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ABSTRACT
This study was conducted to investigate the tenderness properties and microbial
safety of deboned spent hen breast and leg meat samples treated with papain
solutions at different concentrations followed by gamma irradiation at 3 kGy
dose and refrigeration storage at 41 C. Moreover, the effect of irradiation at
the applied does on the proteolytic activity of the enzyme was also examined.
The results indicated that irradiation at 3 kGy dose improved the microbial
safety of papain-treated spent hen meat samples through the significant great
reduction in the counts of total mesophilic and psychrophilic bacteria as well as
the complete elimination of enterobacteriaceae, Staphylococcus aureus, Listeria
monocytogenes and Salmonella spp. Papain solutions at the applied
concentrations (10 mg/ml and 100 mg/ml) retained 41.6% and 79.8% of the
enzyme activity, respectively, after irradiation at 3 kGy dose. However, the
observed residual proteolytic activity of papain (after irradiation of the
enzyme-treated meat samples) induced significant increases in the values of
water holding capacity, cooking yield, solubility of sarcoplasmic and
myofibrillar proteins and collagen solubility of spent hen meat samples.
Moreover, cooked samples of irradiated papain- treated spent hen meat (either
Shawirma, that prepared from breast meat, or the roasted leg meat) received
high sensory scores for their tenderness, juiciness and flavor compared to those
of control samples.
444
INTRODUCTION
After 10-14 months of egg production, laying hens generally produce
fewer and lower quality eggs than younger birds. These older laying hens are
commercially referred to as being "spent hens". These spent hens are considered
under utilized poultry product due to toughness of their meats, the most
important characteristic contributing to their low consumer acceptability. Eating
satisfaction results from the interaction of tenderness, juiciness and flavor, while
tenderness has been identified as the most important factor affecting consumer
satisfaction and perception of the taste 1,2. Thus increasing the utilization of
spent laying hens, as a by-product of the egg industry, is one of the greatest
needs of the poultry industry. There are several means of tenderizing meat
includes treatment by proteolytic enzymes, being one of the popular methods
for meat tenderization. Proteolytic enzymes derived from plants, such as papain,
have been widely used in most parts of the world 2,3.
On the other hand, food safety is a top priority for authorities and
consumers worldwide as the prevalence of foodborne pathogens and the
reported number of cases and outbreaks is still high, affecting personal lives,
business and countries economies4. Nowadays food industries invest
considerable part of their resources to ensure the quality of their products,
mainly with regard to hygiene 5.
From the hygienic point of view, poultry meat has a special position
among all other food products of animal origin, being one of the main products
involved in foodborne infections due to the presence of pathogens included
Salmonella spp., Campylobacter spp., Listeria monocytogenes and others. Even
under the best conditions, it is impossible to produce poultry meat free of
pathogens, and the high prevalence of Salmonella spp in retail poultry reflects
the continued inability of the industry to effectively prevent its spread in raw
poultry meat 5-9.
The highly effective bactericidal properties of ionizing radiation, along
with the fact that irradiation treatment causes practically no temperature rise in
the product and can be applied to muscle foods without major alteration in their
phsyico-chemical or sensory properties, make it an ideal process for the
decontamination of raw chicken meat. The efficiency of gamma irradiation in
445
446
side of the breast fillet to improve the penetration of the enzyme, while the
deboned legs were separated into thigh and drumstick.
Enzyme treatment and marination
Each of the prepared spent hen meat group of samples (breast fillets, leg
thighs, and leg drumsticks) was divided into three main parts. Samples of the
first part were sprayed with the papain- water solution at concentration of 10
mg/ml, while samples of the second part were sprayed with the enzyme solution
at concentration of 100 mg/ml. Samples of the third part were sprayed with
distilled water as a control. After through mixing by hand, meat samples of each
part were individually aerobically packaged in polyethylene pouches and the
pouches were sealed by heat. Special pouches (containing relatively large
amount of samples) were prepared from each part of samples for using in the
sensory evaluation of the cooked samples. Moreover, appropriate samples were
prepared for the microbiological analysis, in which meat samples were minced
and well-mixed under aseptic conditions before packaging (for the uniformity of
samples) in the polyethylene pouches. Pouches of all papain sprayed samples
were transported immediately in an ice chest for irradiation treatment. In
addition, appropriate pouches of the water sprayed samples were also
transported for irradiation treatment to serve as the control samples in the
sensory evaluation of the cooked meat ( for safety precautions), while the rest of
the water sprayed samples were refrigerated stored at 41 C.
Irradiation treatment
Papain-treated samples as well as some of the water sprayed ones were
exposed to gamma irradiation at dose of 3 kGy at room temperature. All
irradiation treatments in this study were carried out using an experimental
Cobalt-60 source at the National Center for Radiation Research and
Technology, Nasr City, Cairo, Egypt.
Storage and sampling for analysis
Irradiated as well as non irradiated spent hen meat samples under
investigation were refrigeration stored at 4 1 C and subjected to the periodical
analysis at 2 days intervals. The rejection of samples was based on the detection
of microbial growth or the mushy texture on the surface of samples (R1) and /or
the detection of off-odor (R2), while values of the rejected samples were
447
discarded after statistical analysis. All analysis in this study were conducted
using three separate pouches (triplicates) and each determination was carried
out in duplicate samples within each replicate.
Analytical methods
Microbial safety
The microbial safety of irradiated and non irradiated raw meat samples of
spent hen meats was assessed during refrigerated storage (41C) throughout
the enumeration of the total mesophilic and psychrophilic bacteria,
enterobacteriaceae, Staphylococcus aureus, Listeria monocytogenes, and the
detection of Salmonella. At time of withdrawal from refrigerated storage, the
outer surface of pouches was sterilized before opening using cotton witted by
70% ethanol. Then 20g aliquots of the minced spent hen meat were removed
aseptically from each of the pouches to prepare the initial 1/10 dilution which
was used for the preparation of other serial dilutions in 0.1 % peptone water.
Colony forming units (CFU) for total mesophilic and psychrophilic bacteria
were determined by plating on plate count agar medium and incubation at 35 C
for 3 days and 7 C for 7 days, respectively 20. Enterobacteriaceae were
enumerated on violet red bile glucose agar medium after incubation for 20-24 h
at 37 C according to Roberts et al., 21. Staphylococcus aureus was counted
using Baird-Parker RPF medium after incubation at 35 C for 24-48 h 22, then
confirmed by the coagulase tests as described by Collins et al. 23. Enumeration
of Listeria monocytogenes was performed (after enrichment using selective
enrichment medium, Oxoid) on Listeria selective medium after incubation at
35 C for 24-48 h 24. Cultures were examined and colonies were biochemically
confirmed according to Bille and Doyle 25.The detection of Salmonella was
carried out using the most probable number technique 26. The samples were
incubated into buffer peptone for 24 h at 37 C. After enrichment at 37 C for
24h in selenite broth, the cultures were streaked on Brilliant green agar and
incubated at 37 C for 24 h, then colonies were biochemically examined in
triple sugar iron agar (TSI) and lysine decarboxilase broth.
Physico-chemical analysis
Moisture content, pH, water holding capacity (WHC) and cooking yield
Moisture contents were determined according to AOAC official methods27.
The pH was assessed using a pH meter on a homogenate consisting of 5g of
448
449
10mg/ml
100mg/ml
80
70
60
50
40
30
20
10
0
Papain concentration
450
Storage
(Days)
Control
Control
Papain
(10mg/ml)
+ 3kGy
Papain
(100mg/ml)
+3kGy
6.043.70g
6.263.62f
6.573.97e
6.724.17d
R2
3.981.69n
3.991.97n
4.062.10lm
4.102.11l
4.122.27kl
4.142.19l
R1
4.051.70m
4.081.86lm
4.092.13lm
4.112.00kl
R1
6.073.72g
6.273.67f
6.584.03e
6.734.21d
R2
3.951.78o
3.991.67no
n
4.002.10
4.021.98mn
kl
4.132.19
4.142.11kl
4.192.17jk 4.201.94j
4.262.29jhi R1
4.292.26hi
R1
5.893.40g
5.993.38f
6.263.70e
6.463.96d
R2
3.311.81o
3.411.92m
3.481.66l
3.571.79k
3.691.90j
3.841.79i
R1
3.321.58no
3.421.80m
3.491.69l
3.581.90k
R1
5.903.32g
6.003.47f
6.283.67e
6.484.04d
R2
3.341.74n
3.421.80m
3.491.78l
3.591.83k
3.691.86j
3.861.82i
R1
3.351.69n
3.431.78m
3.511.81l
3.591.86k
R1
0
5.362.88
ND
ND
5.282.93g
ND
ND
f
5.683.19
ND
ND
5.633.24f
ND
ND
2
5.963.47e
ND
ND
5.963.41e
ND
ND
4
6.213.89d
ND
ND
6.233.91d
ND
ND
6
R2
ND
R1
R2
ND
R1
8
ND
ND
10
R1
R1
12
cfu: colony forming units. ND: Not detected.
R1 and R2: Rejected based on the appearance and odor of the raw meat, respectively. Means with
different superscript within each determination are differ significantly (p<0.05).
451
Storage
(Days)
Control
Control
Papain
(10mg/ml)
+ 3kGy
Papain
(100mg/ml)
+3kGy
0
2
4
6
8
10
12
4.482.00
4.522.04f
4.572.10e
4.621.97d
R2
ND
ND
ND
ND
ND
ND
R1
0
2
4
6
8
10
12
3.321.91g
3.361.73f
3.421.88e
3.481.71d
R1
ND
ND
ND
ND
ND
ND
R2
0
2
4
6
8
10
12
+ve
+ve
+ve
+ve
R2
-ve
-ve
-ve
-ve
-ve
-ve
R1
ND
ND
ND
ND
R1
4.492.05g
4.532.10f
4.582.07e
4.632.13d
R2
ND
ND
ND
ND
ND
ND
R1
ND
ND
ND
ND
R1
3.341.78g
3.371.85f
3.431.77e
3.491.68d
R1
ND
ND
ND
ND
ND
ND
R1
ND
ND
ND
ND
R1
-ve
-ve
-ve
-ve
-ve
-ve
R1
-ve
-ve
-ve
-ve
R1
cfu: colony forming units. ND: Not detected. +ve: positive. ve: negative.
R1 and R2: Rejected based on the appearance and odor of the raw meat, respectively.
Means with different superscript within each determination are differ significantly(P <0.05).
Physico-chemical properties of irradiated papain-treated spent hen meats during cold storage
pH, moisture content, WHC, and cooking yield
Control samples of leg meat showed a significant higher pH value than
that of the breast meat (Table 3).These results was in accordance with the
findings of Kondaiah and Panda 38 and may be due to the differences between
light and dark muscles 39. Papain treatment followed by gamma irradiation had
no significant effects (P <0.05) on the values of pH and moisture contents of
raw spent hen meat samples (Table 3). However, samples of irradiated papaintreated spent hen meat revealed significantly higher (P <0.05) WHC and
452
cooking yield than the control samples during refrigerated storage at 41C
(Table 4).
The muscle pH is highly important and affects the tenderness of meat 40,41.
Moreover, the WHC was found to be very important since many physical
properties such as texture and firmness of raw meat are partially dependent
on the WHC3. The observed results agree with those reported by other
investigators 1, 3, 42.
Storage
(Days)
Table 3. pH values and moisture contents of irradiated papain- treaded spent hen
meat during cold storage (4 1C).
Breast meat
Control
Papain
(10mg/ml)
+ 3kGy
Control
Papain
(10mg/ml)
+ 3kGy
Papain
(100mg/ml)
+3kGy
6.360.2a
pH value
0
2
4
6
8
6.100.02
6.050.01
6.120.02
ab
6.210.03
R2
6.130.02b
6.360.01a
6.340.01a
6.340.01a
6.340.02a
6.360.02a
R1
6.140.03
6.120.01
6.140.02
6.130.02
6.140.03
6.150.02
6.120.2
6.130.01
6.300.02
6.360.01
6.400.03
R1
R2
6.150.02b
10
6.340.01
6.330.02
6.350.02
6.340.01a
R1
12
6.360.03
R1
Moisture content %
0
73.140.32a
72.940.41a
73.000.46a
72.480.44a
72.330.39a
72.460.42a
73.040.41a
73.120.50a
72.930.38a
72.280.46a
72.460.46a
72.380.41a
72.980.38a
73.050.44a
73.120.51a
72.390.38a
72.430.42a
72.410.38a
73.010.44a
73.210.52a
73.010.46a
72.460.41a
72.470.38a
72.390.64a
8
10
12
R2
73.020.39
R1
R2
73.100.41a
R1
72.510.41
R1
72.460.39a
R1
R1 and R2: Rejected based on the appearance and odor of the raw meat, respectively.
Means with different superscript within each determination are differ significantly (P<0.05).
453
Storage
(Days)
Table 4. WHC and Cooking yield of cold stored (4 1 C) spent hen meats as affected by
papain treatment and gamma irradiation.
Breast meat
Control
Papain
(10mg/ml)
+ 3kGy
Papain
(100mg/ml)
+3kGy
40.040.40p
41.300.36o
41.730.42n
41.840.50n
R2
42.410.60m
43.620.42l
45.440.71j
48.130.63g
50.220.81d
51.841.02c
R1
43.650.46l
45.210.51j
47.420.67h
49.830.81e
R1
Control
Papain
(10mg/ml)
+ 3kGy
Papain
(100mg/ml)
+3kGy
35.100.43w
35.260.39v
35.500.44u
35.570.37u
R2
36.880.40s
37.790.43r
39.900.68p
43.510.89l
46.231.00i
48.770.94f
R1
38.040.51q
39.930.76p
42.380.94m
44.601.03k
R1
WHC %
0
2
4
6
8
10
12
Cooking yield %
58.740.81jk 58.910.91jk 59.020.77jk 57.830.91m 58.010.83m 58.040.81lm
0
58.711.01k 59.421.00i 60.330.94gh 57.900.87m 58.430.93l 59.210.86j
2
58.780.92jk 60.041.01h 61.111.02ef 57.911.02m 59.010.71j 60.400.78gh
4
58.910.75jk 60.890.89f 61.880.93d 58.020.94m 60.560.81g 61.120.91ef
6
R2
61.921.00d
R1
R2
61.310.90e
R1
8
b
62.410.94
62.040.78c
10
R1
R1
12
R1 and R2: Rejected based on the appearance and odor of the raw meat, respectively.
Means with different superscript within each determination are differ significantly (P<0.05).
454
In old animals, more intra- and intra- molecular cross- links are formed in
the collagen fibers, and so the amount of solubilization which can occur on
heating is decreased (as in the control samples).Moreover, it has been illustrated
that the enzyme do not attack native collagen and most of the tenderizing occurs
during cooking, between the times when the collagen in the meat melts and the
enzyme is inactivated by heat 46. The observed increase in collagen solubility of
papain-treated samples was consistent with the findings of other authors 1,47.
Storage
(Days)
Table 5. Solubility of sarcoplasmic and myofibrillar proteins during cold storage (4 1C) of
spent hen meat as affected by papain treatment and gamma irradiation.
Breast meat
Papain
(10mg/ml)
+ 3kGy
Control
Papain
(10mg/ml)
+ 3kGy
Papain
(100mg/ml)
+3kGy
13.311.12o
14.621.40m
16.711.54j
18.641.48hi
19.761.77g
21.701.94d
R1
13.861.20n
16.101.48k
18.341.51i
20.941.76f
R1
Control
12.831.10
12.621.07q
12.601.35q
12.611.40q
R2
12.971.22p
14.581.35m
16.641.63i
18.711.52h
19.861.80g
21.932.03d
R1
13.201.37o
15.911.65l
18.481.57i
21.681.86e
R1
12.911.05p
12.731.11pq
12.601.22q
12.611.40pq
R2
Sensory properties
Treatment of spent hen meat with papain followed by gamma irradiation at
3 kGy dose had no significant effects (P <0.05) on the initial sensory attributes
of raw meat samples (Table 7). As shown, similar preference scores were
recorded by the panelists for both treated and control samples indicating that all
samples were highly acceptable as judged by appearance and odor. The same
results show that all samples had an acceptable sensory attributes during
455
Storage
(Days)
Control
Papain
(10mg/ml)
+ 3kGy
4.130.16a
4.140.15a
4.130.16a
4.150.13a
4.130.16a
4.130.14a
6
8
Papain
(100mg/ml)
+3kGy
Papain
(10mg/ml)
+ 3kGy
Papain
(100mg/ml)
+3kGy
4.730.15b
4.750.13b
4.720.15b
4.160.14a
4.750.13b
4.740.16b
4.750.14b
4.160.13a
4.140.16a
4.730.16b
4.760.14b
4.730.16b
4.160.12a
4.150.14a
4.170.13a
4.760.14b
4.780.15b
4.750.14b
R2
4.160.13a
4.750.16b
R1
R1
Control
R2
10
4.150.14a
4.760.14b
12
R1
R1
R1 and R2: Rejected based on the appearance and odor of the raw meat, respectively.
Means with different superscript within each determination are differ significantly (P<0.05).
Solubility %
456
90
80
70
60
50
40
30
20
10
0
Control
Papain (10mg/ml)
+ irradiation
Papain (100mg/ml)
+ irradiation
10
Storage (Days)
90
80
70
Solubility %
60
50
40
30
20
10
0
0
10
Storage (Days)
Fig. 2. Collagen solubility during cold storage (4 1C) of spent hen meat as
affected by papain treatments and gamma irradiation at 3 kGy dose.
457
Table 7. Mean of sensory scores during cold storage (4 1C) of raw spent hen
meat as affected by papain treatments and gamma irradiation.
Storage
(Days)
Control
Breast meat
Papain
Papain
(10mg/ml)
(100mg/ml)
+ 3kGy
+3kGy
Control
8.50.4a
7.9.06ab
8.20.4a
8.40.5a
8.10.4a R2
8.40.3a
8.20.4a
8.30.5a
7.80.3ab
8.10.4a
6.20.3c
4.30.4e R1
0
2
4
6
8
10
12
8.50.4a
8.30.4a
7.40.5b
6.30.3c
3.10.6fgR2
8.60.3a
8.40.4a
8.50.3a
7.90.5ab
8.40.3a
8.20.4a
7.80.5ab R1
8.30.4a
7.80.5ab
8.20.3a
7.50.2b
3.60.4 f R1
7.90.4ab
8.30.5a
8.40.3a
7.80.4ab
5.60.4d R2
8.40.4a
8.30.3a
7.90.5ab
8.10.4a
8.40.3a
7.30.4b
3.4.0.5fg R1
8.20.3a
8.40.4a
7.80.3ab
8.20.4a
3.30.4fg R1
7.90.4ab
8.40.3a
7.80.5ab
8.10.4a
8.30.4a
7.60.5b
7.10.5bc R1
8.30.4a
7.90.5ab
8.20.3a
7.80.4ab
7.40.4b R1
8.40.4a
8.10.3a
7.80.3ab
6.30.4c
2.90.4g R2
Table 8. Mean of sensory scores after cooking of cold stored (4 1 C) spent hen meat as
affected by papain treatments and gamma irradiation.
Storage
(Days)
3.40.3ef
3.50.4ef
3.80.3de
3.70.4de
R2
4.30.4d
5.70.3c
7.10.4b
7.80.5ab
8.50.4a
8.20.5a
R1
0
2
4
6
8
10
12
3.10.4e
3.40.5e
3.60.2de
3.50.3e
R2
4.40.3d
6.30.4c
7.80.4ab
7.90.3ab
7.80.4ab
8.30.4a
R1
0
2
4
6
8
10
12
3.70.3e
4.10.5de
3.90.4e
4.50.3d
R2
4.20.4de
5.90.4c
7.80.3ab
8.00.4ab
8.3.3a
8.40.4a
R1
4.60.3d
7.20.3b
8.10.4ab
8.40.4a
R1
3.10.4f
3.60.3de
3.50.4ef
3.40.3ef
R2
4.10.5d
6.30.4c
7.60.3ab
7.50.4b
8.00.3ab
8.40.4a
R1
4.50.4d
7.40.5b
8.10.4ab
8.30.4a
R1
3.60.5de
5.7.04c
6.60.5bc
7.10.4b
7.90.5ab
8.30.3a
R1
4.70.5d
7.10.4b
7.80.4ab
8.30.3a
R1
4.40.5d
6.80.3bc
7.90.4ab
8.10.3ab
8.00.4ab
8.40.3a
R1
4.60.4d
7.80.4ab
8.30.4a
8.40.3a
R1
3.40.4e
3.20.3f
3.70.5de
3.60.4de
R2
3.50.4e
3.80.3e
4.10.3de
3.90.4e
R2
R1 and R2: Rejected based on the appearance and odor of the raw meat, respectively.
Means with different superscript within each determination are differ significantly (P<0.05).
458
CONCLUSSION
From these results, it could be concluded that spent hen meat can be
successfully treated with papain solutions at concentrations of 10mg/ml or
100mg/ml followed by irradiation at dose of 3 kGy to produce a highly
acceptable tender and microbiologically safe meat with a possible refrigerated
market life of 10 and 6 days, respectively, based on the papain concentration.
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1 2 (2008) 462 443
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