Elevated Carbon Dioxide Atmospheres for Packaging Poultry.
II. Effects of Chicken Quarters and Bulk Packages
J. H. HOTCHKISS,1 R. C. BAKER, 5 ' 3 and R. A. QURESHI 3
Institute of Food Science, Cornell University, Ithaca, New York 14853
(Received for publication November 21, 1983)
1985 Poultry Science64:333-340
INTRODUCTION
High quality ice-packed chicken carcasses
have a shelf-life of a p p r o x i m a t e l y 9 t o 12 days
(Labuza, 1 9 8 2 ) . In addition to a relatively short
shelf-life, ice-packing has o t h e r disadvantages
such as high n o n p r o d u c t shipping weight, need
for special corrugated shippers, and sanitation
problems from c o n t a m i n a t e d melting ice. Modified a t m o s p h e r e packaging (MAP) in consumersized containers w o u l d alleviate these problems
as well as creating o t h e r advantages such as centralized packaging, increased n a m e b r a n d marketing, and longer and cheaper distribution.
O t h e r workers have investigated t h e use of
artificial atmospheres as a m e a n s of extending
t h e shelf-life of fresh p o u l t r y , m o s t often
1
Department of Food Science.
'Author to whom correspondence should be
addressed.
3
Department of Poultry and Avian Science.
333
t h r o u g h t h e use of elevated C 0 2 c o n c e n t r a tions. Wabeck et al. ( 1 9 6 8 ) c o n t i n u o u s l y
flushed vessels containing whole chicken carcasses held at 1 C with 0, 10, and 20% C 0 2
(balance air). T h e higher C 0 2 level reduced
t o t a l c o l o n y forming units b y a factor of 1 0 3
over t h e air samples w h e n held 16 days. T h e y
n o t e d t h a t C 0 2 - h e l d carcasses developed offo d o r s 6 days before air controls. G a r d n e r et al.
( 1 9 7 7 ) c o m p a r e d t h e microbiological a n d sensory quality of whole carcasses p a c k e d in ice t o
t h o s e packaged in air and elevated C 0 2 levels of
50 and 8 0 % . Ice-packed chicken spoiled in 14
days b u t b o t h C 0 2 levels were acceptable a t 23
days. " M i n o r " differences were seen in t h e sensory analysis of t h e C 0 2 packaged chicken after
12 days of storage. Sander and Soo ( 1 9 7 8 )
vacuum packaged and C 0 2 packaged g r o u p s of
whole carcasses in barrier bags and c o m p a r e d
these t r e a t m e n t s t o traditional ice-packing.
A l t h o u g h ice-packing and vacuum packaging
gave shelf-lives of 10 and 15 days, respectively,
C 0 2 - e n r i c h e d atmospheres (50 t o 70%) were
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ABSTRACT
Chicken quarters (breast and leg) one day after slaughter were packaged in glass jars
containing 0, 60, 70, and 80% carbon dioxide (C0 2 ) (balance air) or in permeable film-wrapped
trays, which were stored in large low permeability film bags and flushed with 80% C0 2 (balance
air). Storage temperature and times were 2 C and 7 to 35 days. Microbial analyses indicated a
reduction in aerobic colony forming units in film packaged quarters of between 10 4 and 10' at 14
and 35 days of storage, respectively, when C0 2 was added to the package. Other storage times and
treatments generally fell within this range. Shifts in predominant types of bacteria from Gramnegative to Gram-positive occurred in all C0 2 treatments while air-packaged samples remained predominantly Gram-negative. A residual C0 2 effect was seen when quarters that had been stored in
glass jars in 80% C0 2 were removed and stored in air for 3 days prior to analysis. This effect was
not apparent when storage was in 60% C0 2 ; 70% demonstrated an effect in between these two.
Microbial growth rates for quarters stored in film with 80% C0 2 demonstrated growth rates similar
to air packaged controls when removed from the C0 2 atmosphere. Sensory analyses of raw quarters
resulted in higher scores for C0 2 -stored samples with respect to odor, feel, and overall acceptability, and slightly lower scores for color. Sensory analyses of baked chicken showed that when
C0 2 -stored chicken was compared with fresh chicken, the two samples were rated nearly equal in
appearance, tenderness, flavor, and overall acceptability after 28 days of storage. At 35 days storage, C0 2 treated samples were scored lower in tenderness, juiciness, flavor, and overall acceptability, but were still acceptable. We conclude that elevated C0 2 atmospheres can increase shelflife of fresh chicken carcasses to at least 35 days.
(Key words: shelf-life, carbon dioxide, modified atmosphere packaging, chicken storage)
334
HOTCHKISS ET AL.
MATERIALS AND METHODS
Packaging in Glass-Jars. Breast and leg quarters (64 of each) were obtained one day postslaughter from a local distributor, placed in
sterile glass jars (Ball mason, quart) and sealed
with lids containing rubber septa. Hot wax was
applied to ensure sealing. Jars were randomized
into four sets of 32 jars each (16 breast and 16
leg quarters) and each set flushed (10 volumes)
with 0, 60, 70, or 80% C 0 2 (w/w, balance air)
through the septa. Jars were immediately stored
(2 C) and 8 jars removed every 7 days for 28
days. Four jars were analyzed immediately and
the other 4 jars were opened and allowed to
stand in air (2 C) for an additional 3 days prior
to analysis. Zero time analyses were conducted
at the time of packaging.
Packaging in Films (Bulk-Pack). Leg and
breast quarters (1 each) were placed on 10 X 15
cm (4 X 6") expanded polystyrene trays and
each tray overwrapped with plasticized polyvinylchloride (PVC) low barrier film. Sets of 4
trays were placed in larger barrier bags (56 X 32
cm, Cryovac) that had been fitted with rubber
septa at each end and heat sealed. Each barrier
bag (36 total, equaling 144 trays) was flushed
with 0 or 80% C 0 2 (w/w, balance air) and
stored at 2 C. One bag from each group was
opened every 7th day for 3 5 days. One tray was
analyzed immediately; one tray stored in air (2
C) for an additional 3 days, then analyzed; and
two trays analyzed by the sensory panels.
Microbial Analyses. Tray-packed quarters
were each placed in a sterile quart jar of the
type used to package in glass (described previously). Sterile peptone water (.1% 100 ml)
was added to each jar, which was shaken 30
times. Ten-milliliter aliquots were used to make
serial dilutions. Each dilution (1.0 ml) was used
to make quadruplicate pour plates of plate
count agar (Difco) and incubated at 22 and 37
C. Each dilution (.1 ml) was also spread on
duplicate plates of SFP agar base (containing
polymixin B sulfate and Kanamycin sulfate),
Staphylococcus 110 agar, APT, and pseudomonas isolation agar (Difco). Colony forming
units were counted after the plates had been
incubated at 22 and 37 C for 3 and 2 days,
respectively. Pure cultures were identified in
API strips. Colony forming units are reported
per milliliter of peptone. All microbial identification procedures were the same as we previously reported (Baker et al, 1985).
Physical Analysis. Color, surface pH, and
gas composition methods have been detailed
previously (Baker et al, 1985). Color values
(L, a, b) were converted to yellowness values
using the formula supplied by the instrument
manufacturer.
Sensory Analyses. A panel (n=8) evaluated
both raw and baked (internal temperature of
83 C, determined by thermocouple) chicken
from all treatments twice. Raw quarters were
judged under fluorescent lighting for odor, skin,
interior and joint color, and overall acceptability. Possible scores ranged from 1 (poor)
through 9 (excellent). Baked quarters were
evaluated after skin removal and cutting into
smaller pieces. Individual panelists received the
same muscles, each in a coded cup along with
unsalted crackers, water, and celery. Samples
were judged (1 = poor, 9 = excellent) for appear-
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reported to extend this to 22 to 27 days.
Sensory and color data were not reported,
however.
In two similar papers, Bailey et al. (1979a,b)
reported the effects of elevated CO2 concentrations on whole broilers packaged in flexible
bulk shipping bags. After evacuating the bag, 20
or 65% C 0 2 in air was added back. The 65%
C 0 2 exhibited only one day longer shelf-life
than those held in 20% C 0 2 . They concluded
that CO2 in bulk packages only slightly increased shelf-life over ice-packing from 14 to 18
days. They did not, however, analyze C 0 2
levels during the experiment, so the possibility
exists that actual C 0 2 levels were lower than reported due to loss across the barrier.
In previous work (Baker et al, 1985), we investigated the ability of a wide range of CO2
concentrations to extend the microbial quality
of ground chicken tissue packaged in glass jars.
That work indicated that a shelf-life of greater
than 4 weeks could be achieved with atmospheres containing 80% C 0 2 . That work also
indicated a direct relationship between CO2
level and number of days to spoilage; higher
C 0 2 concentrations produced longer shelf-life.
In the present work, our goal was to apply our
earlier work, first, to chicken breast and leg
quarters packaged in glass jars to eliminate effects due to package permeability, and second,
to a more practical bulk pack situation. In this
latter package, chicken quarters were packaged
into consumer-sized retail packages followed by
packaging several of these smaller packages into
a gas-flushed bulk package.
CARBON DIOXIDE PACKAGING OF CHICKEN QUARTERS
ance, tenderness, juiciness, flavor, and overall
acceptability. Fresh quarters served as controls.
Analysis of variance and least significant difference test were used to determine significance
(Snedecor and Cochran, 1967).
RESULTS AND DISCUSSION
DAYS
FIG. 1. The effect of carbon dioxide (C02) (A) and
0% C02 (A) on the counts of colony forming units
isolated from chicken quarters stored in glass jars at
2 C for 7 to 28 days. Broken lines represent counts
after an additional 3 days storage in ambient air (2 C).
(22 C) was 2.5 X 10 3 cfu/ml. In lower C 0 2
concentrations the differences were somewhat
smaller, 1.6 X 10 2 cfu with 60% C 0 2 , for
example.
When high barrier bags, which contained
chicken quarters packaged in low barrier film,
were flushed with 80% C 0 2 , a large reduction
in colony forming units was seen. As can be
seen in Figure 4, the difference between airflushed controls and 80% C0 2 -flushed bulk
packs was greatest at 14 days, being more than
10 4 cfu. The air control carcasses leveled off
below 10 9 cfu while the 80% flushed
package increased only to 6.3 x 10 7 cfu after
35 days.
Other workers have documented the ability
of elevated C 0 2 to reduce total aerobic counts
but not always to as great of degree. Wabeck et
al. (1968) demonstrated a 1.8 X 10 3 total cfu
reduction when whole chicken carcasses were
exposed to a continuous exchange of 20% C 0 2
(balance air). Bailey et al. (1979b) found a
reduction in total aerobic counts of only 4.0 X
l o ' / c m 2 swabbed in whole chickens stored 18
days under 65% C 0 2 when compared to icepack controls. They concluded that C 0 2 gave
a 5-day increase in shelf-life. Their carcasses
DAYS
FIG. 2. The effect of 70% carbon dioxide (C02) (A)
and 0% C02 (A) on the counts of colony forming units
isolated from chicken quarters stored in glass jars at
2 C for 7 to 28 days. Broken lines represent counts
after an additional 3 days storage in ambient air (2 C).
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The log of the counts of colony forming
units (22 C) vs. days storage are given in Figures
1, 2, and 3 for chicken quarters packaged in
glass with 60, 70, and 80% C 0 2 , respectively.
Leg and breast quarters were also packaged in
glass jars with ambient air as controls and are
also plotted. Broken lines represent samples
that were opened to ambient atmosphere for 3
days prior to analysis. Each data point is the
average of two trials; breast and leg quarter
counts were averaged for each trial as differences in colony forming units were slight.
In all cases, elevated C 0 2 atmospheres resulted in considerably lower aerobic counts
when plates were incubated at both 22 C (Figs.
1, 2, and 3) and 37 C (not shown). The largest
difference in colony forming units was seen
when air controls and 80% CO2 were compared
at 28 days of storage (Fig. 3). This difference
335
336
HOTCHKISS ET AL.
to a lingering inhibition. Other workers have
disputed this residual effect (Finne, 1982).
Enfors et al. (1979) found that upon removing
pork from 100% CO2 atmospheres, total aerobic counts increased at a similar rate to pork
that had been packaged in air only. Use of a
bulk pack system would require that carcasses
have at least a 3 to 4-day shelf-life after removal
from the elevated C 0 2 atmosphere. We tested
both glass-packaged and film-packaged quarters
after removal from the CCVcontaining atmosphere and subsequent storage (2 C) in ambient
air. Similarly to Enfors et al. (1979), we found
that when chicken quarters that had been
packaged in 60% CO2 and the jars subsequently
opened for 3 days, the growth rates of total
aerobic organisms were very similar to the
earlier growth rates of the air packaged controls. As can be seen by observing the slopes of
broken lines in Figure 1, which represent the
air storage period, the growth of CCvpackaged
samples becomes similar to the air growth rate
between 7 and 14 days storage. Figure 1 also
shows that as the CO2 levels build up in the airpackaged controls (see subsequent paragraphs)
some microbial inhibition occurs. When 14-day
controls were opened and stored 3 more days,
0
DAYS
FIG. 3. The effect of 80% carbon dioxide (C02) (A)
and 0% CO, (*) on the counts of colony forming units
isolated from chicken quarters stored in glass jars at
2 C for 7 to 28 days. Broken lines represent counts
after an additional 3 days storage in ambient air (2 C).
7
14
21
28
35
DAYS
FIG. 4. The effect of 80% carbon dioxide (C02) (A)
and 0% C02 (•) on the counts of colony forming units
isolated from chicken quarters stored (2 C) in a bulk
pack for 7 to 35 days. Broken lines represent an additional 3 days storage in ambient air (2 C).
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were packaged in flexible films and CO2 levels
in the containers not determined directly.
The work of Sander and Soo (1978) is similar to the results of the present study. They
found a 2.0 x 10 3 reduction in total aerobic
colony forming units when vacuum packaged
whole carcasses were back flushed with C 0 2
and stored for 18 days at 1.1 C. Results were
similar for anaerobic organisms. Sander and Soo
(1978) concluded that CO2 flushing produced a
shelf-life of 22 to 27 days compared with 10
days for conventional ice-packing.
All test and control samples in our work
were held at 2 C, which is slightly higher than
might be optimum. Microbial colony forming
units would likely have been somewhat lower
in controls and test samples if held at a lower
temperature; however, we chose this higher
temperature in order to represent more severe
conditions of storage and shipment.
Some authors have reported that for products other than chicken, there may be a residual
effect due to elevated CO2 atmospheres (Christopher et al., 1980). That is, after products
have been removed from the CO2 atmosphere
and stored under ambient atmosphere, microbial counts are less than might be expected due
CARBON DIOXIDE PACKAGING OF CHICKEN QUARTERS
(Baker et al, 1985), elevated CO2 levels gave
not only quantitative differences in total counts
but also qualitative changes in microbial populations from quarters packaged in jars (not
shown) and flexible bulk packages (Table 1).
Gram-negative organisms were inhibited in
favor of Gram-positive organisms in the bulk
pack system as would be expected if the C 0 2
permeated the inner barrier. Lactobacillus accounted for 99% of the aerobes on quarters
held under 80% C 0 2 for 3 5 days while Pseudomonas accounted for 89% of the aerobes in the
35 day air controls. Clostridium, which was
detected in our ground chicken muscle study
(Baker et al., 1985), was not found in any
sample. We speculate that the C 0 2 level was less
than 80% inside the inner package because of
the packaging technique used and the O2
tension high enough to preclude Clostridiumtype organisms.
Surface pH values for glass and film packaged fresh chicken quarters averaged 6.01 and
6.12, respectively. The pH of a majority of
samples decreased by less than .9 pH units
during the storage tests. There was no clear
effect due to elevated C 0 2 levels or packaging
method.
When L, a, b values obtained from objective
color measurements were converted to yellowness values, the general trend was a decrease
yellowness during storage. To demonstrate this
TABLE 1. Distribution of microorganisms isolated from chicken parts packaged in bulk packs
Organisms
Storage
Carbon
dioxide
Staphylococcus
Pseudomonas
29
71
(days)
Lactobacillus
(,\i)
0
7
80
0
20
10
60
90
10
14
80
0
16
8
44
92
40
21
80
0
10
4
16
96
74
28
80
0
2
3
10
97
88
35
80
0
1
89
99
11
Clostridium
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the growth rates continued at the same rate as
had occurred during days 7 to 14 of storage.
Those controls that remained packaged had
lower growth rates (i.e., 14 to 28 days, solid
line).
The 70% C 0 2 quarters (Fig. 2) showed similar trends except that the slopes of the broken
lines were less than the air controls. This decrease in growth rate was even more dramatic
in the 80% CO2 quarters. In this test, samples
exposed to ambient air for 3 days after storage
in elevated CO2, showed growth rates (as evidenced by the slope of the broken lines in Fig.
3) very similar to samples that remained in the
elevated CO2 atmosphere. This effect is likely
due to a residual microbial inhibition when
higher (80%) CO2 levels are used. Lower CO2
concentrations (60%) did not demonstrate the
inhibition, and the 70% samples fell somewhere
in between these extremes.
Our bulk pack quarters were similarly removed from the bulk pack and left in ambient
air, wrapped in low barrier film to simulate
retail display (Fig. 4). All samples, with the
exception of the 14-day sample, gave growth
rates only slightly less than the air control packages. It is likely that due to the C 0 2 permeability of the bulk bag film, C 0 2 concentration
inside the inner package was less than 80% and,
hence, a residual effect was not apparent.
As we expected based on our previous work
3 37
338
HOTCHKISS ET AL.
-20-
0
7
14
21
28
35
42
DAYS
FIG. 5. Changes in yellowness as measured by a
Hunter Color Difference meter for highly pigmented
(•) and less pigmented (o) chicken stored under 80%
C02 (2 C) for 35 days. The 42-day value represents a
measurement after 7 additional days of storage in
ambient air (2 C).
appearance of raw quarters packaged in the
bulk pack (Table 2). Up to 21 days storage,
C0 2 -packaged quarters scored as well in color
desirability as the air control. At 35 days C 0 2 packaged samples were consistently lower in
color desirability. However, the CO2 -packaged
samples were consistently higher in desirability
when evaluated for odor, feel, and overall
acceptability. Throughout storage, the C 0 2
packaged samples remained saleable, while the
air-packaged controls by Day 14 had become
unacceptable. Undesirable odors in the quarters
packaged in air were easily detected by panelists at Day 14.
Bulk-packaged chicken quarters, which had
been treated with C 0 2 , were baked to an internal temperature of 83 C and tested for sensory
attributes by the panel throughout the experiment. Fresh quarters were acquired weekly and
tested simultaneously with the C 0 2 packaged
quarters. Results (Table 3) indicated that up to
21 days storage, the C0 2 -packaged chicken
scored nearly as well as fresh chicken in most
attributes. At 28 and 35 days, the C0 2 -treated
quarters scored somewhat lower in all attributes
than fresh chicken but still remained within an
acceptable range. For example, after 35 days
storage, test chicken scored 5.4 in overall acceptability while a fresh chicken scored 7.1.
This difference of 1.7 seems quite small when
one considers that the C0 2 -packaged carcass
was 35 days older than the fresh carcass and
held at 2 C throughout the test period.
The C 0 2 concentrations in the gas surrounding chicken quarters packaged in glass jars
changed throughout the experiment in a manner similar to earlier findings with ground
chicken (Baker et al, 1985). The samples packaged with no added C 0 2 slowly increased in
C 0 2 until levels of 14 to 21% were found at 28
days. Those jars to which C 0 2 had been added
decreased in concentration to values of 40 to
60% after 35 days, presumably due to absorption by the tissue. The chicken packaged in
bulk bags and 80% C 0 2 decreased to 45% C 0 2
within 7 days and remained close to this level
throughout the test. This rapid decrease was
likely due to a combination of mixing with air
inside the smaller packages and absorption by
the chicken flesh.
Elevated C 0 2 atmospheres produce both
quantitative and qualitative differences in the
microorganisms that proliferate on packaged
chicken. With C 0 2 , Gram-positive organisms of
the Lactobacillus sp. comprise the majority of
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loss of color, we packaged 4 chicken breast and
4 chicken leg quarters in glass jars and bulk
packs with 80% C 0 2 . Six of the samples had
highly pigmented skin (yellow) while 2 of the
samples had much lower skin pigment content.
These quarters were removed from the package
weekly and the color of each measured and
then repackaged in the same container and CO2
concentration. Samples were exposed to air
after 35 days for an additional 7 days and reevaluated. Highly pigmented quarters decreased
in yellowness values from an average of 24 units
to 4 units after 35 days while low pigmented
quarters decreased from an initial value of 3 to
—16 after 35 days storage (Fig. 5). When the
skin was returned to ambient air after 35 days,
the yellowness increased slightly. The brackets
in Figure 5 represent ± one standard deviation
and indicate that the sample to sample variation
in skin color is greater than the overall color
change.
Changes in the color of skin, internal flesh,
and joints due to elevated C 0 2 were also
noticed when the sensory panel rated the
CARBON DIOXIDE PACKAGING OF CHICKEN QUARTERS
339
TABLE 2. Sensory panel scores for raw chicken quarters packaged in bulk packs
Days storage (80% C0 2 )'
Atmosphere
()
7
14
21
28
35
Odor
Air
8.2
7.6
7.8
3.5*
7.1*
3.4*
6.8*
2.9*
6.1*
1.8*
5.0*
83
7.3
7.1
4.6*
7.8*
4.9*
6.5*
2.6*
6.0*
4.9*
3.9*
85
7.6
7.6
4.5*
6.9*
5.4
5.1
4.3
4.0
5.0*
3.3*
82
7.6
7.6
4.9
6.6
5.3
4.9
4.9
4.1
5.2*
3.8*
co2
Air
Color (skin)
co2
Air
Color (internal)
co2
Air
Color (joints)
co2
Feel
Air
C0 2
83
7.8
7.8
3.9*
6.4*
3.8
4.7
2.6*
5.0*
2.0*
4.8*
Overall acceptability
Air
82
7.6
7.6
2.6*
7.1*
2.6*
6.2*
2.5*
4.9*
3.0*
4.6*
co2
*Means (n=8) in the same column within a parameter having an asterisk are significantly different (P<.05).
All others are not significant.
1
CO, = Carbon dioxide.
TABLE 3. Sensory panel scores for baked chicken packaged in bulk packs
Days storage (80% C0 2 )'
Parameters
7
14
21
28
35
Appearance
Stored
Fresh
7.8
7.7
7.1
7.8
7.5
7.5
7.1
7.2
6.7*
7.6*
Tenderness
Stored
Fresh
7.0
6.5
6.0*
7.1*
5.5*
7.2*
6.8*
5.7*
5.2*
7.0*
Juiciness
Stored
Fresh
6.4
5.5
5.6
6.4
4.9*
6.7*
5.4*
6.4*
5.6
6.6
Flavor
Stored
Fresh
7.5
7.1
6.7
6.7
6.1
7.2
6.4
7.2
5.6*
7.3*
Overall acceptability
Stored
Fresh
7.4
6.9
6.2
6.9
6.0
7.1
6.0
6.8
5.4*
7.1*
•Means (n=8) in the same column within a parameter having an asterisk are significantly different (P<.05).
All others are not significant.
' CO, = Carbon dioxide.
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Parameter
340
HOTCHKISS ET AL.
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bacteria present while Gram-negative Pseudomonas predominate on chicken held in air. We
think that these microbial changes are not
likely due to a pH shift on the surface of the
chicken but rather due to a biochemical inhibition of bacterial metabolism by one or more
forms of dissolved CO2.
The keeping quality of refrigerated chicken
quarters can be enhanced by the addition of
60 to 80% C 0 2 to the atmosphere surrounding
the tissue and the shelf-life extended to at least
35 days at 2 C and perhaps longer. This technique can also be applied to a bulk packaging
system utilizing low and high barrier films.