1419

Journal of Food Protection, Vol. 72, No. 7, 2009, Pages 1419–1426

Copyright 䊚, International Association for Food Protection

Effect of Gamma Radiation on the Quality and Shelf Life of

Refrigerated Rainbow Trout (Oncorhynchus mykiss) Fillets
SOHRAB MOINI,1 REZA TAHERGORABI,2* SEYED VALI HOSSEINI,3 MOHAMMAD RABBANI,4
ZOYA TAHERGORABI,5 XESÚS FEÁS,6 AND FEREIDOON AFLAKI4

1Department of Food Science and Technology, University of Tehran, P.O. Box 31587-77871, Karaj, Iran; 2Animal and Nutritional Sciences,
West Virginia University, P.O. Box 6108, Morgantown, West Virginia 26506-6108, USA; 3Department of Environmental and Fishery Sciences,
University of Tehran, 31585-4314, Karaj, Iran; 4Department of Fishery, Azad University, Tehran North Campus, P.O. Box 19737-33583,
Tehran, Iran; 5Iran University of Medical Sciences and Health Services, P.O. Box 14155-5983, Tehran, Iran; and 6Departamento de Quı́mica
Analı́tica, Nutrición y Bromatoloxı́a, Universidade de Santiago de Compostela, E-27002 Lugo, Galiza, Spain

MS 08-527: Received 18 October 2008/Accepted 1 February 2009

Downloaded from http://meridian.allenpress.com/doi/pdf/10.4315/0362-028X-72.7.1419 by guest on 23 June 2020

ABSTRACT
The effect of gamma radiation (0, 1, 3, and 5 kGy) on the shelf life of farmed rainbow trout (Oncorhynchus mykiss)
fillets that were treated with sodium acetate and vacuum packaged and subsequently stored under refrigeration was studied by
measuring microbiological, chemical, and organoleptic changes. Radiation affected populations of bacteria, namely, H2S-
producing bacteria and Enterobacteriaceae (P ⬍ 0.05). Initial total viable counts of the control samples were ca. 4.41 log
CFU/g, whereas the respective counts in samples irradiated at 1, 3, and 5 kGy were 3.08, 1.46, and ⱕ1 log CFU/g at day 1
of refrigerated storage. The maximum count of Enterobacteriaceae reached 2.29 and 1.45 log CFU/g at the end of storage for
1 and 3 kGy, respectively, but at a 5-kGy dose no growth of Enterobacteriaceae was observed. Of the biochemical indicators,
thiobarbituric acid values for irradiated trout were higher than for nonirradiated fish (P ⬍ 0.05). Sensory evaluation (taste)
showed a reasonable and good correlation with bacterial populations with storage time. The results revealed that radiation at
a high dose (5 kGy) might induce lipid and protein oxidation, although the growth of microorganisms was inhibited. Therefore,
radiation at a low dose (3 kGy) could be used to control the microbial and safety biochemical indices of O. mykiss for up to
4 weeks at refrigerator temperature without adverse effects on quality and acceptability.

The shelf life and safety of refrigerated fish and fish
products are dictated by the presence of food spoilage and
pathogenic microorganisms (38). Spoilage of refrigerated
fish results from microbial growth and/or activity, which
manifests itself as changes in the sensory characteristics
(production of off-odor and off-taste, slime formation, pro-
duction of gas, etc.) (19).
Fish and shellfish are also known to be carriers of sev-
eral pathogenic microorganisms that are implicated in food-
borne diseases (13). The presence of spoilage and patho-
genic microorganisms in seafood is a major concern for the
fish processing industry, the administration, and consumers.
Despite improved manufacturing facilities and implemen-
tation of effective process control procedures such as haz-
ard analysis and critical control points in the food indus-
tries, the number of foodborne illnesses has increased (54).
This risk factor has prompted food scientists worldwide to
reassess their techniques of food safety assurance in order
to preserve or extend the shelf life of various aquatic food
products (7).
Many methods, including low-temperature storage
(21), reduction of water activity (e.g., smoking (5) and salt-
ing (28)), chemical treatments (e.g., antioxidant treatment
(53)), and novel techniques such as high-pressure treatment
(8) and use of lactic acid bacteria (LAB) metabolites (e.g.,
* Author for correspondence. Tel: ⫹1-304-906-6268; Fax: ⫹1-304-293-
2232; E-mail: Rtahergorabi@gmail.com.
bacteriocins (6)) have been developed for extending the
shelf life and hygienic quality of fish commodities. Re-
cently, as a result of advances in irradiation technology, use
of ionizing radiation has been practiced in fish industries
(9, 41, 52). Gamma radiation at low doses is a cold process
that has been accepted by several countries for extension
of shelf life of marine and freshwater fishery products (25,
55). According to the Joint Expert Committee of Food and
Agriculture Organization/World Health Organization/Inter-
national Atomic Energy Agency (FAO/WHO/IAEA), irra-
diation of any food commodity up to an overall average
dose of 10 kGy presents no toxicological hazard. There has
been worldwide interest in using this technology for pres-
ervation of various foods, including fishery products (25,
56). In addition to the extension of shelf life, this treatment
also improves the hygienic quality and safety of the prod-
ucts (32). According to Mendes et al. (41) there is no con-
troversy among the experts that food irradiation is an eco-
nomical and effective food preservation method that has
been validated in at least 39 countries and approved for 49
different products. Although irradiation is an effective
means for extending the shelf life of fishery products (45),
indirect effects, including the acceleration of lipid oxida-
tion, hydrolysis, and vitamin destruction, still limit its ap-
plication in some food products (14, 46).
In addition to irradiation, vacuum packaging of fresh
fish prior to irradiation was considered essential in order to
1420 MOINI ET AL.
prevent or delay microbial activity and also chemical
changes during postradiation refrigerated storage (9, 29).
Furthermore, several studies have shown that vacuum pack-
aging in combination with chemical preservatives such as
sodium acetate (37) will enhance the shelf life of fish during
storage. So, the main aim of the present study was to eval-
uate the effect of low and medium doses of gamma radia-
tion (1, 3, and 5 kGy), combined with sodium acetate and
vacuum packaging, on the preservation and shelf life of
aquacultured freshwater rainbow trout (Oncorhynchus my-
kiss) fillets, using microbiological, chemical, and organo-
leptic analyses during refrigerator storage.
MATERIALS AND METHODS
Preparation of the samples, irradiation, and storage con-
ditions. A total of 84 freshwater rainbow trout (11 to 12 months
old with average weight and length of 315 ⫾ 17 g and 264 ⫾ 13
mm, respectively) were obtained from a local aquaculture farm
located at Noshahr, in the north of Iran. The fish had not been
starved and were actively feeding on commercial fish feed (from
the Chineh Company, Tehran, Iran). The fish were killed by im-
mersion in ice-cold water (hypothermia) and then transported to
the laboratory within 45 min in foamed polystyrene self-draining
boxes with a suitable quantity of flaked ice (the ice/fish ratio was
⬃3:1, wt/wt). After passing into rigor mortis, the fish were washed
with potable water, skinned, and then filleted manually by use of
a sterile scalpel within ⬃2 h. The preparation process was carried
out in a cold room at a temperature of 7 to 10⬚C. The average
weight of the two fish fillets was 69.4% of the initial average
weight. The fillets were divided into four lots (21 fish in each lot)
and then immersed in separated prechilled (4⬚C) aqueous solution
(2.5%, wt/vol) of sodium acetate for 10 min with a fish-to-dipping
solution ratio of 1:25 (50). After dipping, fillets were allowed to
drain for 4 to 5 min on a sterile stainless wire mesh screen at
10⬚C. Then, each fillet was placed separately in polyamide bags
(S-gruppen, Vinterbro, Norway), 75 ␮m in thickness with an ox-
ygen transmission rate of 30 cm3/m2/24 h atm (the oxygen trans-
mission rate was given by the supplier) (temperature, 23⬚C; rel-
ative humidity, 0%), labeled, and vacuum sealed using a BOSS
N48 vacuum sealer (Boss GmbH, Bad Hamburg, Germany).
Packed samples (both experimental and control) were delivered to
the radiation plant in insulated polystyrene boxes with ice within
12 h of harvesting.
Samples (except controls) were irradiated at the Atomic En-
ergy Organization of Iran (Tehran) using a 60Co radiation source.
The strength of the source was 1,772.264 Ci with a dose rate
capacity of 0.392 Gy/s, and the Gamma Cell 220 (Point source
AECL, IR-79, MDS Nordion International Co. Ltd., Ottawa, On-
tario, Canada) was calibrated by standard Fricke dosimeter. The
doses applied in this study were 1, 3, and 5 kGy, and the actual
doses were within ⫾2% of the target dose. To minimize variations
in the radiation-dose absorption, the boxes were turned 180⬚ half-
way through the irradiation process. During irradiation, the fish
were in flaked ice.
After irradiation, the fish were transported to the laboratory
in ice via insulated polystyrene boxes within 3.5 h and maintained
in a refrigerator (Yakhsaran, Tehran, Iran) at 4 ⫾ 0.5⬚C for 42
days for microbiological, chemical, and organoleptic analysis. The
fillets were sampled on storage days 1, 7, 14, 21, 28, 35, and 42.
On each sampling occasion, three randomly chosen packages from
every group were evaluated microbiologically, chemically, and
sensorially.
J. Food Prot., Vol. 72, No. 7
Microbiological analysis. At each storage interval, 10 g of
sample was aseptically removed and homogenized for 1 min with
90 ml of prechilled (4 ⫾ 0.5⬚C) sterile peptone–physiological sa-
line solution (0.1% neutral peptone–0.85% NaCl; Merck, Darm-
stadt, Germany) in sterile deionized water (pH 7.0 ⫾ 0.05) using
a presterilized Stomacher Lab-Blender (Seward type 400, London,
UK) (42). Further decimal serial dilutions were prepared from this
homogenate in the same chilled sterile diluent. Microbiological
data were expressed as log CFU per gram of fillet. All of the
microbial analyses were performed in triplicate on three subsam-
ples of each of the replicates. All media were purchased from
Oxoid Inc. (London, UK).
In this study, total viable count (TVC) and Pseudomonas
count were determined using plate count agar and Pseudomonas
Agar Base according to the methods of the American Public
Health Association (4) and Mead and Adams (40), respectively.
H2S-producing organisms were enumerated on iron agar Lyngby
by a pour-plating method in anaerobic jars with disposable An-
Downloaded from http://meridian.allenpress.com/doi/pdf/10.4315/0362-028X-72.7.1419 by guest on 23 June 2020
aerocult C bags (Merck) (20). Counts of Enterobacteriaceae and
LAB were determined using violet red bile glucose agar and
deMan Rogosa Sharpe agar according to the method of the Inter-
national Commission on Microbiological Specifications for Foods
(26) and the method of González-Rodriguez et al. (16), respec-
tively.
Chemical analysis. After the sampling for microbial analy-
sis, for all chemical methods, each side (half) of each fillet in each
package was homogenized using a kitchen blender through a plate
(4 mm) for 1 min (SAYA, Model Promeat W-1800, Tehran, Iran)
and analyzed to determine total volatile base nitrogen (TVB-N),
thiobarbituric acid (TBA), and pH, and the other half was used
for sensory assessment. For the chemical analyses, all reagents
were of analytical grade (Merck).
In this study, the TVB-N content of experimental fish was
determined according to the method of Goulas and Kontominas
(17) and expressed in milligrams per 100 g of flesh. The TBA
was determined according to the Kirk and Sawyer (30) method.
The color development was measured at 532 nm by using a UV-
visible spectrophotometer (Jenway 6305, Flested, Dunmow, UK).
TBA value was expressed in milligrams of malondialdehyde
(MDA) per kilogram of fish flesh. The pH of homogeneous mix-
tures of fillets and distilled water (1:10, wt/vol) was determined
using a digital pH-Meter (51). Briefly, a 10-g sample was ho-
mogenized in 100 ml of distilled water for 30 s, and the mixture
was filtered through Whatman no. 42 filter paper (Maidenstone,
England) and maintained at room temperature for 15 min. The pH
value of the filtrate was measured using a digital pH-Meter (Sun-
tex Sp-701, Suntex Instrument Co., Taiwan) with an immersed
electrode according to the manufacturer’s instruction manual at
ambient temperature.
Sensory assessment. The sensorial attributes of cooked fil-
lets were evaluated by a team of five semitrained panelists from
the Department of Fishery, University of Tehran, Iran. Fish sam-
ples (100 g) were cooked individually in a microwave oven (MC-
2007TCR, LG, Korea) at 800 W. The samples were cooked on
50% power for 13 min (15) and served to the panelists after being
cooled to ambient temperature (22 to 23⬚C). Each panelist eval-
uated approximately 20 g of fish. Panelists were asked to score
the odor, taste, and texture of fish by using the Torry scale (44).
Orange juice and water were provided to wash the oral cavity
between treatments. The Torry scale, which is used to evaluate
the freshness of cooked fillets, is a descriptive 10-point scale de-
veloped at the Torry Research Station. This scale has been de-
veloped for lean, medium fat, and fat fish species. Scores are given
J. Food Prot., Vol. 72, No. 7 EFFECT OF GAMMA RADIATION ON QUALITY OF RAINBOW TROUT
from 10 (very fresh) to 3 (spoiled), with a rejection level at 5.5.
It is considered unnecessary to have descriptions below 3, as the
fish is then no longer fit for human consumption (39).
Statistical analysis. On each sampling occasion, three ran-
dom, independent samples from each group were subjected to the
microbiological and chemical analyses and sensory evaluation. All
determinations were performed in triplicate. Descriptive statistics
(means and standard deviations) of analysis results were calculat-
ed for each treatment. All data were subjected to one-way analysis
of variance to test the effects of irradiation. The data were tested
for homogeneity of variances with levels of significance set at P
values of ⬍0.05, and probability values of less than 0.05 were
considered statistically significant (12). Excel and SPSS version
13.5 (SPSS Inc., Chicago, IL) were used for data manipulations
and statistical analysis.
RESULTS AND DISCUSSION
Microbiological analyses. Spoilage of fish is caused
by the growth and activity of specific spoilage organisms,
1421
FIGURE 1. Effect of gamma radiation on
the total viable counts (A), Pseudomonas
spp. (B), H2S-producing bacteria (C), En-
terobacteriaceae (D), and lactic acid bac-
teria (E) of aquacultured freshwater rain-
bow trout (Oncorhynchus mykiss) treated
with sodium acetate, vacuum packaged,
and stored under refrigeration at 4⬚C. ⽧,
Nonirradiated; 䡬 , 1-kGy radiation dose;
䉱, 3-kGy radiation dose; 䡵, 5-kGy radi-
ation dose. Values of ⬍1 log CFU/g of fil-
let are omitted, and significant differences
are not shown.
Downloaded from http://meridian.allenpress.com/doi/pdf/10.4315/0362-028X-72.7.1419 by guest on 23 June 2020
which produce metabolites causing off-odors and conse-
quently cause consumer food rejection (18). However, the
specific spoilage organisms are not the same in every case
and the microbial flora isolated from seafoods differs con-
siderably from one study to another, depending on the spe-
cies of fish, their environment, the mode of capture, and
the type of fish product (whole, whole gutted, fillets, or
slices), as well as the climatic and storage conditions (18).
Nonetheless, Pseudomonas, H2S-producing bacteria, and
LAB are generally predominant in spoiled fish flora, while
different gram-negative bacteria, including Enterobacteri-
aceae, are frequently present (23). In the present work,
changes in the microorganisms of the flesh of O. mykiss
were observed for all measured groups during refrigerator
storage, but all of these parameters were significantly lower
than those of the control (Fig. 1A through 1F) (arithmetic
means ⫾ standard deviation, P ⬍ 0.05).
In the present study, irradiation (at 1, 3, and 5 kGy)
1422 MOINI ET AL.
showed a significant impact on TVC, as its value was lower
(P ⬍ 0.05) than those of the control samples (Fig. 1A).
Although it is widely accepted that the initial microbial load
of freshwater fish varies depending on water conditions and
temperature, most available literature on different fresh-
water fish species (tilapia, striped bass, rainbow trout, silver
perch, and sea bream) reports bacterial counts of 102 to 107
CFU/g (12, 24). Initial total viable counts of the control
samples were ca. 4.41 log CFU/g, whereas the respective
counts in samples irradiated at 1, 3, and 5 kGy were 3.08,
1.46, and ⱕ1 log CFU/g at day 1 of refrigerated storage.
The initial counts indicated an acceptable fish quality, con-
sidering the proposed upper limit for aerobic plate counts
of 5 ⫻ 105 CFU/g for fresh fish (26). Chouliara et al. (9)
reported initial counts for control and irradiated (1 and 3
kGy) sea bream fillets salted with NaCl, vacuum packaged,
and stored in a refrigerator of ca. 4.2, 2.4, and 1.0 log
CFU/g, respectively. Also, Savvaidis et al. (52) reported a
slightly higher initial count of 4.6 log CFU/g (day 1) for
whole vacuum-packaged O. mykiss stored under refrigera-
tion, whereas Jeevanandam et al. (27) and Lakshmanan et
al. (32) reported counts of 4.2 and 4.0 log CFU/g for salted
threadfin bream and whole anchovy stored in ice, respec-
tively. Total mesophilic counts for the control and irradiated
rainbow trout reached an average value of 7 log CFU/g
with storage, which is close to the upper limit of accept-
ability for freshwater and marine fish as defined by the
International Commission on Microbiological Specifica-
tions for Foods (26) after ca. 14 days (0 kGy) and 35 days
(1 kGy), while for 3 and 5 kGy the fish never reached this
population level after 42 days. Savvaidis et al. (52) reported
counts of 7 log CFU/g for vacuum-packaged trout after 9,
14, and 24 days for nonirradiated and irradiated samples at
0.5 and 2 kGy, respectively.
Pseudomonas spp. and H2S-producing bacteria have
been reported to be the specific spoilage microorganisms in
various fish species, including sea bass (43) and rainbow
trout (10) harvested from different arctic, temperate, and
tropical waters. In this study, of the bacterial groups ex-
amined, Pseudomonas spp. had the lowest count in both
groups (irradiated and nonirradiated O. mykiss fillets) (Fig.
1B). It is clear that irradiation reduced (P ⬍ 0.05) the pop-
ulations of Pseudomonas, and especially at 3 and 5 kGy
Pseudomonas organisms were totally eliminated. Lewis et
al. (34) reported that Pseudomonas spp., like other gram-
negative bacteria, are known to have a very low resistance
to irradiation. Therefore, elimination of Pseudomonas by
irradiation could be beneficial to the preservation of fish
products in view of the major role that these species play
in the spoilage of fish (9). Furthermore, one must not forget
that Pseudomonas spp. are obligate aerobic bacteria and
their low population in the control group can be related to
the absence (or very low amount) of oxygen in the package.
In addition, the H2S-producing bacteria in the control
reached a maximum count of 4.89 log CFU/g on day 35
and H2S-producing bacteria were not observed at dose lev-
els of 1, 3, and 5 kGy for 7, 21, and 42 days, respectively
(Fig. 1C). This shows that radiation can reduce the popu-
lation of sulfite-reducing bacteria. This is in agreement with
J. Food Prot., Vol. 72, No. 7
the reduction of H2S-producing bacteria in freshwater and
marine fish (tilapia and Spanish mackerel) by irradiation at
a dose of 1.5 kGy (2) and also of sea bream by irradiation
at 1 and 3 kGy (9).
Enterobacteriaceae were also found to be part of the
spoilage microflora of rainbow trout in salted samples in
refrigerated storage. This finding is consistent with results
reported for different fish species, including fresh Atlantic
salmon (3), sea bass (43), sea bream (9), and rainbow trout
(10), which showed the presence of Enterobacteriaceae at
the end of the storage time of the product under refrigerated
condition. The initial count of Enterobacteriaceae was 1.22
log CFU/g (day 7), and it reached a maximum count of
3.29 log CFU/g for the control sample at the end of the
storage period. The maximum count reached 2.29 and 1.45
log CFU/g at the end of storage for 1 and 3 kGy, respec-
Downloaded from http://meridian.allenpress.com/doi/pdf/10.4315/0362-028X-72.7.1419 by guest on 23 June 2020
tively, but for 5 kGy no growth of Enterobacteriaceae was
observed (Fig. 1D). The presence of Enterobacteriaceae in
the microflora of fish and its spoilage potential must be
considered when fish are obtained from polluted water or
there is a delay in chilling after the catch (35). Furthermore,
the presence of Enterobacteriaceae may occur by cross-
contamination during postprocessing and the filleting pro-
cess. Although this group can grow at low temperatures,
their abundance decreases during ice storage, as they are
poor competitors.
LAB have received particular attention from the food
industry in recent years due to their potential application
as natural preservatives. Short-chain fatty acids such as lac-
tic acid, propionic acid, and butyric acid produced by LAB
may help maintain an appropriate pH and protect against
pathological changes in fish during storage. In this study
the initial LAB count was 1.09 log CFU/g in the control
samples. A final count of 5.07, however, was reached in
the control on the 35th day, whereas samples treated with
1, 3, and 5 kGy reached 4.66, 4.04, and 3.55 log CFU/g,
respectively, at the end of storage. The low LAB count in
this study was expected since LAB tend to grow slowly at
refrigeration temperatures (22). LAB were found to be the
major spoilage microorganisms in fresh vacuum-packaged
Atlantic salmon portions stored at 4⬚C (47).
Chemical analyses. The approximate composition of
the measured edible portions of rainbow trout studied was
as follows: moisture, 72.6% ⫾ 1.12%; fat, 5.73% ⫾ 0.31%;
protein, 18.9% ⫾ 0.63%; and ash, 1.47% ⫾ 0.03%. The
changes in all the biochemical indices measured (TVB-N,
TBA, and pH) observed for the control and the irradiated
rainbow trout during the 42-day storage period under re-
frigeration are shown in Fig. 2A through 2C (P ⬍ 0.05).
The TVB-N may be considered to be a quality index
for unprocessed fishery products. Its increase is related to
the activity of spoilage bacteria and endogenous enzymes
(49). The function of such enzymes results in the formation
of compounds including ammonia, monoethylamine, and
dimethylamine, as well as trimethylamine, imparting char-
acteristics of off-flavors to fish. A level of 35 to 40 mg of
TVB-N per 100 g of fish muscle is usually regarded as an
indication that the product is spoiled (31). However, various
J. Food Prot., Vol. 72, No. 7 EFFECT OF GAMMA RADIATION ON QUALITY OF RAINBOW TROUT
authors have reported different acceptability levels for dif-
ferent fish species, specific treatments, and processing con-
ditions for TVB-N values of 35 to 40 mg/100 g (11), 25
to 30 mg/100 g (36), and 25 to 35 mg/100 g (1). In the
present study, TVB-N values were found to increase grad-
ually with storage period in the control and treated samples
(Fig. 2A). Changes in TVB-N values showed no significant
increase in the control and irradiated samples at 1 and 3
kGy until day 14 of storage. TVB-N values (P ⬎ 0.05) of
ca. 17 to 25 mg of N per 100 g of flesh were observed.
After day 14, TVB-N values for control samples increased
steadily, attaining a final value of 79.8 mg of N per 100 g
of flesh at day 35, whereas the respective values for irra-
diated samples were 52.2 (1 kGy), 39.4 (3 kGy), and 28.2
(5 kGy) mg of N per 100 g of flesh. Since TVB-N is pro-
duced mainly by bacterial decomposition of fish flesh, the
higher level of TVC of nonirradiated samples throughout
the period of storage under refrigeration could account for
the higher TVB-N values of rainbow trout. The TVB-N
acceptance limit of 35 to 40 mg of N per 100 g of flesh
(11) was reached between days 14 and 21 for nonirradiated
samples and between days 21 and 28 for samples irradiated
at 1 and 3 kGy. Samples irradiated at 5 kGy never reached
this level. Suppression of TVB-N values following irradi-
ation at 1.5, 2, and 3 kGy has also been reported for other
fish species such as salted and vacuum-packaged sea bream,
refrigerated carp, whole anchovies, and salted threadfin
bream (9, 24, 27, 32). Therefore, low levels of TVB-N in
samples were due to either a reduced bacterial population
(irradiation) or a decreased capacity of bacteria for oxida-
tive deamination of nonprotein nitrogen compounds (vac-
uum packaging) or both (9).
TBA is a widely used indicator for the assessment of
1423
FIGURE 2. Effect of gamma radiation on
total volatile base nitrogen (A), thiobar-
bituric acid (B), and pH (C) of aquacul-
tured freshwater rainbow trout (Oncorhyn-
chus mykiss) treated with sodium acetate,
vacuum packaged, and stored under re-
frigeration (4⬚C). ⽧, Nonirradiated; 䡬,
1-kGy radiation dose; 䉱, 3-kGy radiation
dose; 䡵, 5-kGy radiation dose.
Downloaded from http://meridian.allenpress.com/doi/pdf/10.4315/0362-028X-72.7.1419 by guest on 23 June 2020
the degree of lipid oxidation. That is an index of lipid ox-
idation measuring MDA content. MDA is formed through
hydroperoxides, which are the initial reaction products of
polyunsaturated fatty acids with oxygen. According to Con-
nell (11), TBA values of 1 to 2 mg of MDA per kg of fish
flesh are usually regarded as the limit beyond which fish
will normally develop an objectionable odor and/or taste.
The results of the present study showed that TBA values
for the control and irradiated rainbow trout samples (Fig.
2B) increased gradually from initial values of ca. 0.4 to 0.9
mg of MDA per kg of flesh to maximum values of ca. 5.29
(nonirradiation) on day 35, and 6.03, 7.26, and 8.21 mg of
MDA per kg of flesh for samples irradiated at 1, 3, and 5
kGy, respectively, on day 28 of storage. After this, TBA
values for both control and irradiated samples decreased
gradually to final values of 4.1, 5.53, 5.95, and 6.47 mg of
MDA per kg of flesh on day 42. It is interesting that the
TBA values for samples irradiated at 1, 3, and 5 kGy were
higher than those for the control samples throughout the
entire storage period. This may be attributed to a higher
concentration of free radicals formed in the substrate upon
irradiation. It is well documented (33) that ionizing radia-
tion is the cause of free radical formation in lipids, which
constitutes the first step of the lipid oxidation chain reaction
leading to carbonyl compound formation. Thus, the higher
the dose, the higher the degree of oxidation (i.e., higher
TBA values) is. The decrease in TBA values after 28 days
of storage may represent the breakdown of MDA to tertiary
degradation products. Similar behavior of TBA values for
nonirradiated and irradiated sea bream (filleted) and whole
anchovy was reported by Chouliara et al. (9) and Laksh-
manan et al. (32). The present results are also comparable
to those obtained for irradiated Indian fish species (14).
1424 MOINI ET AL.
FIGURE 3. Effect of gamma radiation on
odor (A), taste (B) and texture (C) score
of aquacultured freshwater rainbow trout
(Oncorhynchus mykiss) treated with sodi-
um acetate and vacuum-packed stored un-
der refrigeration (4⬚C). ⽧, Nonirradiated;
䡺, 1-kGy radiation dose; 䉱, 3-kGy radi-
ation dose; 䡵, 5-kGy radiation dose.
The pH value of live fish muscle is close to 7.0; how-
ever, postmortem pH can vary from 6.0 to 7.0 depending
on the season, the species, and other factors. In the present
study, changes in pH during storage were not statistically
significant (P ⬎ 0.05) between treatments. Values of pH
for the control and irradiated rainbow trout samples re-
mained between 6.25 and 6.8. Similarly, Chytiri et al. (10)
found pH values between 6.43 and 6.52 for rainbow trout
(filleted) stored in ice and Chouliara et al. (9) reported pH
values of between 6.6 and 6.8 for nonirradiated and irra-
diated sea bream (filleted) treated with sodium acetate, vac-
uum packaged, and stored refrigerated. An initial slight de-
crease in pH values may be attributed to the dissolution of
CO2 in the fish muscle, and a secondary increase in pH
may be attributed to the production of volatile base com-
pounds such as ammonia and trimethylamine as well as
other biogenic amines by fish spoilage bacteria (49).
Sensorial analysis. Freshness is the single most im-
portant attribute when assessing fish quality. Microbiolog-
ical, biochemical, and sensory changes are associated with
deterioration of fish quality during handling and storage.
Although a variety of biochemical, physical, and microbi-
ological methods have been used to assess fish freshness,
sensory evaluation is still the most satisfactory method of
achieving such a goal (48).
Acceptability scores for odor, taste, and texture of
cooked control and irradiated rainbow trout decreased with
J. Food Prot., Vol. 72, No. 7
Downloaded from http://meridian.allenpress.com/doi/pdf/10.4315/0362-028X-72.7.1419 by guest on 23 June 2020
the time of refrigerated storage as shown in Figure 3A
through 3C. A score of 5.5 was taken as the lower limit of
acceptability, which is equivalent to a slight off-odor or off-
taste development (39). Odor (Fig. 3A) and taste (Fig. 3B)
showed a similar pattern of decreasing acceptability. The
lower limit of acceptability of odor and taste was reached
between days 7 and 14 for the control samples and between
days 21 and 28 (for doses of 1 and 3 kGy) and between
days 28 and 35 (for doses of 5 kGy) for the irradiated
samples. Texture scores for both control and irradiated rain-
bow trout (Fig. 3C) decreased at a slower rate than odor
and taste scores. Interestingly, the limit of acceptability for
texture was reached only for the control samples at 42 days.
In general, the higher texture scores of both control and
irradiated fish samples throughout the entire period of re-
frigerated storage may be due to salting (treating of fillets
with sodium acetate), which slows down textural changes
by decreasing the activity of proteolytic enzymes (cathep-
sins) in fish muscle. Jeevanandam et al. (27) reported that
salting of threadfin bream prior to irradiation improved the
texture of irradiated fish samples. Taste data (Fig. 3B) of
cooked rainbow trout correlated rather well with the micro-
biological data (Fig. 1A).
Given that specific spoilage-causing microorganisms
cannot be detected by organoleptic or chemical testing, it
is useful to conduct microbiological, chemical, and organ-
oleptic analyses when assessing the quality of fish.
J. Food Prot., Vol. 72, No. 7 EFFECT OF GAMMA RADIATION ON QUALITY OF RAINBOW TROUT
In this research work, a shelf life of 4 weeks was ob-
tained for aquacultured rainbow trout, dipped in sodium
acetate, vacuum packaged, and irradiated at 1, 3, and 5 kGy
under refrigeration, in comparison to a shelf life of only 2
weeks for the nonirradiated vacuum-packaged and sodium
acetate–dipped rainbow trout.
ACKNOWLEDGMENTS
The authors thank J. M. Regenstein from the Department of Food
Science at Cornell University, Ithaca, NY, and Barbara A. Rasco from the
Department of Food Science and Human Nutrition at Washington State
University, Pullman, for their critical review of the manuscript.
REFERENCES
1. Ababouch, L. H., L. Souibri, K. Rhaliby, O. Ouahdi, M. Battal, and
F. F. Busta. 1996. Quality changes in sardines (Sardina pilchardus)
stored in ice and at ambient temperature. Food Microbiol. 13:123–
132.
2. Abu-Tarboush, H. M., H. A. Al-Khatami, M. Atia, A. A. Abou-Arab,
A. S. Bajaber, and M. A. El-Mojaddidi. 1996. Irradiation and post
irradiation storage at 2 ⫾ 2 degrees C of tilapia (Tilapia nilotica ⫻
T. aurea) and Spanish mackerel (Scomeromorus commerson): sen-
sory and microbial assessment. J. Food Prot. 59:1041–1048.
3. Amanatidou, A., O. Schluter, K. Lemkau, L. G. M. Gorris, E. J.
Smid, and D. Knorr. 2000. Effect of combined application of high
pressure treatment and modified atmospheres on the shelf life of
fresh Atlantic salmon. Innov. Food Sci. Emerg. Technol. 1:87–98.
4. American Public Health Association. 1992. P. 153–168. In C. Van-
derzant and D. F. Splittsloesser (ed.), Compendium of methods for
the microbiological examination of foods, 3rd ed. American Public
Health Association, Washington, DC.
5. Aminullah Bhuiyan, A. K. M., W. M. N. Ratnayake, and R. G. Ack-
man. 1986. Effect of smoking on the proximate composition of At-
lantic mackerel. J. Food Sci. 51:327–329.
6. Arlindo, S., P. Calo, C. Franco, M. Prado, A. Cepeda, and J. Barros-
Velázquez. 2006. Single nucleotide polymorphism analysis of the
enterocin P structural gene of Enterococcus faecium strains isolated
from non-fermented animal foods. J. Mol. Nutr. Food Res. 50:1229–
1238.
7. Chang, K. L. B., J. J. Changm, C. Y. Shiau, and B. S. Pan. 1998.
Biochemical, microbiological, and sensory changes of sea bass (La-
teolabrax japonicus) under partial freezing and refrigerated storage.
J. Agric. Food Chem. 46:682–686.
8. Chevalier, D., A. L. Bail, and M. Ghoul. 2001. The effect of high
pressure treatment (100–200 MPa) at low temperature on turbot
(Scophthalmus maximus) muscle. Food Res. Int. 32:707–713.
9. Chouliara, I., I. N. Savvaidis, N. Panagiotakis, and M. G. Konto-
minas. 2004. Preservation of salted, vacuum-packaged, refrigerated
sea bream (Sparus aurata) fillets by irradiation: microbiological,
chemical and sensory attributes. Food Microbiol. 21:351–359.
10. Chytiri, S., I. Chouliara, I. N. Savvaidis, and M. G. Kontominas.
2004. Microbiological, chemical, and sensory assessment of iced
whole and filleted aquacultured rainbow trout. Food Microbiol. 21:
157–165.
11. Connell, J. 1995. Control of fish quality, 4th ed., p. 157, 159–160.
Fishing News Books Limited, Furnham, Surrey, UK.
12. Duncan, D. 1955. Multiple range tests and multiple F tests. Biomet-
rics 11:1–42.
13. Garrett, E. S., M. L. Jahncke, and J. M. Tennyson. 1997. Micro-
biological hazards and emerging food safety issues associated with
seafoods. J. Food Prot. 60:1409–1415.
14. Ghadi, S. V., and V. Venugopal. 1991. Influence of ␥-irradiation and
ice storage on fat oxidation in three Indian fish. Int. J. Food Sci.
Technol. 26:397–401.
15. Gokoglu, N., P. Yerlikaya, and E. Cengiz. 2004. Effects of cooking
methods on the proximate composition and mineral contents of rain-
bow trout (Oncorhynchus mykiss). Food Chem. 84:19–22.
16. González-Rodriguez, M., J. Sanz, J. Santos, A. Otero, and M. Gar-
1425
cia-López. 2002. Numbers and types of microorganisms in vacuum-
packed cold-smoked freshwater fish at the retail level. Food Micro-
biol. 77:161–168.
17. Goulas, A. E., and M. G. Kontominas. 2005. Effect of salting and
smoking method on the keeping quality of chub mackerel (Scomber
japonicus): biochemical and sensory attributes. Food Chem. 93:511–
520.
18. Gram, L., and P. Dalgaard. 2002. Fish spoilage bacteria—problems
and solutions. Curr. Opin. Biotechnol. 13:262–266.
19. Gram, L., and H. Huss. 1996. Microbiological spoilage of fish and
fish products. Int. J. Food Microbiol. 33:589–595.
20. Gram, L., G. Trolle, and H. H. Huss. 1987. Detection of specific
spoilage bacteria from fish stored at low (0⬚C) and high (20⬚C) tem-
peratures. Int. J. Food Microbiol. 4:65–72.
21. Himelbloom, B. H., C. Crapo, E. K. Brown, J. Babitt, and K. Re-
pond. 1994. Pink salmon (Onchorynchus gorbuscha) quality during
ice and chilled seawater storage. J. Food Qual. 17:197–210.
22. Huis in’t Veld, J. H. J. 1996. Microbial and biochemical spoilage of
foods: an overview. Int. J. Food Microbiol. 33:1–18.
Downloaded from http://meridian.allenpress.com/doi/pdf/10.4315/0362-028X-72.7.1419 by guest on 23 June 2020
23. Ibrahim Sallam, K. 2007. Antimicrobial and antioxidant effects of
sodium acetate, sodium lactate, and sodium citrate in refrigerated
sliced salmon. Food Control 18:566–575.
24. Icekson, I., and A. Gelman. 1996. Prolonging shelf-life of carp by
combined ionizing radiation and refrigeration. J. Food Sci. Agric.
72:353–358.
25. International Atomic Energy Agency. 1989. Radiation preservation
of fishery products. Technical report series 303. International Atomic
Energy Agency, Vienna.
26. International Commission on Microbiological Specifications for
Foods. 1986. Microorganisms in foods. 2. Sampling for microbio-
logical analysis: principles and specific applications, 2nd ed. Uni-
versity of Toronto Press, Toronto.
27. Jeevanandam, K., A. Kakatkar, S. N. Doke, D. R. Bongiwar, and V.
Venugopal. 2001. Influence of salting and gamma irradiation on the
shelf-life extension of threadfin bream in ice. Food Res. Int. 34:739–
746.
28. Jittinandana, S., P. B. Kenney, S. D. Slider, and R. A. Kiser. 2002.
Effect of brine concentration and brine time on quality of smoked
rainbow trout fillets. J. Food Sci. 67:2095–2099.
29. Killoran, J. J. 1983. Packaging of irradiated food, p. 317–326. In E.
S. Josephson and M. S. Patterson (ed.), Preservation of food by
ionising, vol. 2. Radiation. CRC Press, Boca Raton, FL.
30. Kirk, R. S., and R. Sawyer. 1991. Pearson’s composition and analysis
of foods, 9th ed. Longman Scientific and Technical, London.
31. Lakshmanan, P. T. 2000. Fish spoilage and quality assessment, p.
26–40. In T. S. G. Iyer, M. K. Kandoran, Mary Thomas, and P. T.
Mathew (ed.), Quality assurance in seafood processing. Society of
Fisheries technologists, Cochin, India.
32. Lakshmanan, R., V. Venugopal, K. Venkateshwaran, and D. R. Bon-
giwar. 1999. Bulk preservation of small pelagic fish by gamma ir-
radiation: studies on a model storage system using anchovies. Food
Res. Int. 32:707–713.
33. Lee, M., J. G. Sebranek, D. G. Olson, and J. S. Dickson. 1996.
Irradiation and packaging of fresh meat and poultry. J. Food Prot.
59:62–72.
34. Lewis, N. F., M. D. Alur, and U. S. Kumta. 1971. Radiation sensi-
tivity of fish microflora. Indian J. Exp. Biol. 9:45–47.
35. Lindberg, A.-M., A. Ljungh, S. Ahrné, S. Lödfhahl, and G. Molin.
1998. Enterobacteriaceae found in high numbers in fish, minced meat
and pasteurized milk or cream and the presence of toxin encoding
genes. Food Microbiol. 39:11–17.
36. Lopez-Caballero, M. E., M. Perez-Mateos, P. Montero, and A. J.
Borderias. 2000. Oyster preservation by high-pressure treatment. J.
Food Prot. 63:196–201.
37. Manju, S., L. Jose, T. K. Srinivasa Gopal, C. N. Ravishankar, and
K. V. Lalitha. 2007. Effects of sodium acetate dip treatment and
vacuum-packaging on chemical, microbiological, textural and sen-
sory changes of Pearl spot (Etroplus suratensis) during chill storage.
Food Chem. 102:27–35.
38. Martin, J., and J. O. Hearnsberger. 1994. Evaluation of impedance
1426 MOINI ET AL.
microbiology for rapid assessment of shelf-life and quality of pro-
cessed channel catfish, Ictalurus punctatus. J. Appl. Aquaculture 3:
353–362.
39. Martinsdottir, E. 2002. Quality management of stored fish, p. 173–
190. In A. H. Bremner (ed.), Safety and quality issues in fish pro-
cessing. Woodhead Publishing Limited, Cambridge.
40. Mead, G. C., and B. W. Adams. 1977. A selective medium for the
rapid isolation of Pseudomonas associated with poultry meat spoil-
age. Br. J. Poultry Sci. 18:661–670.
41. Mendes, R., H. Alve Silva, M. Leonor Nunes, and J. M. Abecassis
Empis. 2005. Effect of low-dose irradiation and refrigeration on the
microflora, sensory characteristics and biogenic amines of Atlantic
horse mackerel (Trachurus trachurus). J. Eur. Food Res. Technol.
221:329–335.
42. Nedohula, P. C., and D. Westhoff. 1997. Microbiological analysis of
striped bass grown in three aquaculture systems. Food Microbiol.
14:255–264.
43. Papadopoulos, V., I. Chouliara, A. Badeka, I. N. Savvaidis, and M.
G. Kontominas. 2003. Effect of gutting on microbiological, chemi-
cal, and sensory properties of aquacultured sea bass (Dicentrarchus
labrax) stored in ice. Food Microbiol. 20:411–420.
44. Pons-Sánchez-Cascado, S., M. C. Vidal-Carou, M. L. Nunes, and M.
T. Veciana-Nogués. 2006. Sensory analysis to assess the freshness
of Mediterranean anchovies (Engraulis encrasicholus) stored in ice.
Food Control 17:564–569.
45. Radomyski, T., E. A. Murano, D. G. Olson, and P. S. Murano. 1994.
Elimination of pathogens of significance in food by low-dose irra-
diation: a review. J. Food Prot. 57:73–86.
46. Rahman, M. S. 1999. Irradiation preservation of foods, p. 397–419.
J. Food Prot., Vol. 72, No. 7
In M. S. Rahman (ed.), Handbook of food preservation. Marcel Dek-
ker, New York.
47. Rasmussen, S. K. J., T. Ross, J. Olley, and T. McMeekin. 2002. A
process risk model for the shelf life of Atlantic salmon fillets. Int.
J. Food Microbiol. 73:47–60.
48. Reineccius, G. 1990. Off-flavours in foods. Crit. Rev. Food Sci.
Nutr. 29:381–402.
49. Ruiz-Capillas, C., and A. Moral. 2005. Sensory and biochemical
aspects of quality of whole bigeye tuna (Thunnus obesus) during
bulk storage in controlled atmospheres. Food Chem. 89:347–354.
50. Sallam, K. I., and K. Samejima. 2004. Microbiological and chemical
quality of ground beef treated with sodium lactate and sodium chlo-
ride during refrigerated storage. Lebensm.-Wiss. Technol./LWT-Food
Sci. Technol. 37:865–871.
51. Santos, C. L. D., D. James, and P. Teutscher. 1981. Guidelines for
chilled fish storage experiments. FAO Fish technical paper no. 210.
Food and Agricultural Organisation, Rome.
52. Savvaidis, I. N., P. Skandamis, K. Riganakos, N. Panagiotakis, and
M. G. Kontominas. 2002. Control of natural microbial flora and Lis-
teria monocytogenes in vacuum-packaged trout at 4 and 10⬚C using
Downloaded from http://meridian.allenpress.com/doi/pdf/10.4315/0362-028X-72.7.1419 by guest on 23 June 2020
irradiation. J. Food Prot. 65:515–522.
53. Shahidi, F., and P. D. Wanasundara. 1992. Phenolic antioxidants.
Crit. Rev. Food Sci. Nutr. 32:67–103.
54. Soomro, A. H., T. Masud, and K. Anwaar. 2002. Role of lactic acid
bacteria in food preservation and human health—a review. Pakistan
J. Nutr. 1:20–24.
55. Venugopal, V., S. N. Doke, and P. Thomas. 1999. Radiation pro-
cessing to improve the quality of fishery products. Crit. Rev. Food
Sci. Nutr. 39:391–440.
56. World Health Organization. 1994. Wholesomeness of irradiated
food. World Health Organization, Geneva.