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*Corresponding author.
Email: [email protected]
International Food Research Journal 20(1): 17-26 (2013)
Journal homepage: http://www.ifrj.upm.edu.my
1
Velu, S.,
1*
Abu Bakar, F.,
2
Mahyudin, N.A.,
1
Saari, N. and
1
Zaman, M.Z.
1
Department of Food Science, Faculty of Food Science and Technology, Universiti Putra
Malaysia, 43400 UPM Serdang, Selangor D.E., Malaysia
2
Department of Food Service and Management, Faculty of Food Science and Technology,
Universiti Putra Malaysia, 43400 UPM Serdang, Selangor D.E., Malaysia
Effect of modifed atmosphere packaging on microbial fora changes in fshery
products
Abstract
Modifed atmosphere packaging (MAP) has become a popular method for packaging foods as
it can extend the shelf life of food with minimal quality defect. Oxygen, nitrogen and carbon
dioxide are the common gases used in MAP, Oxygen and carbon dioxide inclusive as only these
two gaseous have the preservative effects on the packed food product. Their effect on microbial
changes of any food product throughout storage period is highly depend on type of the product
and packaging materials, appropriate gas composition, storage temperature, the ratio between
gas and product volume, and hygienic manner during processing and packaging. MAP with
highest percentage of carbon dioxide is proven to be more effective than vacuum packaging
in inhibiting the growth of spoilage and pathogenic bacteria in many fshery products. This
article reviews the consequences of MAP towards microbial changes in fshery products.
Introduction
Fish and fshery products are well known nutrition
source as they possess high protein content (Masniyom,
2011). Conversely, fshes are easily perishable foods
with the presence of unsaturated fatty acids. The
products are greatly in risk of spoilage at pH more
than 5.2 and water activity beyond 0.95 (Choubert
and Baccaunaud, 2006; Jeek and Buchtov, 2007).
The rate of quality decline shows a discrepancy in
concern with various factors. They include fsh
species, initial microbial level, and composition in
the tissue and actions of microbial enzymes that lead
to the alteration of autolytic and proteolytic activities.
Bacterial activity leads to prominent unpleasant
changes in aroma due to metabolism of amino acids
into biogenic amines, sulfdes, organic acids and other
compounds (Wilhelm, 1982; Gram and Dalgaard,
2002). Additionally, it has been reported that
approximately 25% of food products lost during post
harvest phase are due to microbial activities (Gram
and Dalgaard, 2002). Moreover there are occurrences
of rancidity in fshes with high fat content. All of this
quality deterioration is determined through microbial,
chemical in terms of the end product of metabolites
(Alur et al., 1995) and physical methods as well as
sensory analysis (Shakila et al., 2003; zyurt et al.,
2009). Nevertheless, the quality deterioration could
be reduced by implementing good and hygienic
handling practices since the moment of catch. Ancient
preservation methods such as refrigeration storage
and icing have been effectively delayed fsh spoilage
over many years (Ashie et al., 1996). However,
the food products tend to be discarded after a short
storage phase (Wilhelm, 1982).
As a complement to those ancient preservation
techniques, MAP has a tendency to prolong the
storage life of foods signifcantly (Church, 1994;
Arritt et al., 2007; Mangaraj and Goswami, 2009).
Effects of MAP in extending shelf life of food can
be enhanced by combining with low temperature
storage (Ohlsson, 1994; Debevere and Boskou, 1996;
Arashisar et al., 2004; Choubert and Baccaunaud,
2006; Goulas and Kontominas, 2007; Yilmaz et al.,
2009). Nevertheless, the effective gas composition
required in MAP method is depending on each type
of fshery product. Thus, this review is intended to
reveal the consequences of MAP with various gas
compositions towards microbial inhibition in a range
of fshery products.
What is modifed atmosphere packaging (MAP)?
A preservation method by altering atmospheric
environment around a perishable food by substituting
with single or a mixture protective gases is known
as modifed atmosphere packaging (MAP) (Arashisar
Keywords
Carbon dioxide
fshery products
MAP
shelf life
spoilage bacteria
Article history
Received: 27 September 2011
Received in revised form:
18 June 2012
Accepted:21 June 2012
Mini Review
18 Velu et./IFRJ 20(1): 17-26
et al., 2004; Del Nobile et al., 2009). According
to Han (2005), MAP executes the basic goal of
packaging which is to protect the food material in
terms of microbiological (bacteria, moulds, yeasts,
and parasites) and physiochemical (toxic substances,
dirt, loss or uptake of moisture) qualities as well as
sensory attributes (color, smell and taste). These value
aspects that refect to the appearance of food products
are greatly infuence the procuring judgments of
purchasers as fresh commodities are preferred far
more than those frozen or processed commodities
(Goulas and Kontominas, 2007). Decline in the
quality characters due to microbial actions and
various chemical reactions either enzyme or non
enzyme catalyzed would lead to consumers negative
response towards the product and subsequently
to fnancial loss for manufacturers and producers
(Goulas et al., 2005; Floros and Matsos, 2005).
Moreover, MAP is merely an additional
system of vacuum wrapping tools by excluding or
optimizing oxygen level in the package in order to
inhibit the growth of aerobic microorganisms and
delays senescence (Al-Ati and Hotchkiss, 2003).
Reduced oxygen level slows down the metabolic
rate of food products especially fruits and vegetables
and therefore slows down the natural aging process.
Conversely, raw material, fsh species, appropriate
gas composition, storage temperature, the ratio
between gas and product volume, hygiene manner
during processing and packaging and properties of
packaging materials are vital factors contributes to
the products life storage in MAP (Sivertsvik et al.,
2002; Goulas and Kontominas, 2007). In addition,
promotion of high value rated fresh fshes in some
European countries has been done through MAP
(Baker et al., 1990).
MAP has been used extensively as approach of
food conservation where the storage life of the food
can be extended as long as possible (Stammen et al.,
1990) with minimal losses in terms of quality aspects
(Ashie et al., 1996; Amanatidou et al., 2000; Arritt
et al., 2007). However, it is acknowledged that the
respiration of the enclosed food material, biochemical
reactions and slow-moving gases in and out of the
packaging materials would lead to the changes
in gaseous atmosphere throughout storage period
which can affect the expected shelf life. In addition
to MAP, several other methods such as chemical
preservatives, use of additives, refrigerated storage,
freezing, drying, and irradiation are commonly being
used to inhibit or slow down decaying rates of food
products (Soccol and Oetterer, 2003). On the contrary,
concern of consumers health and high demand on
fresh and convenient foods without introduction of
chemical preservatives enabling MAP as a preferable
packaging method. Manufacturing frms prefer
MAP as they can sell food products that stay fresh
longer than the products kept in normal atmosphere
condition that spoil more rapidly. MAP products
stored in low temperature condition demonstrates an
effectual conservation way for shelf life extension
(Choubert and Baccaunaud, 2006) and preservation
of quality for a range of fresh supplies such as fruits,
vegetables, red meat, poultry, fsh and fsh products,
bakery products, cheese, milk powder, snacks, bread
and pasta (Lopez-Caballero et al., 2002; Ahn et al.,
2003; Goulas et al., 2005; Pantazi et al., 2008).
Gaseous used in MAP
Selection of gas composition in MAP is highly
depending on the food product desired to be packed.
Single or combination of gases contribute to the
extension of shelf life based on the acceptable microbial
count and organoleptic properties in terms of colour,
odour and feel of the food which being perceived in
the course smell, feel and visual inspection. MAP
is inclusive of common gases of oxygen, nitrogen
and carbon dioxide (Choubert and Baccaunaud,
2006; Jeek and Buchtov, 2007; Masniyom, 2011).
Oxygen and carbon dioxide are inclusive as only
these two gases have the preservative effects on the
packed food product (Soccol and Oetterer, 2003;
Gill and Gill, 2005; Jeek and Buchtov, 2007).
Oxygen is introduced in MAP to inhibit the growth of
anaerobic bacteria and the accumulation of toxin by
Clostridium botulinum type E (Pantazi et al., 2008). It
has a lower degree of solubility in water yet it is being
used in very low concentration as to avoid growth
of spoilage bacteria and fungi. Nevertheless, it leads
to several types of spoilage reactions in the product
mainly oxidative rancidity, browning reactions and
stimulates growth of aerobic bacteria. On the other
hand, MAP with elevated percentage of oxygen,
plays role in restraining TMA reduction process but
on other words this composition of MAP is preferably
limited as it would be desirable for aerobic bacteria
ending up with rapid spoilage.
Nitrogen has low solubility in water and has no
taste, color and odor. Nitrogen plays a role in delaying
oxidative rancidity and inhibiting aerobic bacterial
growth. However, it is not capable in inhibiting
anaerobic bacterial growth. Due to its low solubility,
nitrogen is used to prevent pack collapse in MAP to
equilibrate the volume drop of CO
2
during storage
time. Carbon dioxide is known as antimicrobial agent
(Ohlsson, 1994), soluble in water and lipid (Church,
1994) and gives slight pungent odor at very high
concentration. Carbon dioxide is the component
Velu et al./IFRJ 20(1): 17-26 19
which leads to the effect on microbial growth as it
dissolves readily in water and produces carbonic acid
(H
2
CO
3
). Reduction of pH occurs as accumulation
of H
2
CO
3
raises the acidity of the solution. This
phenomenon prolongs the lag phase and therefore
lowers the microbial growth rate (Bingol and Ergun,
2011) throughout logarithmic phase (Arashisar et al.,
2004). Nevertheless the drop of pH could be minimal
and perhaps there would not be any bacteriostatic
effect.
Decrease in enzymatic activity or direct inhibition
of enzyme system, transmission of membranes that
leads to the changes in cell interior pH and alteration
in physicochemical parameters of protein are the
main theories that have been suggested by researchers
for the occurrence of phenomena mentioned earlier
(Phillips, 1996; Soccol and Oetterer, 2003). Moreover,
solubility of CO
2
declines with rising temperature.
Microbial inhibition capacity of CO
2
is noticeably
superior at temperatures below 10C. Therefore,
interaction of storage temperature and concentration
of CO
2
would lead to signifcant implications on
modifed atmosphere packed foods. In addition, pack
collapse is other important factor to be considered in
MAP, where reduction of headspace volume occurs as
CO
2
(>60%) is highly soluble in the product to impart
the bacteriostatic effect on the microbial load. Gill
and Gill (2005) revealed that CO
2
has the tendency
to readily soluble in muscles and fat tissues of the
food.
Accordingly, reduction in pH occurs followed by
low protein water retention ability. This phenomenon
causes changes in organoleptic properties of the
product (Soccol and Oetterer, 2003; Gill and Gill,
2005), where high percentage of CO
2
probably lead
to negative effects on other aspects of the product
especially on the sensory aspects. According to
Phillips et al. (1996), effciency of carbon dioxide
as anti microorganism mediator is not entire and is
relies on the food product properties and the existence
of microbial fora. For instance, recommended gas
composition for white fsh (low fat fsh) is CO
2
/N
2
/O
2
:
40/30/30, while for and fatty fsh is CO2/N2: 40/60 or
CO
2
/N
2
: 60/40 (Phillips, 1996; Soccol and Oetterer,
2003). Table 1 present the use of various composition
of gas in MAP for various fshery products.
Properties of packaging material
Packaging that made from combination of few
polymers has the tendency to impart greater interaction
effect on the properties of packaging material. The
packaging materials used for MAP are gas proof
with multi layer flms. Polyvinyl chloride (PVC),
polyethylene (PE), polypropylene (PP) (Jacobsson
et al., 2004), polyester (PET), polyamide (PA), and
barrier layers of polyvinylidenchloride (PVDC) and
ethylenvinyl alcohol (EVOH) are commonly used
combination of polymers for the packaging material
of MAP (Mexis et al., 2009; Appendini and Hotchkiss,
2002). According to Mangaraj and Goswami (2009),
PVC, PE, PP and polyethylene terephthalate are more
commonly used for construction of MAP. PA exists
with the characteristics of relatively impermeable to
oxygen and relatively permeable to water vapour,
while other polymers are relatively permeable
to oxygen and relatively impermeable to water
vapour. Engineers made it with unique permeability
properties to control gaseous diffusion in and out of
the packaging.
Mould shaped containers can be formed using the
rigid flms and MAP as well can be applied on daily
applicable plastic bags or pouches. These features can
boost the products market as they can be customized
according to customers preference. Customers not
only prefer to buy food products that stay fresh long,
but may also consider their packaging appearance.
Several criteria that have to be considered upon
selection of the packaging material are as follow:
1. Barrier properties incorporate permeability of various
gaseous (oxygen, carbon dioxide, nitrogen, ethylene
and others), odour, light and moisture.
2. Anti fogging properties which enable good product
visibility.
3. Sealing reliability where the packaging material able to
seal itself and the container.
4. Mechanical criteria of the packaging material such as
tear and tensile strength, friction, puncture resistance,
possibility to be heat-formed and others (Petersen et
al., 1999).
Table 1. Fishery products with various gas proportions in modifed
atmosphere packaging stored at chilled temperature
No Fishery products
Temperature
(C)
Storage
(days)
MAP CO2/N2/O2 References
1 Deepwater pink
shrimp
1.6 0.4 9 40/30/30; 45/50/5 Lopez-Caballero et al.
(2002)
2 Rainbow trout fillets 4 1 14 100/0/0
90/7.5/2.5
40/30/30
Arashisar et al. (2004)
3 Rainbow trout 4 16 40/60/0
40/air
Choubert and
Baccaunaud (2006)
4 Sardines 4 15 60/40/0 Ozogul et al. (2004)
5 Mussels 4 15 50/50/0; 80/20/0
40/30/30/
Goulas et al. (2005)
6 Gutted farmed bass 3 9 70/30/0; 70/10/20;
60/10/30; 60/0/40;
50/20/30; 0/79/21
Torrieri et al. (2006)
7 Scomber colias
japonicus
3
6
15
15
50/50/0
50/50/0
Stamatis and
Arkoudelos (2007)
8 Grouper fillets 2 2 21 80/20/0; 60/40/0 Siah and Ariff (2007)
9 Red claw crayfish 2 21 80/10/10 Chen and Xiong (2008)
10 Pearlspot 0-2 30 40/0/60; 50/0/50;
60/0/40; 70/0/30;
40/30/30
Ravi Sankar et al.
(2008)
11 Swordfish 4 16 40/30/30 Pantazi et al. (2008)
12 Halibut 4 23 50/50/0; 50/0/50 Hovda et al. (2007)
13 Farmed eel 0 37 40/30/30 Arkoudelos et al.
(2007)
14 Salmon 5 1 18 50/0/50 Amanatidou et al.
(2000)
15 Shrimps 3 5 60/40/0; 5.1/2/92.9 Arvanitoyannis et al.,
2011)
20 Velu et./IFRJ 20(1): 17-26
How does the gas mixture introduced into the
packaging?
The procedure begins by placing the product on
trays or inside bags/pouches (specifed for MAP)
in order to apply vacuum as majority of air will be
removed. The ratio between gas and product volume
(gas/product) is commonly determined as 2:1
(Arashisar et al., 2004). This step is then followed
by injection of gas mixture which varies according to
the food products. The tray/bag is then heat sealed to
encapsulate the gas mixture and the product stored at
preferred temperature condition for a recommended
period (Arashisar et al., 2004).
Effect of MAP on micro fora changes
Gram negative microbia such as Pseudomonas,
Psychrobacter, Vibrio, Shewanella and
Photobacterium and gram positive microbes of
Baccillus, Clostridium, Lactobacillus, Micrococcus
and B. thermosphacta are found in marine fshes
(Debevere and Boskou, 1996). The same microbial
groups also present in freshwater fshes except for
Vibrio and Photobacterium. Initial microbial foras
of fsh which have been dominated by gram-positive
microorganisms are generally less susceptible for
spoilage. These phenomena would be the reason
for extended shelf life of certain fshery products
especially for tropical fshes. The mechanism of
spoilage occurs in such a way the gram negative
spoilage microorganisms such as Pseudomonads,
S. putrefaciens and Photobacterium phosphoreum
degrade the protein composition, amino acids and
other nitrogenous compounds into amines, ammonia,
organic sulfdes, and hydrogen sulfde. The rate
of spoilage is higher towards end of storage as pH
of the muscles increased to more than pH 5.2 as
this condition not able to inhibit growth of certain
spoilage bacteria especially facultative anaerobic
bacteria (Jezek and Buchtovz, 2007).
However, application of modifed atmosphere
with CO
2
has been extensively reported to extend
the storage life of food products because it restrains
microbial growth (Ozogul, Polat et al., 2004; Chen
and Xiong, 2008). Deterioration rate of fsh and
shrimp are slower when stored in refrigerated sea
water with dissolved CO
2
compared to that stored
in ice (Reppond et al., 1979). MAP with high
intensity of CO
2
able to inhibit certain percentage
of spoilage microorganisms which causes off-odor
in shrimp, except Carnobacterium divergens and
C. maltaromaticum (Chen and Xiong, 2008). It has
been reported that shrimps packed in 35 to 100%
CO
2
; O
2
or N
2
gas composition and also 50 to 100%
CO2 greatly restrain growth of microbes compared to
air storage of spotted shrimp (Arashisar et al., 2004).
Sah and Ariff (2007) report the act of CO
2
in delaying
the onset of spoilage in fresh muscle food is due to
the inhibition of aerobic, psychrotrophic and gram-
negative spoilage bacteria.
Total bacterial count
Total bacterial count of deepwater pink shrimp
stored under MAP condition (40-45% CO
2
) is two
log cycles lower that that stored in ice and ambient
temperature (Lopez Caballero et al., 2002). This
is mainly due to the restrain effects of CO
2
on the
microorganism growth as other researchers have
concluded that 50 to 100% CO
2
and 35 to 100%
CO
2
. Sixty rainbow trout (Oncorhynchus mykiss
W.) samples kept over four weeks at 4C in MAP
of 60/40 N
2
/CO
2
and 60/40 air/CO
2
showed rising
of total aerobic plate count from 4 log CFU/g to 7
log CFU/g. Similar results have also been observed
in hake (Merluccius merluccius) and Jack Mackerel
(Trachurus japonicus) (Choubert and Baccaunaud,
2006). Arashisar et al., (2004) have studied the
consequences of modifed atmosphere on microbial
changes of rainbow trout fllets. It was found that
MAP of CO
2
: 100%, CO
2
/N
2
/O
2
: 90/7.5/2.5 and CO
2
/
N
2
/O
2
: 40/30/30 each with certain level of inhibition
on aerobic bacterial counts. They revealed that
MAP of 100% CO
2
exhibited the greater inhibitory
effect as the count reached 10
5
CFU/g on 14th day
of storage for mesophilic bacterial count. Arashisar
et al. (2004) have noted that the effect of CO
2
: 90%
and CO
2
: 40% are lower in comparison with CO
2
:
100%. In addition, according to Lopez-Caballero et
al. (2002), comparable to shrimps stored under iced
and air condition, MAP of CO
2
/N
2
/O
2
: 40/30/30 and
CO
2
/N
2
/O
2
: 45/50/5 have showed greater inhibition
for total bacterial count.
Ozogula et al. (2004) had investigated the effect
of MAP (CO
2
/N2: 60/40) on total viable count and
histamine forming bacteria count in sardines (Sardina
pilchardus) kept at 4C. The outcome illustrated the
lowest total viable count (TVC) in MAP compared
to vacuum packaging and air. Moreover, Goulas
et al. (2005) has carried out research on microbial
changes (total viable count, Pseudomonas spp.,
H
2
S producing bacteria and lactic acid producing
bacteria) of refrigerated mussels stored under
modifed atmosphere packaging of CO
2
/N
2
: 50/50,
CO
2
/N
2
: 80/20 and CO
2
/N
2
/O
2
: 40/30/30. As the
results obtained, MAP with composition of CO
2
/N
2
:
80/20 attained lowest count for total viable count
7.0 logs CFU/g on 15 days of storage which is also
similar for vacuum packaging. However control and
other MAP conditions reached the microbiological
Velu et al./IFRJ 20(1): 17-26 21
acceptable limit (7 logs CFU/g) on 8
th
and 11
th
day
of storage respectively. Goulas et al. (2005) reported
that this inhibitory effect would be mainly due to high
concentration of CO
2
as it inhibits growth of aerobic
microorganisms.
Torrieri et al. (2006) have conducted a study on
gutted farmed bass (Dicentrarchus labrax) with certain
formulation of modifed atmosphere packaging
at storage temperature of 31 C for 9 days. They
used gas composition for MAP are as follows: A (O
2
/
CO
2
/N
2
: 0/70/30), B (O
2
/CO
2
/N
2
: 20/70/10), C (O
2
/
CO
2
/N
2
: 30/60/10), D (O
2
/CO
2
/N
2
: 40/60/0), E (O
2
/
CO
2
/N
2
: 30/50/20) and F (O
2
/CO
2
/N
2
: 21/0/79). In
terms of aerobic mesophilic bacteria (AMB), MAP
of B and E showed greater inhibition compared to
the other MAP compositions. AMB of below l log
CFU/g at 0 day found to be 2.5 10
6
logs CFU/g and
2.2 10
7
logs CFU/g, respectively in B and E at 9
day which is still under the upper acceptability limit.
It has been reported that high levels of AMB observed
in D and F was due to high percentage of oxygen
in the package headspace. Ahead of that, quality
assessment of Scomber colias japonicas in modifed
atmosphere (CO
2
/N
2
: 50/50) and vacuum packaging
at temperatures of 3 and 6 C have been studied by
Stamatis and Arkoudelos (2007). Total viable count
(TVC) for MAP samples stored at 3 and 6 C were
6.6 logs CFU/g and 6.7 logs CFU/g, respectively
after 15 days of storage. TVC in Samples stored
under vacuum packaging and air for both 3 and 6 C
reached the upper acceptability level (7 logs CFU/g)
at day 6 and 10 of storage, respectively.
Another study has also been conducted on fresh
grouper (Epinephelus sp.) fllets under two different
modifed atmosphere (MA) condition of CO
2
/N
2
:
80/20 and CO
2
/N
2
: 60/40 (Siah and Ariff 2007). They
found that aerobic plate count in samples treated with
MAP of CO
2
/N
2
: 80/20 is lower than that treated with
CO
2
/N
2
: 60/40 and stored in 100% air. Total viable
count (TVC) on smoked mullet (Mugil cephalus)
stored at 4 C in MAP with gas ratio of CO
2
/N
2
/O
2
:
35/60/5 was reported to be lower if compared to the
samples packed under vacuum conditions (Ibrahim
et al., 2008). Upon storage period, TVC showed
increment on both MAP and vacuum condition yet
as mentioned the corresponding counts appeared to
be lower in MAP (Ibrahim et al., 2008). Precooked
red claw crayfsh (Cherax quadricarinatus) was
stored under MAP (CO
2
/O
2
/N
2
: 80/10/10), aerobic
polyvinylchloride packaging (PVCP) and vacuum
packaging (VP) and shelf enhancement assessments
were carried out by Chen and Xiong (2008). Aerobic
plate count (APC) remained low during the frst
three days of storage of all three packaging systems.
However, APC of samples stored in VP and PVCP
increased rapidly from day 7 to 21 (end of storage).
Moreover, at the end of storage, APC in PVCP, VP
and MAP are 9.73, 8.41 and around 3 logs CFU/g,
respectively. This is showed that MAP remained the
best treatment to keep microbiological count in red
claw crayfsh under the acceptable limit.
Ravi Sankar et al. (2008) have studied the effect
of various gas proportions of MAP for pearl spot
as each proportion is different for various fshery
products. Pearl spot has been packed into MAP of
CO
2
/O
2
with ratio of 40/60, 50/50, 60/40, 70/30 and
CO
2
/O
2
/N
2
: 40/30/30 and stored at 0-2C for 30 days
of storage. Samples treated with MAP of CO
2
/O
2
:
60/40 exhibited lowest mesophilic aerobic count at
the end of storage. While sample with other treatments
have reached the upper acceptability limit at around
day 30. Swordfsh (Xiphias gladius) which is well-
liked in Greece have been evaluated by Pantazi et al.
(2008) in MAP CO
2
/N
2
/O
2
: 40/30/30 under storage at
4 C for 16 days. They revealed that total viable count
in MAP samples was signifcantly lower compared
to that in air samples on day 16, although the upper
acceptability limit of 7 logs CFU/g has been reached
on day 11. Farmed eel (Anguilla anguilla) stored at
0 C under modifed atmosphere packaging (CO
2
/N
2
/
O
2
: 40/30/30) and vacuum packaging were studied for
quality attributes by Arkoudelos et al. (2007). Total
aerobic plate count increased from 2.8 log CFU/g
(day 0) to 7.4 and 7.8 log CFU/g on day 31 and 37
in samples treated with vacuum and MAP storage,
respectively. It has been reported that based on upper
acceptability limit for marine species, eels stored
under air, vacuum and MAP reached 7 logs CFU/g
on day 18, 28 and 34, respectively. This clearly
demonstrates that eels stored under MAP (CO
2
/N
2
/
O
2
: 40/30/30) signifcantly extends the shelf life
longer than air and vacuum condition (Arkoudelos et
al., 2007).
H
2
S producing bacteria
The common H
2
S producing bacteria species are
Shewanella putrefaciens, certain Pseudomonas,
Vibrio and Aeromonas spp. (Debevere and Boskou,
1996). Vogel, Venkateswaran et al. (2005) reported
Shewanella baltica as the main signifcant H
2
S
producing species in ice stored Danish marine fsh.
Pseudomonas putrefaciens identifed for the species
as it revealed the ability to form H
2
S in haddock fllets
(Levin, 1968).
Lopez-Caballero et al. (2002) reported that MAP
retarded growth of H
2
S producing microorganisms
in shrimps. They found that H
2
S producing
microorganisms count in shrimp kept at MAP of CO2/
22 Velu et./IFRJ 20(1): 17-26
O
2
/N
2
: 40/30/30 and CO
2
/O
2
/N
2
: 45/5/50 was around
1.1 and 1.6 log CFU/g, respectively after nine days
of storage period. However, the particular bacterial
count in shrimp treated with ice and air storage was
around 3.3 and 3.1 logs CFU/g, respectively within
the time period as MAP treatment (Lopez-Caballero
et al., 2002). Moreover, Goulas et al. (2005) found
that H
2
S producing bacterial count of refrigerated
mussels kept in CO
2
/N
2
: 80/20 remained under
microbiological acceptable limit throughout 15 days
storage period. In contrast, H
2
S producing bacterial
count of refrigerated mussels treated with MAP of
CO
2
/N
2
: 50/50 (7.4 log CFU/g) and CO
2
/O
2
/N
2
:
40/30/30 (8.0 CFU/g) exceed the microbiological
acceptable limit on day 15 of storage. Samples of
pearl spot has been counted for the H
2
S producing
bacteria by Ravi Sankar et al. (2008) who revealed
that the lowest count of H
2
S producing bacteria
was observed in pearl spot treated with MAP CO
2
/
O
2
: 60/40 compared to other ratio of CO
2
and O
2
. In
addition, MAP CO
2
/O2/N
2
: 40/30/30 signifcantly
inhibited the growth of H
2
S producing bacteria in
Mediterranean swordfsh stored at 4C for 16 days
(Pantazi et al., 2008).
Enterobacteria counts
MAP inhibited the growth of Enterobacteria in
shrimp during storage (Lopez-Caballero et al., 2002).
Enterobacterial count in shrimp packed with MAP of
CO
2
/O
2
/N
2
: 40/30/30 and CO
2
/O
2
/N
2
: 45/5/50 is 2.8
and 3.7 log CFU/g, respectively. The count was lower
compared to that of shrimp treated with ice (5.0 logs
CFU/g) and air condition (5.6 log CFU/g) at the end
of storage (Lopez-Caballero et al. 2002). Inhibition
of Enterobacterial growth is also observed in rainbow
trout fllet treated with MAP of both 100% CO
2
and O
2
/
N
2
/CO
2
: 2.5/7.5/90 after 6 days of storage (Arashisar
et al., 2004). However, lower percentage of CO
2
is
required to delay the growth of Enterobacterial count
in gutted farmed bass (Dicentrarchus labrax) stored
at 31 C for 9 days (Torrieri et al., 2006).
Ravi Sankar et al. (2008) revealed that MAP
treatment with various compositions of CO
2
and O
2

effectively suppressed the count of Enterobacteria
in pearl spot below the upper acceptability limit
with least count observed in MAP CO
2
/O
2
: 60/40.
Mediterranean swordfsh stored in MAP CO
2
/O
2
/
N
2
: 40/30/30 exhibited as low as 4.2-5.6 logs CFU/g
of Enterobacteriaceae count on day 16 of storage
(Pantazi et al., 2008). Arkoudelos et al. (2007) found
that Enterobacterial count in farmed eel (Anguilla
anguilla) treated with modifed atmosphere (CO
2
/N
2
/
O
2
: 40/30/30), vacuum packaging and air condition
were 3.0, 3.4 and 4.5 log CFU/g, respectively, after
stored at 0 C for about 1 month.
Histamine forming bacteria
Clostridium perfringens, some strains of
Enterobacter cloacae and Enterobacter aerogenes,
Klebsiella oxytoca, Klebsiella pneumoniae, Proteus
mirabilis, and Vibrio alginolyticus were identifed
as histamine producers where these microorganisms
possess histidine decarboxylate activity (Lopez-
Sabater, Rodriguez-Jerez et al., 1994; Yoshinaga,
1982). Niven et al. (1981) concluded that Proteus
morganii and Klebsiella pneumonia are the majority
species involved in the production of histamine in
scombroid fsh and mahi mahi. Proteus morganii,
Klebsiella pneumonia and Enterobacter aerogenes
were classifed as prolifc histamine producers,
while Hafnia alvei, Escherichia coli and Citrobacter
freundii were reported as slow histamine producers
(Taylor and Speckhard, 1983). Morganella morganii,
Proteus vulgaris, Proteus mirabilis, Proteus spp.,
Staphylococcus genus and S. epidermidis are also
categorised as prolifc histamine producing bacteria
(Ababouch et al., 1991; Hernandez-Herrero et al.,
1999; Kim et al., 2002).
Histamine forming bacteria was not given much
emphasis on studies related to MAP. Ozogul et al.
(2004) have included this count in sardine samples
stored in MAP of CO
2
/N
2
: 60/40. Histamine forming
bacteria has increased in sardines samples (Sardina
pilchardus) from all treatments (MAP CO
2
/N
2
: 60/40,
vacuum packaging and air) throughout the storage
period at 4 C. However, histamine forming bacterial
count was lower compared to other treatments.
Pseudomonas spp.
Goulas et al. (2005) found that MAP of CO2/
N
2
: 80/20 and vacuum packaging effective to inhibit
growth of Pseudomonas spp. (6.8 0.3 log CFU/g) in
mussels during 15 days of storage. However, the count
of Pseudomonas spp. in samples treated with MAP of
CO
2
/O2/N
2
: 40/30/30 and CO
2
/N
2
: 50/50 reached the
microbiological acceptable limit on day 8 and 11 of
storage, respectively. Goulas et al. (2005) concluded
that this inhibitory effect is mainly due to the high
concentration of CO
2
. Pseudomonas and Shewanella
putrefaciens count is used as spoilage indicator in
iced fsh and fsh products. Stamatis and Arkoudelos
(2007) have also reported that Pseudomonas count
in fresh chub mackerel (Scomber colias japonicas)
fllets treated with MAP CO
2
/N
2
: 50/50 was below
7 log CFU/g after stored at 3 and 6 C for 15 days.
According to Arkoudelos et al. (2007), farmed eel
(Anguilla anguilla) stored at 0 C under modifed
atmosphere packaging (CO
2
/N
2
/O
2
: 40/30/30) shows
Velu et al./IFRJ 20(1): 17-26 23
Pseudomonas counts of 4.2 log CFU/g on day 37 of
storage. Arkoudelos et al. (2007) further stated that
Pseudomonas count is lower in farmed eel treated
with MAP than with air condition (7.3 logs CFU/g
at day 18) and vacuum packaging (5.9 log CFU/g at
day 31).
Coliform count
Enterobacter, Citrobacter and Aeromonas are
those major strains classifed for coliform bacteria.
Aeromonas hydrophila reported to be more common
isolates among the other genera (Niemi and Taipalinen,
1982). Chen and Xiong (2008) reported that samples
of precooked and peeled red claw crayfsh showed
similar trends of packaging effectiveness for coliform
counts as observed for aerobic plate count. Coliform
count was low in all packaging treated samples until
7 day. Rapid increase in coliform count was observed
in both PVCP and VP treated samples, reaching about
8.5 logs CFU/g on day 21 of storage. While samples
treated with MAP showed lowest coliform count
(below 3 logs CFU/g) at the end phase of storage (21
day). Greater signifcant difference has been observed
for both APC and coliform count between MAP and
other packaging system at the end of storage period
(Chen and Xiong, 2008).
Halophilic bacterial count
Bacteria in the family of Halobaculum,
Halorubrum, Natrialba, Natronomonas and
Haloterrigena were classifed as extreme
halophilic aerobic Archaea. Other species including
Halobacterium cutirubrum, H. halobium, H.
salinarium, H. saccharovorum, H. trapanicum,
H. volcanni (Kamekura 1998). Halobacterium
cutirubrum, H. salinarium and Pseudomonas
salinaria are some of halophilic bacteria studied by
Lanyi (1974) for properties of protein obtained from
the particular enzymes.
Ibrahim et al. (2008) found that halophilic
bacterial count increased in both MAP and under
vacuum conditions after two weeks of storage and
followed by decline on the third week of storage at 4
C for smoked mullet samples. However with respect
to storage period, halophilic bacterial count showed
increment particularly for those smoked mullet
samples stored under vacuum condition than the one
stored under MAP (Ibrahim et al., 2008).
Psychotrophic counts
Pseudomonas, Vibrio, Falvobacterium and
Moraxella are some important psychrotrophic Gram
negative bacteria which lead to microbial spoilage
of seafood (Khan et al., 2005). Pseudomonas and
Achromobacter are rapid growing psychrotrophic
bacteria which cause spoilage in seafood (Montville
and Curran, 1993). Bacillus cereus is one of the most
common psychotropic species (Cosentino et al.,
1997).
International fsh trade organizations used upper
acceptability limit of 6 log CFU/g aerobic plate
counts for Halibut (Hippoglossus hippoglossus),
also as an indicator for frst-rate shelf life for halibut.
Accordingly, Hovda et al. (2007) studied the effect of
MAP on farmed halibut with gas proportions of CO
2
/
O
2
and CO
2
/N
2
of each 50/50 at storage temperature
of 4 C. On day 23, psychotrophic counts obtained
for both MAP CO
2
/N
2
and CO
2
/O
2
of 50/50 were
below 7.0 logs CFU/g. In short, Hovda et al.
(2007) concluded that halibuts packed with oxygen
fortifcation shows superior storage life extension
as compared to MAP fortifed with 50/50: CO
2
/N
2
.
Pearl spot stored in MAP of CO
2
/O
2
: 40/60, CO
2
/O
2
:
50/50, CO
2
/O
2
: 60/40, CO
2
/O
2
: 70/30 and CO
2
/O
2
/N
2
:
40/30/30 demonstrated similar psychotrophic counts
for all the treatment at day 30 when stored at 0-2 C
(Ravi Sankar, Lalitha et al., 2008). However, MAP
of CO
2
/O
2
: 60/40 which found to be the prominent
treatment for other bacteria encountered in the
study proves the same trend with lowest count for
psychotrophic bacteria (Ravi Sankar et al., 2008).
MAP and other methods
Traditional preservation methods such as salting,
chilling, superchilling, freezing, smoking and others
extend shelf life of fshery products as known earlier.
The particular shelf life is being lengthened further
with introduction of packaging mainly MAP (Phillips,
1996). Superchilled Atlantic Salmon (Salmo salar)
fllets has shelf life of 10 days based on the aerobic
mesophiles (6 log (CFU/g as the microbiological
limit). Conversely MAP samples exhibited extended
shelf life of 16 and 22 days respectively depending on
the CO
2
concentration on the packages. MAP samples
remained about 5 logs (CFU/g) for psychotropic
bacterial counts after 28 days of storage which is
about 8 days later than the control sample (Fernandez
et al., 2009). Superchilled samples of spotted wolf
fsh (Anarhichas minor) showed lower aerobic and
psychrotrophic count compared to samples air samples
(Rosnes et al., 2006). CO
2
atmosphere packaged cold
smoked salmon samples extended shelf life for fve
to six weeks by limiting the lactic acid bacteria as
only four weeks shelf life in 5 C (Paludan-Maller et
al., 1998).
Lauzon et al. (2009) reported total viable
psychrotrophic and H
2
S producing bacterial count
were lower in brined MAP fsh that air packed brined
fsh and unbrined fsh samples stored at superchilling
24 Velu et./IFRJ 20(1): 17-26
temperatures of 2 and 3.6 C. Sensory shelf life
of cod fllets has been extended in MAP combined
with superchilling condition than superchilled air
samples. Base on microbiological result, smoked
trout has longest shelf life of 47 days in MAP
packages of higher composition of CO
2
compare to
only 33 days shelf life in vacuum packaged samples.
Similarly, extended shelf life has been observed in
MAP samples of six days than in air stored maatjes
herring samples (Lauzon and Martinsdattir, 2005).
Atlantic salmon fllets showed signifcantly greater
shelf life in MAP than samples stored in air (Hansen
et al., 2009). Furthermore, it has been reported MAP
inclusive of certain composition CO
2
and of O
2
(O
2
/
CO
2
: 50/50 or O
2
/CO
2
: 70/30) retain colour of meat
samples for extended period (Li and Xie, 2008).
Conclusion
Application of MAP has increased consumer
demand due to its technical opportunity with signifcant
pursue in extending storage life of fshery products,
helped in providing good quality food products,
avoids or lessens usage of chemical preservatives.
MAP also improved other quality characteristics such
as stabilizing color of food products and prevent bad
odor. MAP in combination with natural preservatives
namely antioxidants and antimicrobial inclusive
of essential oils tends to extensively prolong the
storage life of commodities. Conversely, the use of
MAP has its own risk besides the benefts. It may
cause number of potential disadvantages which has
to be considered such as increase in product cost,
requirement of skilled staff during production, and
possibly chemical and microbiological hazardous
appeared in packed products. MAP has been proved
as an effective packaging method to extend the shelf
life of a wide range of fsheries products. The use of
MAP can also delay the growth of many spoilage
and undesired microorganisms as well as inhibit
their toxin production to ensure the safety of fsheries
products.

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