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Received: January 2010 Accepted: Agust 2010
84 Iranian Journal of Fisheries Sciences 10(1) 75 - 2011
Effect of Gamma irradiation and frozen storage on microbial
quality of Rainbow trout (Oncorhynchus mykiss) fillet
Oraei, M.1*; Motalebi, A. A.2; Hoseini, E.1; Javan, S.3
Abstract
The effect of gamma radiation (1, 3 and 5 kGy) on microbial
quality of farmed rainbow
trout
(Oncorhynchus mykiss) fillets which were stored under frozen conditions
(-20°
C) was
studied by measuring microbiological changes in 5 months. Gamma irradiation and
increasing of frozen storage time had significant effects (P<0.05) on the reduction of
microorganism's
population. The total count showed that all samples maintained acceptable
microbiological quality until the end of the fifth month of frozen storage. The lowest
microbial load at the end of the fifth month of frozen storage
was
related to irradiated
samples
at 3 kGy (2 Log CFU/g). Yeasts
and molds
were below the detection levels
in
both
irradiated samples at 1 and 5 kGy until the end of the third month and in irradiated samples
at
3 kGy throughout the
frozen storage. The population of
yeasts and molds increased in
irradiated samples at 1 and 5 kGy in the fourth
and fifth month of frozen storage. Growth of
coliform bacteria and Salmonella
wasn't
observed
in control and irradiated samples due to
good hygienic quality of fish breeding, fishing, handling, filleting and packaging and also
effect of freezing on elimination and inactivation of mesophilic microorganisms.
Keywords:
Gamma irradiation,
Frozen Storage,
Rainbow
trout (Oncorhynchus mykiss),
Microbiological analysis
__________________
1- Department of Food Science and Technology, Science and Research Branch, Islamic Azad University, P.O.BOX: 14155-
4933, Tehran, Iran.
2- Iranian Fisheries Research Organization, P.O.BOX: 14155-6116 Tehran, Iran.
3- Iranian Fish Processing Research Center. Bandar Anzali, Iran.
*Corresponding Author: (email addresses: Marjan.Oraei@yahoo.com
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radiation (
76 Oraei et al., Effect of Gamma irradiation and frozen storage on microbial……
Introduction
The rainbow trout (Oncorhynchus mykiss)
belongs to the Salmonidae and is one of
the main fish species farmed in Iran. The
demand for rainbow trout in Iran and other
country markets has increased significantly
over the past decade and this could be due
to its desirable characteristics (taste,
aroma, white flesh) resulting in a high-
quality product and nutritional value
(FAO, 2010a,b; Iranian Fisheries
Organization, IFO, 2009). The major
problem of distribution of seafood or
fishery products is their susceptibility to
spoilage, mainly due to contamination of
spoilage and pathogenic microorganisms
(Özden and Erkan, 2010). Fish spoilage
occurs following growth and activity of
special microorganisms and lipid oxidation
which cause off-odor and off-taste by
production of some metabolites changing
sensory characteristics and customer
acceptability (Moini et al., 2009;
Rostamzad et al., 2010). Therefore there is
an obvious need for development of new
technologies and efficient fish preservation
methods which permit shelf-life extension
of these products (Chouliara et al., 2004).
Besides traditional methods such as ice
storage, rapid chilling, freezing, smoking
and heating (Farkas, 1990, 1999;
Himelblooom et al., 1994), various
methods involving the use of organic
acids, antimicrobials (Al-Dagal and
Bazarra, 1999; Gelman et al., 2001),
antioxidants (Haghparast et al., 2010),
edible coating (Motalebi et al., 2010),
modified atmosphere packaging
(Masniyom et al., 2002) and ionizing
Savvaidis et al., 2002;
Chouliara et al., 2004; Erkan and Özden,
2007) have been proposed to extend the
shelf-life of fish and fisheries products.
The irradiation of food products is a
physical treatment involving direct
exposure to electron or electromagnetic
rays, for their long time preservation and
improvement of quality and safety
(Mahindru, 2005). Cobalt-60 (60Co)
produces electromagnetic γ-rays which
have too much energy. During radiation,
DNA molecules undergo swelling and
break alongside the chain, preventing them
from functioning normally. As a result, the
parasites and microorganisms that have
been affected are no longer capable of
reproducing themselves and they die
(Lacroix and Ouattara, 2000). Therefore
food irradiation provides safety and
extends the shelf life of fisheries products
because of its high effectiveness in
inactivating pathogenic and spoilage
microorganisms without deteriorating
product quality (Özden and Erkan, 2010).
The alteration in microbial population and
composition as a result of irradiation
depends on the dose of irradiation, storage
temperature, packaging conditions and fish
species (Özden et al., 2007). Freezing
controls growth of microorganisms and
biochemical changes in fish as a
preservation method for long time storage
(Motalebi et al., 2010). When irradiation is
used in combination with freezing, the
irradiation doses can be reduced through
synergistic action without affecting the
product quality (Lacroix and Ouattara,
2000). A review of the scientific and
technical literature revealed some
information about the effects of irradiation
on microbiological characteristics of
irradiated food (Lamuka et al., 1992;
Dogbevi et al., 1999; Thayer and Boyd,
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Iranian Journal of Fisheries Sciences, 10(1), 2011 77
2000; Ouattara et al., 2001, 2002; Badr,
2004; Chouliara et al., 2004; Javanmard et
al., 2006; Özden et al., 2007; Sedeh et al.,
2007; Fallah et al., 2008; Turgis et al.,
2008 ; Ahmed et al., 2009; Moini et al.,
2009).
The aim of this study was to
determine the effect of gamma irradiation
process in low-dose (1, 3 and 5 kGy) and
frozen storage on microbial quality of
rainbow trout fillets.
Materials and methods
A total of 10 kg freshwater rainbow trout
(Oncorhynchus mykiss) with an average
weight of 300-500 grams were obtained
from a local aquaculture farm located at
Saravan-Foman road, in the north of Iran.
The fish were then transferred to the
laboratory at the National Fish Processing
Technology Research Center at Anzali
port in Iran. After passing into rigor
mortis, the fish were washed with tap
water, skinned, beheaded, gutted and then
filleted by a sterile scalpel and washed
again. Each fish was divided into four
fillets (about 70-80 g each). Each fillet was
separately placed in a plastic film bag. The
fillets were divided into four lots (20 fillets
in each lot): 0 kGy (control) and irradiated
samples (1, 3 and 5 kGy) (Moini et al.,
2009). Packed samples were delivered to
the radiation plant in insulated polystyrene
boxes with ice/fillets weight ratio to 2:1.
The ice was placed in plastic film bags.
Gamma irradiation was carried out in the
Nuclear Research Center for Agriculture
and Medicine, Karaj, Iran. Fish samples
were gamma irradiated using a 60Co source
irradiator (Gamma cell Px-30, dose rate
0.23 Gy sec-1). The applied dose levels
were 0 (control), 1, 3, and 5 kGy (Moini et
al., 2009). During irradiation the packed
fish were next to sealed ice covering. The
dose rate was established using alanine
transfer dosimeter. After irradiation,
irradiated and non-irradiated fillets were
transported to the laboratory at the
National Fish Processing Technology
Research Center at Anzali port in Iran in
insulated polystyrene boxes with ice-fillets
weight ratio to 2:1. In the laboratory, fillets
were exposed to rapid freezing in a spiral
freezer (Koppens SVR C400/17-50, UK).
Fillet depth reached to -20° C within 25
minutes. Then frozen fillets were kept in a
cold storage at -20° C for 5 months.
Rainbow trout fillets were analyzed for
microbiological quality at the first day of
frozen storage as 1-month sampling
intervals for 5 months. The first day of the
first interval was registered as day zero.
For the microbiological analysis 10 g of
rainbow trout fillet was removed with a
sterile scalpel and minced under aseptic
conditions. Then it was homogenized for 2
minutes with 90 ml of 0.1% (w/v) sterile
peptone water (Merck, Germany) using a
lab-blender 400 stomacher (Seward
medical, UK). Subsequent dilutions were
prepared by mixing a 1-ml sample with 9
ml of sterile peptone water. All analyses
were carried out in duplicate. For
determination of total bacterial count, 1 ml
of appropriate dilutions were poured-
plated with melted plate count agar (PCA)
(Merck, Germany) and then were
incubated at 35-37° C for 48 h. For the
numeration of total coliforms, 1 ml of
appropriate dilutions were poured-plated
with melted violet red bile agar (VRBA);
plates were incubated at 37°C for 48 h.
Total yeasts and molds were enumerated
on potato dextrose agar (Merck, Germany)
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78 Oraei et al., Effect of Gamma irradiation and frozen storage on microbial……
after incubation at 25° C for 3–5 days. For
detection of Salmonella spp., 10 g of the
sample was homogenized with 90 ml
lactose broth (Merck, Germany) and
incubated at 35° C for pre-enrichment.
Selective enrichment was performed in
tetrathionate broth (Merck, Germany) at
43° C for 24 h and selenite cystine broth
(Merck, Germany) at 35° C for 24 h
followed by plating on Salmonella-
Shigella (SS) agar (Merck, Germany) and
brilliant-green phenol-red lactose sucrose
(BG) agar (Merck, Germany) incubated at
35° C for 24 h. Suspected colonies
developed on each plate served to
biochemical and serological analysis
(American Public Health Association,
APHA, 1992).All data from microbial
analysis were subjected to factorial
analysis of variance (ANOVA) and
Duncan's multiple range test (P<0.05) to
evaluate the effect of irradiation and
different applied doses in this study and
frozen storage time on microbiological
characteristics of rainbow trout fillets.
Differences between means were
considered significant when P<0.05. SPSS
version 18.0 was used for statistical
analysis.
Results
The values of total count, yeasts and molds
count, coliforms count and Salmonella
detection of non-irradiated (control) and
irradiated (1, 3 and 5 kGy) rainbow trout
fillets during frozen storage (-20° C) are
shown in Table 1.Initial total bacterial
counts of the control samples were 4.38
Log CFU/g, whereas the counts in samples
irradiated at 1 kGy were 3.45 Log CFU
and in irradiated samples at 3 and 5 kGy
were not detectable at day 0 of frozen
storage. Microbial load of irradiated
samples at 5 kGy until the end of the first
month and in the irradiated samples at 3
kGy until the end of the fourth month were
below detection level.
Table 1: Microbial flora count (Log CFU/g) in non-irradiated and irradiated (1, 3 and 5 kGy) of rainbow
trout fillets during frozen storage (-20° C)
Microbial Flora Radiation Dose
(kGy) Storage Time (Month)
0 1 2 3 4 5
Total Count
0 4.38±1.53 aw 3.65±0.06 a
bw
3.30±0 aw 3.65±0.06 aw 3.30±0 aw 3.45±0.21
bw
1 3.45±0.21 ax 3.23±0.33
abx
2.00±0 ax 2.45±0.21 ax 2.00±0 ax 2.69±0.12
b
x
3 ND ay 2.00±0
ab
yND ay ND ay ND ay 2.00±0
b
y
5 ND az ND abz 2.00±0 az 1.00±1.41 az 2.00±0 az 2.47±0
bz
Yeasts and
Molds
0
1 ND ND ND ND ND ND
ND ND ND ND 1.00±0 1.00±0
3
5 ND ND ND ND ND ND
ND ND ND ND 1.00±0 1.15±0.21
Coliforms
0 ND ND ND ND ND ND
1 ND ND ND ND ND ND
3 ND ND ND ND ND ND
5 ND ND ND ND ND ND
Salmonella
0
1 ND ND ND ND ND ND
ND ND ND ND ND ND
3
5 ND ND ND ND ND ND
ND ND ND ND ND ND
ND = not detected; a-b Means within a row, which are not followed by a common superscript letter(s) are
significantly different (P<0.05); w-z Means within a column, which are not preceded by a common superscript
letter(s) are significantly different (P<0.05).
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Iranian Journal of Fisheries Sciences, 10(1), 2011 79
The lowest microbial load at the end of the
fifth month of frozen storage was related
to irradiated samples at 3 kGy (2 Log
CFU/g). Yeasts and molds were not
detected in irradiated samples at 3 kGy
throughout the frozen storage time and in
irradiated samples at 1 and 5 kGy until the
end of the third month of frozen storage.
The population of yeasts and molds
increased in irradiated samples at 1 and 5
kGy in the fourth and fifth month of frozen
storage.
Coliform and Salmonella bacteria
were not detected in all irradiated and
control samples throughout the storage.
Discussion
Although it is widely accepted that the
initial microbial load of freshwater fish
varies depending on water conditions and
temperature, most of the available
literature on different freshwater species
(Tilapia, Striped bass, Rainbow trout,
Silver perch and Sea bream) reports
bacterial counts of 2 to 7 Log CFU/g
(Moini et al., 2009). The initial counts and
the counts in all the time during the frozen
storage indicated to an acceptable fish
quality, considering the proposed upper
acceptability limit for total bacterial counts
of 2×107 CFU/g for fresh and frozen fish
(ISIRI, 1999).
The results of total microbial count
showed that microbial load of irradiated
samples (at 1, 3 and 5 kGy) were
significantly (P<0.05) lower than controls
throughout the storage period. This finding
confirms the significant effect (P<0.05) of
irradiation on the reduction of microbial
count. Food spoilage microorganisms are
generally very susceptible to irradiation; a
90% reduction of most vegetative cells can
be accomplished with 1–1.5 kGy (Brewer,
2009). In irradiated samples the highest
and lowest microbial counts were related
to 1 and 3 kGy, respectively. Because the
highest radiation dose in this study (5 kGy)
might induce lipid oxidation. These
reaction metabolites made a good media
for microbial growth. In this study
increasing frozen storage time caused a
significant (P<0.05) reduction effect on
microbial count. Freezing is known to
reduce viable cell counts by 1-2 Log units,
with extended storage causing additional,
time dependent reductions (Yammamoto
and Harris, 2001).
Moini et al. (2009) reported that
irradiation at 1, 3 and 5 kGy had a
significant reduction effect on the total
viable count of rainbow trout fillets.
Ahmed et al. (2009) in evaluating the
efficiency of gamma radiation (3, 5 and 8
kGy) in combination with low temperature
(-20° C) storage of degutted fresh Pampus
chinensis, reported that total bacterial
count (TBC) was affected by the radiation.
In their study, initial bacterial load of
control was maximum (1.3×104 CFU/g)
followed by 3 kGy irradiated fishes (2×102
CFU/g) and at 5 and 8 kGy the samples
were completely sterilized resulting in no
bacterial growth. TBC values in their
investigation suggest that the irradiated
samples remain acceptable after 90 days at
-20°C. Sedeh et al. (2007) reported that
irradiation (0.5, 1, 2 and 3 kGy) and
storage at low temperature had a
significant reduction effect on microbial
loads of bovine meat. They reported that
the combined effect of irradiation and
frozen storage was more effective than
each treatment alone on decreasing total
bacteria counts. Javanmard et al. (2006)
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80 Oraei et al., Effect of Gamma irradiation and frozen storage on microbial……
reported that irradiation (0.75, 3 and 5
kGy) and freezing storage (-18°C) had a
significant reduction effect on microbial
loads of chicken meat. The combination of
frozen storage plus irradiation resulted in
greater overall reductions of microbial
loads, extending shelf life of chicken meat
for commercial application and critical
conditions. Jørgensen and Hansen, (1965)
reported that the irradiation of vacuum-
packed gutted trout at 2 kGy a total viable
aerobic count of 106 CFU/g was not
reached within 4 weeks in ice storage. At
doses of 1 and 0.5 kGy this count was
reached after 26 and 23 days, respectively.
Non-irradiated fish which were spoiled in
the third week of ice storage reached a
count of 106 CFU/g after 15 days.
According to my results, yeasts and
molds were not detected in irradiated
samples at 3 kGy throughout the frozen
storage time and in irradiated samples at 1
and 5 kGy until the end of the third month
of frozen storage. It has been stated that
yeasts and molds are sensitive to the
irradiation process because of their large
genomic structure (Fallah et al., 2010).
Because of some metabolite production in
lipid oxidation and bacterial growth
reactions in 5 and 1 kGy, the population of
yeasts and molds increased in the fourth
and fifth months of frozen storage. Ahmed
et al. (2009) reported that in evaluating the
efficiency of gamma radiation (3, 5 and 8
kGy) in combination with low temperature
(-20° C) storage of degutted fresh Pampus
chinensis, the total mold count (TMC)
increased with the increase of storage
period. So that TMC values were 3.1×105,
5.3×103, 3.8×104 and 3.5×104 CFU/g in
control, 3, 5 and 8 kGy treated samples
respectively at the end of 90 days. Fallah
et al. (2008) reported that the irradiation
dose of 1.5 kGy reduced the initial counts
of yeasts and molds by 2 Log units, while
at 3 kGy yeasts and molds were below the
detection levels during 6 days of storage.
Badr (2004) reported that irradiation of
rabbit meat at 1.5 and 3 kGy significantly
reduced the counts of yeasts and molds by
84% and 94%, respectively. H2S-
producing bacteria such as Salmonella are
generally predominant in spoiled fish flora
(Moini et al., 2009). Because of good
hygienic quality of production, fishing,
handling, filleting, washing and packaging,
coliform bacteria and Salmonella were not
detected in irradiated and control samples.
Radiation sensitivity of non-sporeforming
pathogenic bacteria such as Salmonella in
meat and fishery products is well
documented (Badr, 2004; Fallah et al.,
2008; Moini et al., 2009). Like other gram
negative bacteria, Salmonella and
coliforms have a very low resistance to
radiation. Therefore elimination of these
bacteria by radiation could be beneficial to
the preservation of fish products in view of
the major role that these species play in the
spoilage of fish (Moini et al., 2009). In
addition, rainbow trout fillets were
exposed to quick-freezing and then stored
at -20° C. About 90% of bacteria are
present in fish die at the time of freezing.
These bacteria such as Salmonella spp. are
related to the mesophilic bacteria group.
Psychrophilic bacteria that survive in cold
conditions are inactive until fish are frozen
due to absence of free water for their
growth and activation (Johnstone et al.,
1994). Moini et al. (2009) have reported
that the H2S-producing bacteria in the
control rainbow trout samples reached a
maximum count of 4.89 Log CFU/g on
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Iranian Journal of Fisheries Sciences, 10(1), 2011 81
day 35 and were not observed at dose
levels of 1, 3 and 5 kGy for 7, 21 and 42
days, respectively. Fallah at al. (2008)
have reported that no coliforms were
detected in irradiated (1.5 and 3 kGy)
camel meat during refrigerated storage at
3±1° C. Sedeh et al. (2007) reported that
the optimum dose of gamma radiation in
order to decrease coliforms and specially
for elimination of Salmonella of red meat
was obtained at 3 kGy. With an increase in
irradiation, the number of coliforms
decreased. therefore irradiation
significantly reduced them. Also
irradiation and frozen storage was more
effective than each treatment alone at
decreasing coliform counts. Javanmard et
al. (2006) reported that at the first day of
frozen storage Salmonella Typhimurium
was found in one non-irradiated chicken
meat. However at irradiated samples (0.75,
3 and 5 kGy) no Salmonella was observed.
Irradiation and frozen storage was reported
more effective than each treatment alone at
decreasing total and coliform counts. Badr
(2004) reported that irradiation at 1.5 kGy
was not enough for complete elimination
of Salmonella of rabbit meat, while at 3
kGy Salmonella was not detected.
According to all obtained data from
microbial analysis, low-dose gamma
irradiation (especially 3 kGy) can be
applied for microbial control and the safety
of rainbow trout and shelf life extension in
frozen state. Gamma irradiation at 3 kGy
was more effective than irradiation at 1
and 5 kGy in eliminating microorganisms
of rainbow trout fillets. In addition, the
current study showed the synergistic effect
of two preservation methods, food
irradiation and freezing in low temperature
on extending the shelf-life of rainbow trout
fillet by reducing the microorganism's
load.
Acknowledgments
This study was supported by Iranian
Fisheries Research Organization. We wish
to thank National Fish Processing
Technology Research Center at Anzali
port in Iran for performing the experiments
and Atomic Energy Organization of Iran,
Karaj Nuclear Research Center for
Agriculture and Medicine for performing
the irradiation.
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