention
(Davey et al, 2000). The rate of postharvest oxidation of AA in plant tissues has
been reported to depend upon several factors such as temperature, water content,
storage atmosphere and storage time (Lee and Kader, 2002).
The effect of controlled atmospheres on the ascorbate content of intact fruit
has not been extensively studied. The results vary among fruit species and culti-
vars, but the tendency is for reduced O
2
and/or elevated CO
2
levels to enhance
the retention of ascorbate (Weichmann, 1986; Kader et al, 1989). A reduction in
temperature and of O
2
concentration in the storage atmosphere have been
described as the two treatments which contribute to preserve vitamin C in fruits
and vegetables (Watada, 1987) and so Delaporte (1971) and others observed that
loss of AA can be reduced by storing apples in a reduced oxygen atmosphere.
However, Haffner et al (1997) have shown than AA levels in various apple cul-
tivars decreased more under ultra low oxygen (ULO) compared to air storage.
On the other hand, increasing CO
2
concentration above a certain threshold seems
to have an adverse effect on vitamin C content in some fruits and vegetables. It
has been reported that the effect of elevated CO
2
on AA content varied among
commodities and was dependent on CO
2
level and storage temperature and dura-
tion (Weichmann, 1986). Bangerth (1977) observed accelerated AA losses in
apples and red currants stored in elevated CO
2
atmospheres. Vitamin C content
was reduced by high CO
2
concentrations (10–30% CO
2
) in strawberries and
blackberries and only a moderate to negligible effect was found for black cur-
rants, red currants and raspberries (Agar et al, 1997). Storage of sweet pepper for
6 days at 13 °C in CO
2
enriched atmospheres resulted in a reduction in AA content
(Wang, 1977). Wang (1983) noted that 1% O
2
retarded AA degradation in Chinese
cabbage stored for 3 months at 0 °C. He observed that treatments with 10 or 20%
CO
2
for 5 or 10 days produced no effect, and 30 or 40% CO
2
increased AA de-
composition. Veltman et al (1999) have observed a 60% loss in AA content of
‘Conference’ pears after storage in 2% O
2
+ 10% CO
2
. There were no data avail-
able to show whether a parallel reduction in O
2
concentration alleviates the
negative CO
2
effect. Agar et al (1997) proposed that reducing O
2
concentration
in the storage atmosphere in the presence of high CO
2
had little effect on the
vitamin C preservation. The only beneficial effect of low O
2
alleviating the CO
2
effect could be observed when applying CO
2
concentrations lower than 10%.
In fresh-cut products, high CO
2
concentration in the storage atmosphere has
also been described to cause degradation of vitamin C. Thus, concentration of 5,
Modified atmosphere packaging (MAP) 357
10, or 20% CO
2
caused degradation of vitamin C in fresh-cut kiwifruit slices
(Agar et al, 1999). Enhanced losses of vitamin C in response to CO
2
higher than
10% may be due to the stimulating effects on oxidation of AA and/or inhibition
of DHA reduction to AA (Agar et al, 1999). In addition, vitamin C content de-
creased in MAP-stored Swiss chard (Gil et al, 1998a) as well as in potato strips
(Tudela et al, 2002). In contrast, MAP retarded the conversion of AA to DHA
that occurred in air-stored jalapeno pepper rings (Howard et al, 1994; Howard
et al, 1998). Wright and Kader (1997a) found no significant losses of vitamin C
occurred during the post cutting life of fresh-cut strawberries and persimmons
for 8 days in CA (2% O
2
, air + 12% CO
2
, or 2% O
2
+ 12% CO
2
) at 0°C. In studies
of cut broccoli florets and intact heads of broccoli CA/MAP resulted in greater
AA retention and shelf-life extension in contrast to air-stored samples (Barth
et al, 1993; Paradis et al, 1996). Retention of AA was found in fresh-cut lettuce
packaged with nitrogen (Barry-Ryan and O’Beirne, 1999). They suggest that
high levels of CO
2
(30–40%) increased AA losses by conversion into DHA due
to availability of oxygen in lettuce (Barry-Ryan and O’Beirne, 1999). This fact
has also been shown in sweet green peppers (Petersen and Berends, 1993).
The reduction of AA and the relative increase in DHA could be an indication that
high CO
2
stimulates the oxidation of AA, probably by ascorbate peroxidase as in
the case of strawberries (Agar et al, 1997) and of spinach (Gil et al, 1999).
Mehlhorn (1990) demonstrated an increase in ascorbate peroxidase activity in
response to ethylene. High CO
2
at injurious concentrations for the commodity
may reduce AA by increasing ethylene production and therefore the activity
of ascorbate peroxidase. Ascorbate oxidase from green zucchini fruit, which
catalyses the oxidation of AA to DHA, has been found to be unstable and to lose
activity below pH 4 (Maccarrone et al, 1993). This could partially explain the
lower DHA content of the strawberries (pH 3.4–3.7) and the higher DHA content
of the persimmons (pH 5.4–6.0) (Wright and Kader, 1997a) as well as the
tendency of some vegetables at pH near to neutral to lose AA during storage (Gil
et al, 1998b).
In conclusion, the loss of vitamin C after harvest can be reduced by storing
fruits and vegetables in atmospheres of reduced O
2
and/or up to 10% CO
2
as Lee
and Kader (2002) have reported. CA conditions do not have a beneficial effect
on vitamin C if high CO
2
concentrations are involved, although the concentra-
tions above which CO
2
affects the loss of AA must be estimated for each com-
modity (Kader, 2001).
16.7.2 Carotenoids
Carotenoids form one of the most important classes of plant pigments and play
a crucial role in defining the quality parameters of fruit and vegetables. Their
role in the plant is to act as accessory pigments for light harvesting and in the
prevention of photo-oxidative damage, as well as acting as attractants for pol-
linators. The best documented and established function of some of the caro-
tenoids is their provitamin A activity, especially of b-carotene. a-Carotene and
358 The nutrition handbook for food processors
b-crytoxanthin also possess provitamin A activity, but to a lesser extent than does
b-carotene. Many yellow, orange or red fruit and root vegetables contain large
amounts of carotenoids, which accumulate in the chloroplast during ripening or
maturation. In some cases, the carotenoids present are simple, e.g. b-carotene in
carrot or lycopene in tomato, but in other cases complex mixtures of unusual
structures are found, e.g. in Capsicum. Carotenoids are found in membranes, as
microcrystals, in association with proteins or in oil droplets. In vivo, carotenoids
are stabilised by these molecular interactions, that are also important in deter-
mining the bioavailability of the carotenoids. Plant materials do not contain
vitamin A, but provide carotenoids that are converted to vitamin A after inges-
tion. Provitamin A carotenoids found in significant quantities in fruits may have
a role in cancer prevention by acting as free radical scavengers (Britton and
Hornero-Mendez, 1997). Lycopene, although it has no provitamin A activity, has
been identified as a particularly effective quencher of singlet oxygen in vitro (Di
Mascio et al, 1989) and as an anticarcinogenic (Giovannucci, 1999). Carotenoids
are unstable when exposed to acidic pH, oxygen or light (Klein, 1987). The effect
of controlled and modified atmospheres on the carotenoid content of intact fruits
has not been well studied. Modified atmospheres including either reduced O
2
or elevated CO
2
are generally considered to reduce the loss of provitamin A,
but also to inhibit the biosynthesis of carotenoids (Kader et al, 1989). Reducing
O
2
to lower concentrations enhanced the retention of carotene in carrots
(Weichmann, 1986). The carotene content of leeks was found to be higher after
storage in 1% O
2
+ 10% CO
2
than after storage in air (Weichmann, 1986).
Few studies on the effect of CA storage on the provitamin A carotenoid content
of fresh-cut products have been published. Wright and Kader (1997b) found for
sliced peaches and persimmons, that the limit of shelf life was reached before
major losses of carotenoids occurred. Low changes in carotenoids have been
observed in minimally processed pumpkin stored for 25 days at 5°C in MAP
(Baskaran et al, 2001). Petrel et al (1998) found no changes on the carotenoid
content of ready to eat oranges after 11 days at 4°C in MAP (19% O
2
+ 5% CO
2
and 3% O
2
+ 25% CO
2
). In addition, the content of b-carotene in broccoli florets
increased at the end of CA storage (2% O
2
+ 6% CO
2
) and remained stable after
returning the samples to ambient conditions for 24 h (Paradis et al, 1996). Lutein,
the major carotenoid in green bean tissue, also showed an accumulation after
13 days of CA storage (1% O
2
+ 3% CO
2
) and in these conditions retained
carotenoids up to 22 days at 8°C (Cano et al, 1998). However, Sozzi et al (1999)
have observed that CA of 3% O
2
and 20% CO
2
both alone and together with
ethylene prevented total carotenoid and lycopene biosynthesis on tomato. After
exposing the fruits to air, total carotenoids and lycopene increased but were in
all cases significantly lower than those which were held in air.
16.7.3 Phenolic compounds
There is a considerable evidence for the role of antioxidant constituents of fruits
and vegetables in the maintenance of health and disease prevention (Ames et al,
Modified atmosphere packaging (MAP) 359
1993). Epidemiological studies show that consumption of fruits and vegetables
with high phenolic content correlates with reduced cardio- and cerebrovascular
diseases and cancer mortality (Hertog et al, 1997). Recent work is also beginning
to highlight the relation of flavonoids and other dietary phenolic constituents to
these protective effects. They act as antioxidants by virtue of the free radical scav-
enging properties of their constituent hydroxyl groups (Kanner et al, 1994; Vinson
et al, 1995). The biological properties of phenolic compounds are very variable
and include anti-platelet action, antioxidant, antiinflamatory, antitumoral and
oestrogenic activities, which might suggest their potential in the prevention of
coronary heart diseases and cancer (Hertog et al, 1993; Arai et al, 2000).
In the last few years there has been an increasing interest in determining rel-
evant dietary sources of antioxidant phenolics and red fruits such as strawberries,
cherries, grapes and pomegranates have received considerable attention due to
their antioxidant activity. However, storage under CA/MAP conditions has been
focused on keeping the visual properties and few studies have been made on
the effect on the nutritional quality. Generally an increase in phenolics is con-
sidered a positive attribute and enhances the nutritional value of plant product.
However, many secondary metabolites typical of wild species of fruits or
vegetables have toxic effects although they are not considered here. In addition,
the organoleptic and nutritional characteristics of fruit and vegetables are strongly
modified by the appearance of brown pigments. Oxidative browning is mainly
due to the enzyme polyphenol oxidase (PPO) which catalyses the hydroxylation
of monophenols to o-diphenols and, in a second step, the oxidation of colour-
less o-diphenols to highly coloured o-quinones (Vámos-Vigyázó, 1981). The o-
quinones non-enzymatically polymerise and give rise to heterogeneous black,
brown or red pigments called melanins decreasing the organoleptic and nutri-
tional qualities (Tomás-Barberán et al, 1997; Tomás-Barberán and Espin, 2001).
Controlled atmospheres and modified atmosphere packaging (MAP) can
directly influence the phenolic composition as reflected in the changes observed
in anthocyanins. Carbon dioxide-enriched atmospheres (>20%) used to reduce
decay and extend the postharvest life of strawberries induced a remarkable
decrease in anthocyanin content of internal tissues compared with the external
ones (Gil et al, 1997). Holcroft and Kader (1999) related the decrease in straw-
berry colour under CO
2
atmosphere, with a decrease of important enzyme activ-
ity involved in the biosynthesis of anthocyanins, phenylalanine ammonialyase
(PAL; EC 4.3.1.5) and glucosyltransferase (GT; EC 2.4.1.91). A moderated CO
2
atmosphere (10%) prolongs the storage life and maintains quality and adequate
red colour intensity of pomegranate arils (Holcroft et al, 1998). However, the arils
of pomegranates stored in air were deeper red than were those of the initial con-
trols and of those stored in a CO
2
enriched atmosphere.
Modified atmospheres can also have a positive effect on phenolic-related
quality, as in the case of the prevention of browning of minimally processed
lettuce (Saltveit, 1997; Gil et al, 1998b). In addition, modified atmosphere pack-
aging of minimally processed red lettuce (2–3% O
2
+ 12–14% CO
2
) decreased
the content of flavonol and anthocyanins of pigmented lettuce tissues when com-
360 The nutrition handbook for food processors
pared to air storage (Gil et al, 1998b). The increase of soluble phenylpropanoids
observed in the midribs of minimally processed red lettuce after storage in air
was avoided under MAP. When minimally processed Swiss chard was stored in
MAP (7% O
2
+ 10% CO
2
), no effect was observed on flavonoid content after 8
days cold storage when compared to that stored in air (Gil et al, 1998b). In addi-
tion, the total flavonoid content of fresh-cut spinach remained quite constant
during storage in both air and MAP atmosphere (Gil et al, 1999).
Abnormal browning frequently occurs when fruits are stored in very low
oxygen atmospheres. Extended treatment in pure nitrogen enhances the appear-
ance of brown surfaces in fruits, which then rot rapidly when they are returned
to air (Macheix et al, 1990). These observations are probably the result of cell
disorganisation under anaerobiosis, but may also be related to variations in phe-
nolic metabolism.
There is a decrease in all phenolic compounds (e.g. anthocyanins, flavonols,
and caffeoyl tartaric and p-coumaroyl tartaric acids) in both skin and pulp of grape
berries rapidly brought under anaerobiosis in CO
2
enriched atmosphere (Macheix
et al, 1990). Anaerobiosis generally appears to be harmful for the fruit products
formed, with the frequent appearance of unwanted browning or loss of antho-
cyanins. In contrast, this treatment becomes necessary in the case of removal of
astringency from persimmom fruit by means of an atmosphere of CO
2
or N
2
.
These treatments result in the production of acetaldehyde, and deastringency is
due to the insolubilisation of kaki-tannin by reaction with the acetaldehyde
(Haslam et al, 1992).
16.7.4 Glucosinolates
Brassica vegetables, such as cabbage, Brussels sprouts, broccoli and cauliflower
are an important dietary source for a group of secondary plant metabolites known
as glucosinolates. The sulphur-containing glucosinolates are present as glucosides
and can be hydrolysed by the endogenous plant enzyme myrosinase (thiogluco-
side glucohydrolase EC 3.2.3.1). Myrosinase and the glucosinolates are physi-
cally separated from each other in the plant cell and therefore hydrolysis can only
take place when cells are damaged, e.g. by cutting or chewing (Verkerk et al,
2001). The hydrolysis generally results in further breakdown of glucosinolates
into isothiocyanates, nitriles, thiocyanates, indoles and oxazolidinethiones. Glu-
cosinolate degradation products contribute to the characteristic flavour and taste
of Brassica vegetables. Glucosinolates and their biological effects have been
reviewed in detail (Rosa et al, 1997). Indol-3-ylmethylglucosinolates, which
occur in appreciable amounts in several Brassica vegetables, are of interest for
their potential contribution of anticarcinogenic compounds to the diet (Loft et al,
1992) and so broccoli has been associated with a decreased risk of cancer based
on several beneficial properties such as the level of vitamin C, fibre and glu-
cosinolates. The glucosinolate content in Brassica vegetables can vary depend-
ing on the variety, cultivation conditions, harvest time and climate. Storage and
processing of the vegetables can also greatly affect the glucosinolate content.
Modified atmosphere packaging (MAP) 361
Processes such as chopping, cooking and freezing influence the extent of hydrol-
ysis of glucosinolates and the composition of the final products (Verkerk et al,
2001).
There are a few reports describing the effects of storage on the glucosinolate
content; for instance the storage of white and red cabbage for up to five months
at 4°C which does not seem to affect the levels of glucosinolates (Berard and
Chong, 1985). However, there is still little information about the influence of
CA/MAP on total or individual glucosinolate content of Brassica vegetables but
an increase in total glucosinolate content was reported in broccoli florets when
stored in air or CA while the absence of O
2
with a 20% CO
2
resulted in total loss
(Hansen et al, 1995).
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| 课件名称： | 食品加工营养手册（英文版） |
| 课件分类： | 食品 |
| 课件类型： | 电子图书 |
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