Yasemin Yildirim · M ¨uge ˙Inu˘gur Spoilage and shelf life of sardines Sardina pilchardus packed in modified atmosphere Received: 4 August 2005 / Revised: 26 October 2005 / Accepted: 31
Trang 1DOI 10.1007/s00217-005-0194-8
O R I G I NA L PA P E R
Nuray Erkan · ¨Ozkan ¨Ozden ·
Didem ¨ Uc¸ok Alakavuk · S¸ Yasemin Yildirim ·
M ¨uge ˙Inu˘gur
Spoilage and shelf life of sardines (Sardina pilchardus) packed
in modified atmosphere
Received: 4 August 2005 / Revised: 26 October 2005 / Accepted: 31 October 2005 / Published online: 16 December 2006
C
Springer-Verlag 2005
Abstract The effect of modified atmosphere packing
(%)) on the quality of sardine stored in refrigerator was
investigated in terms of sensory, chemical and
microbio-logical analysis Although chemical and microbiomicrobio-logical
analyses indicated that modified atmosphere packing
pro-longed the shelf life of sardine compared with that of air
packing, sensory analysis showed that the extension of shelf
air and MAP storage conditions
Keywords Sardine Modified atmosphere packing
Shelf life Fish quality
Introduction
Storage of fish products on ice under modified atmosphere
packing (MAP) prolongs the shelf life for some days
This is becoming a very favorable alternative for fresh fish
preservation [1] The shelf life of fresh fish is limited by
the growth and biochemical activities of Gram-negative,
psychrotrophic strains of Pseudomonas, Achromabacter,
Flavobacterium and Moraxellla species in the presence of
by packaging of products in an impermeable film under a
con-ditions, the growth of common spoilage microorganisms
is inhibited and microaerophilic strains of lactic acid
bac-teria become the dominant spoilage microorganisms As
a result of the inhibition of spoilage microorganisms,
lev-els of chemical compounds, for example, trimethylamine
N Erkan ( ) · ¨O ¨Ozden · D ¨U Alakavuk · S¸ Y Yildirim ·
M ˙Inu˘gur
Istanbul University, Faculty of Fisheries, Department of the
Seafood Processing and Quality Control,
Ordu Cad No.: 200 34470 Laleli/Istanbul, Turkey
e-mail: nurerkan@istanbul.edu.tr
(TMA), total volatile nitrogen (TVB-N), which are chem-ical indicators of microbial spoilage of food, are also re-duced [3] Many reports have observed that the shelf life
indirectly responsible for the quality deterioration of fish They involve lipolysis, lipid oxidation, and interaction of the products of these processes with nonlipid components such as protein Lipid oxidation takes place mostly in fatty fishes These fishes contain more free lipids and more dark muscles compared to the white muscles The oxidation of the tissue lipids has a very large effect on the quality of fish [7] Lipid deterioration limits shelf life of oily fish such as
gly-colipids and phospholipids are hydrolyzed by lipases to free fatty acids, which then undergo further oxidation to produce low molecular weight compounds, such as alde-hydes and ketones These compounds are responsible for off-flavor, off-odour, and taste of fish [3] Ruiz-Capillas
shelf life of fish products in MAP can be extended, de-pending on raw materials, temperature, gas mixtures, and packaging materials [11] Thus the objective of this study was to determine the effect of MAP storage on the shelf
life of sardine (Sardine pilchardus) by monitoring sensory,
chemical, and microbiological changes throughout
Materials and methods
Fresh sardine (Sardina pilchardus) which is a pelagic
Mar-mara Sea species was obtained from a fishing port Fresh fish in wooden boxes with ice was transported to the lab-oratory in 6 h Twenty kilograms samples were used for the experiment The fishes were ungutted These fishes were individually beheaded, gutted, and washed They were washed once, with tap water after landing Gutting
of the fishes was carried out manually in the fish process-ing plant and were divided into three lots The sardines
Trang 2placed in high-barrier plastic film bags (UPM-Kymmene,
Walki-Pack, Plastic Films Factory (Valkeakoski, Finland)
The characteristics of the plastic film bags were as follows:
90±2% RH g/m2days atm Control samples were packaged
under atmospheric conditions Gas packed in a Henkovac
model E-173, vacuum-packaging machine (Switzerland)
de-terminations were done by triplicate at days 1, 3, 5, 7
and 9
Sensory assessment
The cooked white fishes were assessed using the simplified
Torry Sensory Scheme [12] Panelists were asked to score
odor, taste and texture of fish using a 0–10 acceptability
6= ‘good’, 5.9–4 =‘sufficient’, 4 = ‘limit of acceptable’,
≤3 = ‘unacceptable’.
Chemical analysis
Measurement of pH
Aliquots of 10 sardines were filleted from each sampling
lot and homogenized using a food processor Samples were
prepared according to Manthey et al [13] by blending 5 g of
the homogenate with 10 ml distilled water for 1 min at room
temperature in an Ultra-Turrax (IKA T 25 Basic, Germany)
pH was monitored using a WTW pH Meter (InoLab pH
Level 1 model, Weilheim, Germany) Determinations were
carried out in triplicate at days 1, 3, 5, 7 and 9 during the
storage period
Determination of total volatile basic nitrogen (TVB-N)
Total volatile basic nitrogen was determined according to
the Antonacopoulos and Vyncke, [14] method For total
volatile basic nitrogen, fish muscle (10 g) was
homoge-nized with 6% perchloric acid (90 ml) for 1 min in an
Ultra-Turrax (IKA T 25 Basic, Staufen, Germany) The
homogenates were filtered through a filter paper
(What-man No 1) and filtrates alkalized by NaOH (20%), before
distillation duplicate filtrates were distilled in a Velp Marka
model UDK 140, Milano, ˙Italy apparatus The distillate was
titrated with 0.01 N HCl
Determination of trimethylamin nitrogen (TMA-N)
This was determined by the method of AOAC, [15] Ten
grams homogenized samples were weighed, blended with
90 ml of 7.5% trichloracetic acid solution and filtrated
Blended solution was fixed with formaldehyde (20%) Four milliliters extract was transferred into test tubes and 1 ml
solution were added The tubes were shaken and 5 ml toluene layer was pipetted Five milliliters picric acid work-ing solution (0.02%) was added The contents were mixed and transferred to a spectrophotometric cell Absorbance at
410 nm against the blank was measured At the same time, standards were prepared and measured Results of TVB-N
and TMA-N were expressed as mg/100 g muscle The P
value was calculated according to the following expression [16]
P(%)= TMA− N
TVB− N × 100
Determination of lipid oxidation
The distillation method of Tarladgis et al [17] as modified
by Witte et al [18] was used to determine the degree of lipid oxidation in meat samples Lipid oxidation is mea-sured using tiobarbituric acid (TBA values), which were expressed in mg malonaldehyde/kg meat Malonaldehyde was a breakdown product of lipid oxidation Peroxid value (PV) was determined by a titrimetric Wheeler method [19] after fat extraction [20]
Determination of histamine
Histamine content was determined in triplicate by the en-zyme linked- immunosorbent assay (ELISA) methods [21] with commercial rapid histamine test kits (Veratox his-tamine test kits from Neogen, Lansing, USA and Canada) Results were read using a micro well reader (Neogen Stat Fax 303) with a 650 nm filter
Microbiological analyses Samples (25 g) were mixed with 225 ml of pepton wa-ter (Merck, Kat No.: 107228) diluents in a Stomacher (Stomacher, IUL Instrument, Spain) Further serial dilu-tions were made in tubes before plating The media and incubations were: for mesophilic aerobic plate count PCA
for psychrotrophic bacteria PCA agar (PCA, Merck, Kat
putrefaciens) Iron agar 25 ◦C, 2 days [24]; and for
En-terobacteriaceae VRGB agar (Merck, Kat No.: 110275)
colony forming units (log CFU) per gram of sample Sul-fite reducing Clostridias were determined in Differential Reinforced Clostridial Broth (Merck, 111699) after
Trang 3(MPN, 3 tubes/dilution) method Results were expressed as
log MPN/g of samples Anaerob Clostridias were
investi-gated in the same way, except that an anaerobic atmosphere
kit (Merck, 113829) was placed, together with the plates,
inside the anaerobiosis jar (Merck, 116387) [25]
Statistical analysis
Significant differences between the samples were
calcu-lated by Excel XP 2003 by one-way analysis of variance
Honestly Significant Difference test Pearson’s regression
analysis was performed to determine the correlation
be-tween analyses [26]
Results and discussion
Sensory analysis
Sensory scores of air and MAP packaged sardines
cor-responding limit for taste and odor was reached after 5 days
for control and group A samples, after 7 days for B group
to the species, the initial microbial flora, area of catch,
the method of catching, processing method, and storage
method Pacheco-Aguilar et al [27] Nunes et al [28],
re-ported that the limit of acceptability for whole sardine was
5 days Ozden and G¨oko˘glu [29] concluded that the shelf
life of gutted sardine in refrigerator is extremely limited,
typical 6 days after catch whereas Gennari et al [30]
re-ported that organoleptic rejection of the whole sardine was
reached at 8 days in ice storage The storage life of fish
is affected by the initial microbial load of the fish, storage
temperature, and packing methods This long shelf life of
fish was achieved due to the maintenance of chilled
temper-ature at harvest and during the storage of packing materials
This result is in agreement with those of Dhananjaya and
(60/40) gas mixture on the storage life of herring This
author reported that the stored MAP herring was still
ac-ceptable after 14 days, although the control sample was
barely acceptable after 12 days of storage Storage life
13 days, while air-packaged tilapia has a storage life of
12 days; in vacuum, 9 days and 3 days in air
Chemical analysis
At the beginning of the storage, the pH value was 6.02– 6.03 and 6.03 for sardine in air and MAP The pH val-ues increased to 6.20 by the end of the storage period for sardine packed in air and 6.21 and 6.23 for sardine packed in MAP Values of pH showed statistically
during the entire period of storage The pH increases were
in agreement with the findings of Manthey et al [13], El Marrakchi et al [33] and Nunes et al [28] for other fish species stored in ice During the storage period, the pH value increased according to the storage time, but the pH value is not a criterion of spoilage It has to be supported
by other chemical and sensory analyses [34] The pH of live fish muscle is close to the value 7.0 However, chilled fish pH can vary from 6.0 to 6.5 depending on fish species and other factors [35] In fish, refrigerated in aerobic con-ditions, the rise in pH is mainly due to the production of trimethylamine and other volatile bases due to the spoilage
by bacteria Growth of these species and therefore, gener-ation of trimethylamine and volatile bases were inhibited when samples were stored in carbon dioxide enriched at-mospheres producing a drop in pH [36] Sardine muscle
pH decreases rapidly during postmortem The pH of MAP packaged fish were not good indicators of spoilage [6] The TVB-N content in muscle increased in the period between the first and 9th days of storage in the control and MAP groups Finally, average TVB-N values as
18.19 mg/100 g were determined in groups A and B and
in control groups, respectively after 9 days of storage The TVB-N limit of acceptability (35 mg/100 g) for consump-tion of fish for hake steaks have been reported by Ord´onez
et al [36] as 7 days of storage in air, 11 days when packaged
Table 1 Changes in sensory
analyses in sardine during the
period of iced storage
Texture score of cooked fish
C 9.1±0.1 8.8±0.01 7.8±0.01 5.2±0.1 4.0±0.42
A 9.2 ±0.2 8.7 ±0.2 7.9 ±0.01 5.1 ±0.1 4.0 ±0.33
B 9.1±0.3 8.8±0.01 7.9±0.01 5.2±0.1 4.2±0.20 Odor score of
cooked fish
C 8.9 ±0.5 7.1 ±0.1 5.9 ±0.01 2.8 ±0.2 2.1 ±0.2
B 8.9 ±0.2 7.5 ±0.25 6.12 ±0.3 3.6 ±0.2 2.8 ±0.1 Flavor score of
cooked fish
A 8.9 ±0.6 7.6 ±.0.24 4.2 ±0.1 2.9 ±0.01 2.2 ±0.3
B 9.1±0.4 7.75±0.01 5.1±0.2 4.2±0.01 2.95±0.25 C: control group; A: group A;
B: group B
Trang 4Table 2 Changes in chemical analyses in sardine during the period of iced storage
pH C 6.01 ±0.01 6.06 ±0.003 6.17 ±0.003 6.15 ±0.01 6.20 ±0.02
A 6.03 ±0.003 6.03 ±0.01 6.16 ±0.01 6.12 ±0.003 6.21 ±0.003
TVB-N (mg/100 g muscle) C 10.64 ±0.11 21.31 ±0.09 23.44 ±0.43 26.46 ±0.5 18.19 ±0.19
A 10.60±0.28 20.45±0.52 21.69±0.10 25.41±0.15 36.08±1.3
B 10.88 ±0.16 20.57 ±0.13 24.81 ±0.40 24.4 ±0.38 35.5 ±1.15 TMA-N (mg/100 g muscle) C 2.38±0.03 2.32±0.07 4.11±0.03 6.82±0.08 7.74±0.53
A 2.41 ±0.09 2.61 ±0.05 5.64 ±0.19 6.82 ±0.08 9.69 ±0.25
A 22.73±0.15 12.76±0.09 26.0±0.15 26.84±0.10 26.86±0.07
B 22.61 ±0.10 10.69 ±0.07 13.10 ±0.20 15.41 ±0.45 20.59 ±0.56
A 12.30 ±0.03 26.29 ±0.02 52.56 ±0.02 34.42 ±0.03 52.86 ±0.02
B 12.30±0.04 22.56±0.04 25.94±0.02 23.57±0.04 45.26±0.02
PV (mmol O2/kg) C 2.90 ±0.01 7.28 ±0.02 9.97 ±0.07 10.29 ±0.2 12.11 ±0.28
B 3.60 ±0.03 3.46 ±0.22 7.58 ±0.02 9.70 ±0.35 9.93 ±0.3 TBA (mg malonaldehyde/kg) C 1.02±0.01 5.49±0.03 6.62±0.25 6.43±0.4 7.31±0.03
A 1.08 ±0.07 3.45 ±0.09 7.42 ±0.18 6.98 ±0.1 4.53 ±0.01
C: control group; A: group A; B: group B
TMA are products of bacterial spoilage and their contents
are often used as an index to assess the keeping quality and
the shelf life of seafood products Higher TVB-N values
in the range 25–35 mg/100 g indicate that the fishes were
slightly decomposed/edible and decomposed/inedible
con-centration of TVB-N never reaches 20 mg/100 g in many
fatty fishes [39]
The pattern of increase in the TMA-N value from day
0 to day 9, for sardines kept under three different packing
TMA-N values is fairly linear with storage time in three
level of TMA-N between sardine held in air and in group
A and particularly in groups B (7 days) The observed
shelf life of sardines was found to be 9 days (TMA-N
value, 7 mg/100 g) in group B, 7 days (TMA-N value,
6.82 mg/100 g) in group A and for fish stored in air Initial
P values under air and MAP packaged sardines were 22.36,
22.73 and 22.61%, respectively The value of P increased
and its level reached more than 42.55% for air treatment,
26.86% for group A and 20.59% for group B
Initial values of TMA in muscle from these values
agreed with Morocco sardine [33], for mackerel [40],
and for herring [41] In the postmortem animal, enzymes
from spoilage microorganisms primarily metabolize the
extractive fraction of the fish muscle, producing a wide
variety of volatile compounds resulting in off-flavors and
odors [42] Trimethylamine oxide (TMAO), found in a
large number of marine fish and shellfish, is broken down to
trimethylamine (TMA) either by the endogenous enzymes
The quantitative level of TMA in fish is considered a major index of the quality of marine fish [44] The rejection limit is usually 5–10 mg TMA-N/100 g muscle; however,
in numerous fatty fishes the concentration of TMA-N never reaches the limit of 5 mg TMA-N/100 g [39] Ababouch et al [38] reported similar levels of TMA-N (5–10 mg/100 g) of sardine El Marrakchi et al [33] proposed that TMA-N levels for first grade, second grade,
muscle of fish sample, respectively G¨oko˘glu et al [45]
TMA-N levels at day 0 and 10 were 1.45 and 10.1 mg TMA-N/100 g muscle, respectively The level of TMA was typically around 10–15 mg/100 g, in aerobically stored fresh fish, rejected by sensory panels [46] The concentration of TMA was found to be 13.5 mg in herring
of TMA sardines in air, followed by sardines stored in vacuum packed and the lowest in MAP with the same
trimethylamine production in MAP-cod, but it is on the
results have been reported by Hoz et al [49] and Ord´onez
et al [36] for salmon steak and hake slices under carbon dioxide enriched atmospheric conditions with TMA con-tent lower than that of air conditions Pastoriza et al [50]
TMA-N value of tilapia, 0.07 mg/100 g This value
Trang 5increased to 2.59 mg/100 g after 9 days (rejection time) of
storage in air packed samples and 1.83 mg/100 g after 13
Biogenic amines are formed in foods by the bacterial
and enzymatic decarboxylation of free amino acids They
are of great importance from the point of food intoxication
and also as chemical indicators of spoilage Histamine, a
biogenic amine, is rarely found in fresh fish, but its level
increases with the progress of fish decomposition
Infor-mation is presently available only on the production of
histamine and other biogenic amines in fish such as tuna,
mackerel, sardine, horse mackerel, anchovy, mahi-mahi,
and flying fish [52] A biogenic amine level has been
pro-posed as another way for assessing fish hygienic quality
[53] Histamine value increased after day 3 of storage in the
samples kept in air and MAP In these samples, a histamine
value of approximately 46 ppm after 5 days of storage was
recorded, close to the value of decomposed limit (50 ppm)
for fish in FDA In samples, stored in modified atmospheres,
these bases were produced at a slower rate reaching a value
close to 52 and 45 ppm by 9th day in sardine packaged
respectively Jhaveri et al [54] found initial histamine level
of 20 ppm in Atlantic mackerel They also stated that the
levels increased to value of 100 ppm in 15 days in ice El
Marrakchi et al [33] reported that the amount of histamine
in sardine flesh at the time of rejection (12 days) in ice was
162 ppm Pacheco-Aguilar et al [27] found a very small
amount of histamine (1.8 ppm) in Monterey sardine
mus-cle in ice The content of histamine sardine stored in air
day of sensory acceptability At the time of rejection, the
contents of histamine in herring and mackerel stored in VP
[49] reported that histamine in salmon steaks, at the time
(40/60)) Ord´onez et al [36] found that histamine
concen-tration increased during refrigerated storage of hake steaks
(40/60)) 8.46 ppm Histamine is a chemical hazard
moni-tored by the Food and Drug Administration of the USA for
the safety of seafood products Current FDA [56] guidelines
have established histamine levels of 200 ppm as indicative
of contamination in tuna, 500 ppm as indication of serious
health hazard and lately defined a new hazard action
The increase in PV, which is considered as the starting
point of spoilage, began on day 3 in the control, on days
and 5 mg malonaldehyde/kg TBA value is taken as a limit
of acceptability for consumption of fish, air and in the
a shelf life of 3 days, whereas it would be extended up to 5
atmo-sphere The effect of autolytic enzymes on seafood spoilage
resulting from hydroperoxide formation has been discussed
already However, there are other types of spoilage related
to hydroperoxide formation that are nonenzymatic, namely, oxidative rancidity and nonenzymatic browning These are mainly due to chemical changes in muscle tissues as a re-sult of a wide range of factors, particularly the nature of the lipids Oxidative rancidity has been long recognized as a major cause of seafood and food spoilage The process in-volves oxidation of unsaturated fatty acids or triglycerides
in seafood [3] Factors that may influence lipid oxidation, and thus seafood spoilage, include free radical mechanism, various biochemical substances, temperature, water activ-ity, pH, and chemical environment [57] The primary prod-uct of lipid oxidation is fatty acid hydroperoxide, measured
as peroxide value TBA value measured as secondary prod-uct of lipid oxidation TBA consists mainly of malondialde-hyde as representative of aldemalondialde-hydes [9] Ludorff and Meyer, [34] proposed the following Peroxide value (PV) scale as a
good’, PV =2–5 ‘good’, pH=5–8 ‘acceptable’, pH=8–10
G¨oko˘glu, [8] correlated sensory evaluation with oxidation
malonaldehyde/kg muscle for incipient and moderate ox-idation, respectively TBA index is widely used indicator for the assessment of degree of lipid oxidation [59] It was suggested that a maximum level of TBA value indicating the good quality of the fish frozen, chilled or stored with ice is 5 mg Malonaldehyde/kg [28]
Microbiological analysis There was an initial lag phase with no significant growth
of all microorganisms (aerobic, psychrotrophic, sulphide producing bacteria, Enterobacteria and sulphide reducing
3 and 5 After 5 days in control group samples there were no further significant increases in surface counts
(p <0.05) showing that the stationary phase in bacterial
growth had been attained The results of microbiological analysis showed that fish started to spoil after 5 days be-cause of bacterial activity
to delay spoilage of fresh seafood by inhibiting psy-chrotrophic, aerobic, and Gram-negative bacteria [5] Ini-tial bacterial population, gas/fish ratio, and packaging ma-terials are important factors affecting the shelf life of fish in packages [60] Gobantes et al [61] have accepted the
industry generally considers spoilage to occur when the
refriger-ated squid, the microbial limit of acceptability is
et al [64] reported that mesophilic aerobic counts showed
a slight increase for redfish during storage, reaching a value
Trang 6Table 3 Changes in microbiological analyses in sardine during the
period of iced storage
Psychrotrophic
bacteria count
(log cfu/g)
Total aerob mesophilic
bacteria count
(log cfu/g)
C 3 3.30 3.95 3.70 3.70
H2S-producing
bacteria counts
(log cfu/g)
C 3 3.47 4.70 4.18 3.70
Enterobacteriaceae
(log cfu/g)
Pseudomonas spp
(log cfu/g)
Sulphide reducing
Clostridia’s
(log MPN/g
C 0.47 0.47 0.56 1.63 0.87
A 0.47 0.47 0.47 0.96 0.96
B 0.48 0.56 0.48 1.63 0.96 C: control group; A: group A; B: group B
ex-ceed microbiological limit Jhaveri et al [54] reported that
an initial mesophilic aerobic count of iced Atlantic
day 15 Eifert et al [65] reported hybrid striped bass
Handumrongkul and Silva, [66] however, reported a count
of 6–7 log cfu/g for striped bass after 12 days of under MAP
refrigeration Reddy et al [6] found initial aerobic bacteria
counts and anaerobe bacteria count in MAP packed tilapia
were 4.3 and 3.2 log cfu/g, respectively This count reached
packed tilapia samples Villemure et al [4] reported
packed gutted cod are lower than in air packed samples
the amount of mesophilic bacteria count in herring flesh
at the time of rejection in MAP (10 days) and in vacuum
initial TVC of iced sardines 4log cfu/g, reaching the limit
packing and at day 10, for MAP Bacterial spoilage under
aerobic storage conditions of refrigerated fish to
Gram-negative psychrotrophic organisms dominated by
Pseu-domonas spp and Shewanella spp [67] Psudomonas are
effectively inhibited by atmospheres enriched with 20% or
more of carbon dioxide although Shewanella is more
inhib-ited by higher carbon dioxide concentrations (about 40%)
<3 log cfu/g for groups A and B samples, respectively,
during the 5 day period of storage refrigerator Many
bac-teria are endowed with histidine decarboxylase activity, but
only few species have been associated with histamine pro-duction during fish spoilage [49] Vaz-Pirez and Barbosa [69] reported for seafood the Enterobacteriaceae limit as
3 log cfu/g Statistical analysis showed significant
differ-ences only for the Enterobacteriaceae counts results in
Cor-relation between microbial counts and histamines results
determined for control group sardine: r, 0.6657; for group
A sardine: r, 0.8401, and for B group sardine: r, 0.9248.
Ruiz-Capillas et al [10] found initial of Enterobacteriaceae counts 2.92 log cfu/g in hake slices They also stated that
the Enterobacteriaceae counts increased to value of 4–5
log cfu/g in MAP samples in 10 days The inhibitory
storage in 14 days Initial Pseudomonas spp counts of all
samples after 7 days of storage whereas the MAP samples could not reach this content (3 log cfu/g) after 5 days of
reduc-ing anaerobe Clostridia’s counts ranged from 0.47–0.48 log MNP/g for control and MAP sardine samples These counts exceed very high levels after 5 days of storage in all group fish samples
Microbial counts (total plat count, psychrotrophic
Clostridias, Pseudomonas, Enterobacteriaceae), biochem-ical parameters (pH, total volatile nitrogen, trimethylamin
sardine (Sardina pilchardus) under MAP atmosphere
(%)) and air atmospheres were determined Control group samples (in air atmosphere packing) were unfit for human
5/35/60 (%)) were spoiled after 5 days Group B samples
3 days and ‘good quality’ up to 7 days The samples were
unfit for human consumption after 7 days
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