11.1 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. The potential advantages and
disadvantages of MAP have been presented by Farber (1991), Parry (1993)
and Davies (1995).
Whilst there is considerable information available regarding suitable gas
mixtures for different food products, 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
? effect of MAP on the nutritional quality of packaged food products.
Current research and gaps in knowledge are discussed in the following sections.
11.2 Carbon dioxide as an antimicrobial gas
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. 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 dissolved in
11
MAP, product safety and nutritional
quality
F. Devlieghere and J. Debevere, Ghent University, Belgium and
M I Gil, CEBAS-CSIC, Spain
the water phase and the fat phase of the food. This results, after equilibrium, 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 inhibition
of microorganisms in modified atmospheres is determined by the concentration
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
inhibition has been examined in several studies. 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 ration 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
induction 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 carboxylation and decarboxylation reactions, although inhibition of
other enzymes has also been reported (Jones and Greenfield, 1982).
MAP, product safety and nutritional quality 209
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
membrane, 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 30oC. Molin (1983) determined the
resistance 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 putrefaciens in marine fish, and Devlieghere and
Debevere (2000) compared the sensitivity for dissolved CO
2
of different
spoilage bacteria at 7oC. In general, Gram-negative microorganisms such as
Pseudomonas, Shewanella and Aeromonas are very sensitive to CO
2
. Gram-
positive bacteria show less sensitivity 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 11.3.
11.3 The microbial safety of MAP: Clostridium botulinum and
Listeria monocytogenes
Modified atmospheres containing CO
2
are effective in extending the shelf-life of
many food products. However, one major concern is the inhibition of normal
aerobic spoilage bacteria and the possible growth of psychrotrophic food
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 (<7oC). At these conditions, only
psychrotrophic pathogens can proliferate. The effect of CO
2
on the different
psychrotrophic foodborne pathogens is described below.
A particular concern is 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
210 Novel food packaging techniques
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 three 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, particularly 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
modified atmosphere (vacuum, 100% CO
2
, or 70% CO
2
/30% air). In Tilapia
fillets, a modified atmosphere (75% CO
2
/25% N
2
), at 8oC, 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 4oC (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 4oC but not at 10oC nor at 15oC (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 NaC1 concentrations and chilled temperatures.
Listeria monocytogenes is considered a psychrotrophic foodborne pathogen.
Growth is possible at 1oC (Varnam and Evans, 1991) and has even been
reported at temperatures as low as 1.5C (Hudson et al., 1994). The growth of
L. monocytogenes 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 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). Listeria growth in anaerobic CO
2
enriched atmosphere has been
demonstrated in lamb in an atmosphere of 50:50 CO
2
/N
2
, at 5oC (Nychas,
1994); in frankfurter type sausages in atmospheres of distinct proportions of
CO
2
/N
2
, at 4, 7 and 10oC (Kra¨mer and Baumgart, 1992) and in pork in an
atmosphere of 40:60 CO
2
/N
2
, at 4oC (Manu-Tawiah et al., 1993). However,
other authors have not detected growth in chicken anaerobically packaged in
30:70 CO
2
/N
2
, at 6oC (Hart et al., 1991); in 75:25 CO
2
/N
2
at 4oC (Wimpfheimer
et al., 1990) and at 4oC 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. monocytogenes on modified
atmosphere packaged fresh-cut vegetables, although the results depended very
much on the type of vegetables and the storage temperature (Berrang et al.,
1989a; Beuchat and Brackett, 1990; Omary et al., 1993; Carlin et al., 1995;
MAP, product safety and nutritional quality 211
Carlin et al., 1996a and 1996b; Zhang and Farber, 1996; Juneja et al., 1998;
Bennick et al., 1999; Jacxsens et al., 1999; 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
existence 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
industrially ‘anaerobically’ modified atmosphere packaged food products. Most
publications 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 27oC, in an
anaerobic 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 4oC. 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 cultured in buffered nutrient broth, at 7.5oC, 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).
11.4 The microbial safety of MAP: Yersinia enterocolitica and
Aeromonas spp.
Yersinia enterocolitica is generally regarded as one of the most psychrotrophic
foodborne pathogens. Growth of Y. enterocolitica was reported in vacuum
packaged lamb at 0oC (Doherty et al., 1995; Sheridan and Doherty, 1994;
Sheridan et al., 1992), beef at 2oC (Gill and Reichel, 1989), pork at 4oC
(Bodnaruk and Draughon, 1998; Manu-Tawiah et al., 1993), fresh chicken
breasts (O
¨
zbas et al., 1997) and roast beef at 3oC but not at 1.5oC (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 11.1. 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.
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
212 Novel food packaging techniques
variety of vacuum packaged fresh products, such as chicken breasts at 3oC
(O
¨
zbas et al., 1996), lamb at 0oC under high pH conditions (Doherty et al.,
1996), and at 2oC (Gill and Reichel, 1989), and in sliced roast beef at 1.5oC
(Hudson et al., 1994). Devlieghere et al. (2000a) developed a model, predicting
the influence 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 regarding the effect of CO
2
on the growth of A. hydrophila on
meat are summarised in Table 11.2.
In a study by Berrang et al. (1989b), regarding controlled atmosphere storage of
broccoli, cauliflower and asparagus stored at 4oC and 15oC, fast proliferation of A.
hydrophila was observed at both temperatures, but growth was not significantly
affected by gas atmosphere. Garcia-Gimeno et al. (1996) published the survival of
A. hydrophila on mixed vegetable salads (lettuce, red cabbage and carrots)
Table 11.1 Growth of Yersina enterocolitica in different atmospheres
Product pH Temp. Storage Atmosphere Increase Reference
type (oC) time (%O
2
/ (log
(days) CO
2
/N
2
) cfu/g)
Beef >6.0 2 126 0/100/0 0 Gill and
63 vacuum 2.4 Reichel
0 98 0/100/0 0 (1989)
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 beef 56 vacuum 4.2 (1994)
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
6.21 30 0/100/0 1.7 (1998)
(high) 25 vacuum 2.6
Pork 6.0 35 0/20/80 4.1 Manu-
chops 4 35 0/40/60 4.0 Tawiah et al.
35 10/40/50 4.0 (1993)
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
28 80/20/0 6.8
28 0/50/50 8.5
28 0/100/0 5.6
28 vacuum 8.1
MAP, product safety and nutritional quality 213
packaged under MA (initial 10% of O
2
-10% CO
2
, after 48h 0% O
2
-18% CO
2
) and
stored at 4oC while at 15oC a fast growth was noticed (5 log units in 24h). The
combination of high CO
2
concentration and low temperature was revealed as
responsible for the inhibition of growth. Bennik et al. (1995) concluded 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 difference 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., 1999).
Table 11.2 Growth of Aeromonas hydrophila in different atmospheres
Product pH Temp. Storage Atmosphere Increase Reference
type (oC) time (%O
2
/ (log
(days) CO
2
/N
2
) cfu/g)
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 6.1 1.5 112 0/100/0 0 Hudson et al.
roast 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
214 Novel food packaging techniques
11.5 The effect of MAP on the nutritional quality of non-
respiring food products
By using modified atmosphere packaging, the shelf-life of the packaged
products can be extended by 50–200%, however, questions could arise regarding
the nutritional consequences of MAP on the packaged food products. This
section will discuss the effect of MAP on the nutritional quality of non-respiring
food products while the effect of MAP on the nutritional value of respiring
products, such as fresh fruits and vegetables, will be discussed in detail in the
following sections.
Very little information is available about the influence of MAP on the
nutritional 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
refrigeration 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 packaging fresh meat and marine fish. Some oxidative reactions can occur
with nutritionally important compounds such as vitamins and polyunsaturated
fatty acids. However, no quantitative information is available about these
degradation reactions in products packaged in O
2
enriched atmospheres.
11.6 The effect of MAP on the nutritional quality of fresh
fruits and vegetables: vitamin C and carotenoids
During the last few years many studies have demonstrated that fruit and
vegetables 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 biosyntheses and oxidation of phenolic compounds.
MAP, product safety and nutritional quality 215
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 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.
11.6.1 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). Ascorbic 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.
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 that 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
cultivars, 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
216 Novel food packaging techniques
been described as the two treatments which contribute to preserve vitamin C in
fruits and vegetables (Watada, 1987). 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 that AA levels in various apple
cultivars 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
level and storage
temperature and duration (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 currants, red currants and raspberries (Agar et al.,
1997).
Storage of sweet pepper for six days at 13oC 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 three months at 0oC.
He observed that treatments with 10 or 20% CO
2
for five or ten days produced
no effect, and 30 or 40% CO
2
increased AA decomposition. 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 available 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 present 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, concentrations of
5, 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
decreased 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 and Hernandez-Brenes 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 eight days in CA (2% O
2
, air + 12% CO
2
, or
2% O
2
+ 12% CO
2
) at 0oC.
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
MAP, product safety and nutritional quality 217
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 atmosphere 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
concentrations above which CO
2
affects the loss of AA must be estimated for
each commodity (Kader, 2001).
11.6.2 Carotenoids
Carotenoids form one of the more 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
pollinators. The best documented and established function of some of the
carotenoids is their provitamin A activity, especially of -carotene. A-Carotene
and -crytozanthin also possess provitamin A activity, but to a lesser extent than
does -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. -
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 determining the bioavailability of the
carotenoids. Plant materials do not contain vitamin A, but provide carotenoids
that are converted to vitamin A after ingestion. Provitamin A carotenoids found
in significant quantitites 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
218 Novel food packaging techniques
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 5oC 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 4oC in MAP (19% O
2
+ 5% CO
2
and 3% O
2
+ 25% CO
2
). In addition, the content of -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 8oC (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.
11.7 The effect of MAP on the nutritional quality of fresh
fruits and vegetables: phenolic compounds and glucosinolates
11.7.1 Phenolic compounds
There is considerable evidence for the role of antioxidant constituents of fruits
and vegetables in the maintenance of health and disease prevention (Ames et al.,
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 scavenging properties of their constituent hydroxyl groups (Kanner
et al., 1994; Vinson et al., 1995). The biological properties of phenolic com-
pounds are very variable and include anti-platelet action, antioxidant,
antiinflamatory, antiumoral 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).
MAP, product safety and nutritional quality 219
In the last few years there has been an increasing interest in determining
relevant 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 considered 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 colourless o-diphenols to highly coloured o-quinones (Va′mos-
Vigya′zo′, 1981). The o-quinones non-enzymatically polymerise and give rise to
heterogeneous black, brown or red pigments called melanins decreasing the
organoleptic and nutritional qualities (Toma′s-Barbera′n et al., 1997; Toma′s-
Barbera′n and Espin, 2002).
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
strawberry colour under CO
2
atmosphere, with a decrease of important enzyme
activity involved in the biosynthesis of anthocyanins, phenylalanine
ammonialyase (PAL; EC 4.3.1.5) and glucosyltransferase (GT; EC 2.4.1.9.1).
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 controls 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
packaging 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 compared 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 eight days cold storage when compared to that stored in
air (Gil et al., 1998b). In addition, the total flavonoid content of fresh-cut
spinach remained quite constant during storage in both air and MAP atmosphere
(Gil et al., 1999).
220 Novel food packaging techniques
Abnormal browning frequently occurs when fruits are stored in very low
oxygen atmospheres. Extended treatment in pure nitrogen enhances the
appearance 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 phenolic 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 anthocyanins. In contrast, this treatment becomes necessary in the case of
removal of astringency from persimmon 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).
11.7.2 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
(thioglucoside glucohydrolase EC 3.2.3.1). Myrosinase and the flucosinolates
are physically 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. Glucosinolate 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 glucosinolates.
The glucosinolate content in Brassica vegetables can vary depending on the
variety, cultivation conditions, harvest time and climate. Storage and processing
of the vegetables can also greatly affect the glucosinolate content. Processes
such as chopping, cooking and freezing influence the extent of hydrolysis of
glucosinolates and the composition of the final products (Verkert 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 4oC which does not seem to affect the levels of glucosinolates (Berard and
Chong, 1985). However, there is still little information about the influence of
MAP, product safety and nutritional quality 221
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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