The effects of modified atmosphere gas composition on microbiological criteria, color and oxidation values of minced beef meat


Esmer, O.K.; Irkin, R.; Degirmencioglu, N.; Degirmencioglu, A.

Meat Science 88(2): 221-226

2011


This paper reports the effects of modified atmosphere gas compositions with different concentrations of CO(2)/O(2)/N(2) on color properties (L*, a* and b* values), oxidation stability (TBARS value) and microbiological properties of minced beef meat stored at +4 °C. Sampling was carried out on the 1st, 3rd, 5th, 7th, 9th, 11th and 14th day of storage. The gas mixtures used were as follows: (i) %30O(2) + %70CO(2) (MAP1), (ii) %50O(2) + %50CO(2) (MAP2), (iii) %70O(2) + %30CO(2) (MAP3), (iv) %50O(2) + %30CO(2) + %20N(2) (MAP4), and (v) %30O(2) + %30CO(2) + %40N(2) (MAP5). Control samples (AP) were packaged under atmospheric air. Pseudomonas, lactic acid bacteria, Brochothrix thermosphacta, and Enterobacteriaceae members were monitored. Among these five modified atmosphere gas compositions, the best preservation for minced beef meat was in MAP4 gas combination maintaining acceptable color together with oxidation stability and acceptable microbial loads until the end of storage period of fourteen days.

Contents
lists
available
at
ScienceDirect
Meat
Science
journal
homepage:
www.elsevier.com/locate/meatsci
S
.
SCIE
.
SCIEN
k.
The
effects
of
modified
atmosphere
gas
composition
on
microbiological
criteria,
color
and
oxidation
values
of
minced
beef
meat
Ozlem
Kizilirmak
Esmer
a
'
*
,
Reyhan
Irkin
b
,
Nurcan
Degirmencioglu
C
,
Ali
Degirmencioglu
b
Ege
University
Food
Engineering
Department,
35100
Bornova,
Izmir,
Turkey
b
Balikesir
University
Susurluk
Vocational
School,
Susurluk,
TR10600,
Balikesir,
Turkey
Balikesir
University
Bandirma
Vocational
School,
Bandirma,
TR10600,
Balikesir,
Turkey
ARTICLE INFO
ABSTRACT
Meat
Science
88
(2011)
221-226
Article
history:
Received
4
May
2009
Received
in
revised
form
31
May
2010
Accepted
14
December
2010
Keywords:
Minced
beef
meat
Modified
atmosphere
packaging
Color
Oxidation
stability
Microbiological
properties
This
paper
reports
the
effects
of
modified
atmosphere
gas
compositions
with
different
concentrations
of
CO
2
/0
2
/N
2
on
color
properties
(L*,
a*
and
b*
values),
oxidation
stability
(TBARS
value)
and
microbiological
properties
of
minced
beef
meat
stored
at
+4
°C
Sampling
was
caned
out
on
the
1st,
3rd,
5th,
7th,
9th,
11th
and
14th
day
of
storage.
The
gas
mixtures
used
were
as
follows:
(i)
%300
2
+%700O
2
(MAP1),
(ii)
%500
2
+%500O
2
(MAP2),
%700
2
+
%300O
2
(MAP3
),
(
iv)
%500
2
+
%300O
2
+
%20
N2
(MAP4),
and
(v)%300
2
+%300O
2
+%40N
2
(MAP5).
Control
samples
(AP)
were
packaged
under
atmospheric
air.
Pseudomonas,
lactic
acid
bacteria,
Brochothrix
thermosphacta,
and
Enterobacteriaceae
members
were
monitored.
Among
these
five
modified
atmosphere
gas
compositions,
the
best
preservation
for
minced
beef
meat
was
in
MAP4
gas
combination
maintaining
acceptable
color
together
with
oxidation
stability
and
acceptable
microbial
loads
until
the
end
of
storage
period
of
fourteen
days.
©
2010
Elsevier
Ltd.
All
rights
reserved.
I.
Introduction
The
modified
atmosphere
packaging
is
a
technique,
which
is
widely
used
to
extend
the
shelf-life
and
to
improve
the
quality
of
perishable
foods
including
meat
and
meat
products
stored
at
refrigeration
temperatures
or
below.
Color,
lipid
oxidation,
and
microbial
criteria
are
the
most
important
quality
criteria
for
storage
of
fresh
red
meat.
Therefore,
the
modified
atmosphere
packaging
must
stabilize
both
the
color
and
oxidation,
as
well
as
retard
the
microbial
growth.
It
is
included
that
20-30%
CO
2
+
70-80%
0
2
in
conventional
gas
composition
of
modified
atmosphere
packaging
of
fresh
red
meat.
Oxygen
is
required
for
myoglobin—the
principle
protein
responsible
for
the
meat
color
(Mancini
&
Hunt,
2005)
to
keep
it
in
oxygenated
form,
which
gives
the
bright
cherry
red
color
to
meat.
However,
the
presence
of
oxygen
also
increases
the
rate
of
lipid
oxidation,
which
causes
undesirable
changes
in
color
and
flavor
(Love
&
Pearson,
1971).
While
the
use
of
high
oxygen
concentration
is
known
to
prolong
the
color
stability
by
promoting
the
formation
of
oxymyoglobin,
it
is
also
expected
to
increase
the
rate
of
lipid
oxidation
(Zhao,
Wells,
&
McMillin,
1994;
Cayuela
&
Gil,
2004;
O'Grady,
Monahan,
Burke,
&
Allen,
2000).
Lipid
oxidation
is
particularly
pro-
noummd
in
ground
meats,
where
the
disruption
of
muscle
cell
structure
exposes
label
lipid
components
to
oxygen
(Sato
&
Hegarty,
1971).
*
Corresponding
author.
Tel.:
+90
232
3113020;
fax:
+90
232
3427592.
E-mail
address:
ozlem.kizilirmak@ege.edu.tr
(0.
Kizilirmak
Esmer).
0309-1740/$
-
see
front
matter
C
2010
Elsevier
Ltd.
All
rights
reserved.
doi:10.1016/j.meatsci.2010.12.021
The
gas
atmosphere
also
creates
a
selective
pressure
on
the
microflora
of
meats.
Aerobic
chilled
storage
favors
the
growth
of
gram-negative,
aerobic
rod-shaped
bacteria
including
Pseudomonas.
Many
other
bacteria
are
present
but
Pseudomonas
spp.
predominate
and
produce
off-odors
from
protein
break-down
and
amino-acid
metabolism.
Under
anaerobic
conditions
of
chilled
storage
with
elevated
levels
of
carbon
dioxide,
while
the
slower
growing
lactic
acid
bacteria
are
encouraged,
the
growth
of
aerobic
spoilage
microflora
is
discouraged.
In
the
presence
of
oxygen,
growth
of
Brochothrix
thermosphacta
occurs
and
can
cause
spoilage
of
meats.
In
this
research,
it
was
aimed
to
determine
the
effects
of
five
different
modified
atmosphere
packaging
gas
compositions
with
different
concentrations
of
0
2
/CO
2
/N
2
on
the
color
properties,
oxidation
stability
and
microbiological
properties
of
minced
beef
meat.
To
date,
numerous
researches
have
been
carried
out
in
regards
to
the
modified
atmosphere
packaging
of
fresh
meat.
Most
of
these
studies
involved
samples
as
a
whole
muscle
or
in
the
form
of
steak
(Kennedy,
Buckley,
&
Kerry,
2004;
Jakobsen
&
Bertelsen,
2000;
Zakrys,
Hogan,
O'Sullivan,
Allen,
&
Kerry,
2008),
not
minced
meat.
However,
minced
meat
is
more
sensitive
to
oxidation
because
of
its
porous
structure
and
it
has
more
susceptibility
to
microbial
spoilage
due
to
the
grounding
process.
For
this
reason,
in
this
research
color,
oxidation
stability
and
microbiological
properties
were
evaluated
extensively
for
modified
atmosphere
packaging
application
of
minced
beef
meat
in
order
to
determine
the
effects
of
different
gas
compositions
on
properties
of
minced
beef
meat.
0.K
Esmer
et
al.
/
Meat
Science
88
(2011)
221-226
222
2.
Materials
and
methods
2.1.
Meat
samples
Meat
from
pectoralis
major
and
minor
muscles
of
beef
carcasses
from
2-year-old
cattle,
after
48
h
from
postmortem
were
purchased
from
a
local
establishment
in
Bandirma,
Turkey.
The
meat
was
trimmed,
of
all
exterior
fat
and
connective
tissue,
and
minced
in
a
sterilized
meat
mincer
in
3
mm
size.
The
samples
were
transported
to
the
laboratory
under
refrigeration
conditions.
The
fat
content
of
the
minced
meat
samples
was
22%.
2.2.
Packaging
parameters
The
minced
meat
samples
were
placed
in
"Poly
Ethylene
Terephtalate
(PET)/Ethylene
Vinyl
alcohol
(EVOH)/Low
Density
Polyethylene
(LDPE)"
trays
in
750
pm
thickness
and
sealed
with
a
laminated
film
of
"Oriented
Poly
Propylene
(OPP)/Low
Density
Poly
Ethylene
(LDPE)/Ethylene
Vinyl
alcohol
(EVOH)/Low
Density
Poly-
ethylene
(LDPE)"
in
77
pm
thickness,
with
an
oxygen
transmission
rate
of
3.5
cm
3
/m
2
/
2
4
h
(23
C,
0%
RH).
Modified-atmosphere
packag-
ing
was
carried
out
using
Multivac
R-230
(Multivac,
Germany)
packaging
machine.
3/1
(vol/wt)
ratio
of
headspace
to
meat
was
used
in
modified
atmosphere
packaging.
Table
1
illustrates
the
modified
atmosphere
gas
combinations
used
to
package
the
meat
samples.
Control
samples
(Air
packaged—AP)
was
also
packaged
with
ambient
air
without
giving
any
gas
composition.
The
samples
were
stored
in
the
dark
under
refrigeration
conditions
(
+
4
°C)
for
14
days.
Analyses
were
carried
out
on
the
1st,
3rd,
5th,
7th,
9th,11th
and
14th
day
of
storage.
The
whole
experiment
was
replicated
twice.
2.3.
Methods
Gas
composition
The
gas
composition
of
headspace
in
package
was
measured
using
a
digital
PBI
Dansensor
Check
Pointer
0
2
/CO
2
(Ringsted,
Denmark)
analyzer
and
expressed
as
%0
2
and
%CO
2
.
The
remaining
gas
was
N2.
Color
Color
analysis
was
carried
out
using
a
Hunter
Lab
CFIX-45-2
(Reston,
Virginia,
USA)
by
assessing
L*,
a*
and
b*
values.
The
instrument
was
calibrated
with
black
and
white
standard
plates
before
the
analysis.
The
reported
data
are
the
mean
of
four
determinations.
Lipid
oxidation
The
extent
of
lipid
oxidation
was
determined
through
thiobarbituric
acid
reactive
substances
(TBARS)
in
mg
malonaldehyde/kg
of
meat
as
described
by
Tarladgis,
Watts,
Younathan,
and
Dugan
(1960).
Microbiological
analysis
25
g
of
each
sample
was
diluted
in
225
ml
sterile
0.1
g/100
ml
peptone
water
and
homogenized
in
a
stomacher
for
90
s
at
room
temperature.
Table
1
Gas
compositions
of
MAP
samples.
02
CO
2
N2
MAP1
30
70
0
MAP2
50 50
0
MAP3
70
30
0
MAP4
50
30
20
MAPS
30 30
40
A
serial
10-fold
dilution
series
was
prepared
in
0.1
g/100
g
peptone
water.
Pseudomonas
count
was
enumerated
on
Pseudomonas
agar
supplemented
with
CFC
at
25
°C
for
48
h
(Mead
&
Adams,
1977).
Lactobacillus
were
counted
on
double-layer
pH
5.6
MRS
agar
(Oxoid)
incubated
at
30
°C
for
48
h
(Russo,
Ercolini,
Mauriello,
&
Villani,
2006).
Brochothrix
thermosphacta
was
enumerated
on
Streptomycin
Thallous
Acetate
Agar
(STAA)
at
25
°C
for
48
h
(Gardner,
1966).
Enterobacter-
iaceae
members
were
determined
on
double-layer
violet-red-bile-
dextrose
agar
(VRBG,
Oxoid)
at
37
°C
for
24
h
(Govaris
et
al.,
2007).
Microbiological
data
were
transformed
into
logarithms
of
the
number
of
colony
forming
units
(cfu/g).
Statistical
analysis
The
data
obtained
from
analyses
were
subjected
to
variance
analysis
in
order
to
determine
the
effect
of
gas
composition
of
modified
atmosphere
packaging
and
storage
time
on
each
variable.
The
analysis
was
performed
by
ANOVA
one-way
analysis,
using
SPSS
8.0.
To
identify
the
different
groups,
the
Duncan's
post
hoc
test
was
applied.
3.
Results
and
discussion
3.1.
Headspace
composition
The
gas
composition
of
each
package
changed
significantly
within
storage
period
(p<_0.05).
It
is
known
that
gaseous
environment
within
a
modified
atmosphere
pack
is
not
static.
It
may
be
the
result
of
microbial
growth,
the
permeability
of
packaging
material,
and
respiration
of
the
product
or
the
gas
absorption
by
the
food.
As
it
is
seen
from
Table
2,
0
2
concentration
decreased
and
CO2
concentration
increased
in
all
samples
starting
from
the
1st
day
of
storage,
but
this
change
was
more
evident
in
AP,
MAP1(0
2
/CO
2
/
N
2
:30/70/0)
samples
which
contain
less
0
2
concentrations
than
the
other
samples.
As
stated
by
O'Grady
et
al.
(2000),
relative
changes
in
gaseous
atmospheres
within
the
modified
atmosphere
packs
were
higher
at
a
lower
oxygen
level.
Similar
results
related
the
changes
in
the
headspace
atmospheres
were
reported
in
other
studies
(O'Grady
et
al.,
2000;
Kennedy
et
al.,
2004;
Koutsoumanis,
Stamatiou,
Drosinos,
&
Nychas,
2008;
Ercolini,
Russo,
Torrieri,
Masi,
&
Villani,
2006).
It
is
an
expected
result
for
CO
2
concentration
to
decline
due
to
the
absorption
of
CO
2
in
meat
(Jakobsen
&
Bertelsen,
2002),
but
this
decline
cannot
be
monitored
by
reason
of
microbial
growth.
During
storage,
the
majority
of
microorganisms
present
in
meat
utilize
available
oxygen
in
the
headspace
while
some
members
of
the
meat
microflora
such
as
B.
thermosphacta
and
lactic
acid
bacteria
(LAB)
produce
carbon
dioxide
as
a
metabolic
product
(Nychas,
1994).
3.2.
Color
The
evolution
of
L*,
a*
and
b*
values
is
shown
in
Table
3.
The
effect
of
gas
compositions
on
L*
value
of
minced
meat
samples
were
not
statistically
significant
(p
>0.05
),
whereas
the
L*
values
were
significantly
affected
by
the
storage
time
(p
0.01).
L*
values
showed
a
varying
trend,
irrespective
of
packaging
treatments
throughout
the
entire
storage
period.
This
result
shows
us
that
varying
concentrations
of
CO
2
or
0
2
gases
in
MAP
applications
does
not
affect
the
lightness
of
minced
beef
meat
and
this
result
is
consistent
with
the
findings
of
Soldatou,
Nerantzaki,
Kontominas,
and
Savvaidis
(2009).
Both
gas
composition
and
storage
period
had
a
significant
effect
on
the
a*
values
(redness)
of
minced
beef
samples
(p
0.01
).
In
1st
day
of
storage,
a
significant
difference
was
not
observed
among
samples
but,
after
the
1st
day
a*
values
started
to
decrease.
The
lowest
values
were
obtained
for
MAP1
(0
2
/CO
2
/N
2
:30/70/0)
and
MAP2
(0
2
/CO
2
/N
2
:50/50/0)
samples
where
a*
values
were
below
10
at
the
9th
day
of
storage
for
both
samples.
High
CO
2
concentrations
led
to
sharp
decreases
in
the
a*
value
O.K.
Esmer
et
al.
/
Meat
Science
88
(2011)
221-226
223
Table
2
Changes
in
gas
composition
valuesa
of
modified
atmosphere
packages.
Gas
comp.
Days
02
CO
2
N
2
(%)
AP
1
17.70
±
1.70`
3.95
±
0.78
a
7835
±
1.13
a
3
1635
±
1.60
bc
735
±
0.21
b
7630±
1.81
a
5
15.40
±
1.95
bc
8.10±
1.13"
76.50
±
3.08
a
7
14.50
±
137"
10.05
±
0A9
b
75.45
±
1.87
a
9
13.65
±
1.74"
1835
±
035`
68.00
±
2.09
a
11
12.30
±
1.10"
18.50±
0.42`
69.20±
1.53
a
14
7.60±139
a
2230±
0.57
d
70.10±
1.96
a
MAP1
1
31.60
±
0.14
f
6835
±
0.07
a
0.05
±
0.07
a
3
29.80
±
0.14
c
69.45
±
035
b
0.75
±
0.21a
5
28.15
±
0.21
d
7130±
0.00`
0.55
±
0.21
a
7
26.50
±
0.57
c
73.20±
0.28
d
030±
0.28
a
9
26.25
±
0.21
c
73.25
±
0.21
d
0.50
±
0.00
a
11
24.75
±
0.21
b
75.00±
0.14'
0.25
±
035
a
14
21.15
±
0.21
a
78.55
±
0.49
f
030±
0.28
a
MAP2
1
50.40
±
0.57c
48.65
±
035a
0.95
±
0.21a
3
49.20
±
0.28
abc
49.95
±
0.54b
0.85
±
036
a
5
4930
±
0.28bc
49.60±
0.14
ab
1.10±
0.42a
7
49.70
±
0.57c
49.50
±
0.00a
b
0.80±
0.57a
9
48.10
±
0.00
ab
51.50±
0.28`
0.40
±
0.28
a
11
48.15
±
o.ma"
51.40±
0.14c
0.45
±
0.07
a
14
48.00
±
0.00a
51.90±
0.14c
0.10±
0.14a
MAP3
1
72.80
±
0.28`
26.60
±
0.28a
0.60
±
0.00a
3
70.10
±
0.14"
29.45
±
0.07
b
0.45
±
0.07
a
5
6935
±
1.20
ab
30.05
±
1.13
1
'
0.60
±
0.07
a
7
69.50
±
0.28a
b
29.90
±
0.00
1
'
0.60
±
0.28a
9
68.25
±
0.07
a
3135
±
035`
0.40
±
0.42a
11
68.10
±
ale
31.55
±
0.07
c
035
±
0.07
a
14
68.10
±
0.00a
31.65
±
0.49`
0.25
±
0.49a
MAP4
1
55.60
±
0.49`
28.40
±
0.57
a
16.00±
1.06
a
3
54.25
±
035
bc
2830±
0.42
a
17.45
±
0.07
a
5
51.15
±
1.48
ab
`
28.45
±
035
a
20.40±
1.84
ab
7
51.40
±1.84a
b
c
29.65
±
035
ab
18.95
±
2.19
ab
9
45.70
±
2.2V
30.55
±
134
ab
23.75
±
0.92
b
11
46.80
±
2.40
a
31.95
±
0.49
b
21.25
±
1.91a
b
14
47.80
±
2.26
ab
31.85
±
0.07
b
2035
±
2.19
ab
MAPS
1
34.55
±
0A9
b
27.80±
0.85
a
37.65
±
035
a
3
32.10
±
0.28
ab
28.15
±
1.06
a
39.75
±
0.78
a
5
31A0±
0.14
ab
29.25
±
0.78
a
3935
±
0.64
a
7
31.65
±
0.26
ab
29.60±
0.14
a
38.75
±
2.12a
9
30.10
±
0.00
ab
30.65
±
0.07
a
39.25
±
0.07
a
11
27.80
±
2.69
a
31.15
±
0.49
a
41.05
±
3.18
a
14
28.65
±
1.77a
34.50±
1.70
b
36.85
±
3.46
a
aEach
value
is
the
mean
of
two
batch
production
with
two
samples
analyzed
per
batch
(n=4).
Means
with
different
lowercase
letters
in
the
same
column
are
significantly
different
(p<0.05).
and
rapid
discoloration
of
meat
in
high-CO
2
atmospheres
was
also
reported
by
Martinez,
Djenane,
Cilia,
Beltran,
and
Roncales
(2005)
as
an
effect
of
the
decrease
in
pH.
The
discoloration
appeared
earlier
in
MAP5
(02/CO2/N2:30/30/40)
samples
than
MAP3(0
2
/CO
2
/N
2
:70/30/0)
and
MAP4(0
2
/CO
2
/N
2
:50/30/20)
samples
and
the
a*
value
was
determined
as
14.48
±
2.75
on
the
9th
day
of
storage
and
declined
to
8.22
±
0.59
on
the
14th
day
of
storage.
There
were
no
significant
statistical
and
visual
differences
between
the
a*
values
of
MAP3
(02/CO2/N2:70/30/0)
and
MAP4(0
2
/CO
2
/N
2
:50/30/20)
samples
and
the
redness
was
kept
until
the
14th
day
of
storage
with
these
gas
compositions.
Jakobsen
and
Bertelsen
(2000)
also
expressed
the
stability
of
the
a*
value
between
55-80%
0
2
and
the
color
stability
did
not
increase
markedly
after
increasing
the
oxygen
level
from
55%
to
80%.
It
must
be
emphasized
that
high
standard
deviations
were
obtained
for
the
a*
values
especially
for
MAP5(02/CO2/N2:30/30/40)
and
AP
samples
towards
the
end
of
the
storage
period.
This
situation
depends
on
to
the
regional
differences
in
the
redness
of
samples
because
of
the
usage
of
oxygen
during
the
storage
and
oxygen
deficiency
until
the
end
of
storage
period.
The
b*
value
changed
significantly
with
the
gas
compositions
of
modified
atmosphere
packaging
and
the
storage
period
(p<0.01),
and
decreased
throughout
the
whole
storage
period.
The
correlation
between
the
a*
and
b*
value
was
found
to
be
significant
(r
2
:
0.908
and
p<0.01).
This
means
that
the
decrease
in
the
a*
value,
which
stands
for
the
loss
of
redness
in
color
of
the
meat
and
transition
of
its
color
to
brownish
red
by
formation
of
metmyoglobin,
leads
to
the
decrease
in
the
b*
value.
O'Sullivan
et
al.
(2003)
expressed
that
the
b*
value
was
more
correlated
to
brown
by
sensory
panelists.
3.3.
Oxidative
stability
Table
3
illustrates
the
TBA
values
of
samples.
It
was
found
that
the
gas
composition
was
not
statistically
significant
(p
>0.05)
for
oxidative
stability,
whereas
the
storage
time
was
significant
(p<0.05).
Oxidative
stability
decreased
for
the
whole
storage
period.
The
TBA
values
of
all
samples
were
about
2.5
except
MAP1
(02/CO2/
N
2
:30/70/0)
on
the
5th
day
of
storage
and
the
TBA
values
of
both
MAP1(0
2
/CO
2
/N
2
:30/70/0)
and
MAP2(0
2
/CO
2
/N
2
:50/50/0)
samples
were
higher
than
the
other
samples
(p<0.05)
on
the
7th
and
9th
day
of
storage.
This
result
shows
us
that
high
CO
2
concentration
also
leads
to
the
decrease
in
oxidation
stability
together
with
discoloration.
The
MAP1(0
2
/CO
2
/N
2
:30/70/0)
and
MAP2(02/CO2/N2:50/50/0)
samples
were
not
analyzed
anymore
because
of
the
very
high
TBA
values
and
discoloration.
The
TBA
values
of
MAP3
(0
2
/CO
2
/N
2
:70/30/0)
samples
were
virtually
higher
than
MAP4(0
2
/CO
2
/N
2
:50/30/20),
MAP5(02/
CO
2
/N
2
:30/30/40)
and
AP
throughout
the
whole
storage
period.
At
the
end
of
storage
period,
the
best
sample
was
the
MAP4(0
2
/CO
2
/N
2
:50/
30/20)
and
AP,
whereas
the
ordinary
gas
composition
MAP3
(02/CO2/
N
2
:70/30/0)
was
the
worst
case
because
of
the
higher
oxygen
concentration.
Decrease
in
lipid
oxidation
stability
with
higher
oxygen
concentrations
was
also
determined
by
various
authors
(Kennedy
et
al.,
2004;
Jakobsen
&
Bertelsen,
2000;
O'Grady
et
al.,
2000;
Jayasingh,
Cornforth,
Brennand,
Carpenter,
&
Whittier,
2002;
Zakrys
et
al.,
2008).
They
both
decreased
the
oxidation
stability
significantly
to
increase
the
carbon
dioxide
concentration
more
than
30%
and
increase
the
oxygen
concentration
from
50
to
70%.
Among
the
five
modified
atmosphere
packages
with
different
gas
composition,
MAP4
(0
2
/CO
2
/N
2
:50/30/20)
gave
the
best
results
for
oxidative
stability.
However,
Jakobsen
and
Bertelsen
(2000)
did
not
find
any
significant
effect
of
reducing
the
oxygen
from
80
to
55%
on
the
oxidation
stability
of
meat.
3.4.
Microbiological
analyses
Fig.
1
illustrates
the
results
of
the
viable
counts
of
the
targeted
microbial
groups
from
minced
meat
samples
packaged
under
different
gas
compositions
of
MAP
and
AP.
In
aerobic
packaging
of
ground
meat,
all
the
microbial
groups
showed
viable
counts
higher
than
those
of
other
MAP
applications
did
and
as
stated
in
the
literature
(Ercolini
et
al.,
2006).
Pseudomonas
spp.
particularly
were
the
dominant
population
in
the
first
three
days
of
storage
for
AP
control
samples
followed
by
lactic
acid
bacteria,
Enterobacteriaceae
and
B.
thermosphacta.
However,
packaging
under
modified
atmosphere
delayed
and
restricted
the
growth
of
these
microorganisms
depend-
ing
on
the
gas
composition
of
package.
Packaging
under
MAP1
(0
2
/CO
2
/N
2
:30/70/0)
combination
delayed
the
growth
of
LAB,
Enterobacteriaceae
family
and
completely
inhibited
the
growth
of
Pseudomonas
spp.
and
B.
thermosphacta.
MAP2(02/CO2/
N
2
:50/50/0)
combination
restricted
the
growth
of
LAB
and
delayed
the
growth
of
Enterobacteriaceae
family
and
completely
inhibited
the
growth
of
Pseudomonas
spp.
and
B.
thermosphacta.
MAP3
(02/
CO
2
/N
2
:70/30/0)
combination
favored
the
growth
of
LAB
and
Enterobacteriaceae
family
and
restricted
the
growth
of
Pseudomonas
spp.
and
B.
thermosphacta
in
comparison
with
AP
samples.
MAP4(02/
CO
2
/N
2
:50/30/20)
gas
combination
restricted
all
microorganisms
and
completely
inhibited
the
growth
of
Enterobacteriaceae
family
at
the
end
of
eleven
days
of
storage.
MAP5
(02/CO2/N2:30/30/40)
gas
combination
delayed
the
growth
of
LAB
and
Enterobacteriaceae
family,
but
the
(a)
8,00
0
7,00
-
i
-
o-AP
-
0-1111AP1
-A-
MAP2
-F
MAP3
-K-
MAP4
-
6-MAP5
P
u
ca
(..)
V
a
_i
2,00
-
11
14
5,00
-
4,00
-
3,00
-
1,00
1.day
3
5
7
9
time
after
packaging,
days
1.day
3
5
7
9
11
14
time
after
packaging,
days
(c)
7,00
-
*-AP
-
0-1111AP1
-A-MAP2
--MAP3
-x-IIIIAP4
-
e-MA1
3
5
Pseu
domonas
spp.,
log
c
fu
/g
6,00
-
5,00
-
4,00
-
3,00
-
2,00
-
1,00
-
0,00
E
,
E
,
E
,
6,00
5,00
4,00
3,00
-
2,00
-
1,00
-
0,00
7,00
(b)
7,00
(d)
-
*-AP
-
N-MAP1
-A-MAP2
-x-MAP3
-X-MAP4
-
4,-MA1
3
5
En
tero
bac
ter
iaceae,
Iog
c
fu
/g
5,00
-
4,00
-
3,00
-
2,00
iii....---
---
1,00
-
0,00
6,00
-
B.
thermosp
ac
ta
log
c
fu
/g
224
0.K
Esmer
et
at
/
Meat
Science
88
(2011)
221-226
Table
3
Changes
in
L*,
a*,
b*
and
TBA
values
a
of
minced
beaf
meat
samples
packaged
under
different
modified
atmosphere
packaging
conditions
with
storage
period.
Times
(days)
1
3
5
7
9
11
14
L*
AP
42.92
±
0.44
1
'
A
43.88
±
0.73
1
'
A
43.03
±
1.61
1
'
A
43.24
±
135
a
A
42.45
±
035
a
A
42.10±
0.69
a
A
43.18
±
1.15
a
A
MAP1
40.12
±
1.4?
A
40.26
±
030
a
A
40.17
±
0.23
ab
A
42.01
±
0.23
a
"
4332
±
1.69
a
B
NA
NA
MAP2
41.19
±
1.22a
b
A
3931
±
2.09
a
A
39.06±
0A9
a
A
41.10±330
a
A
41.15±
2.07a
A
NA
NA
MAP3
40.70
±
1.0?
A
41.00
±
1.23a
b
AB
43.65
±
2.62`"
43.67
±
1.52
a
"
44.70
±
1.2e
B
43.21
±
0.9V
.B
43.05
±
133
a
AB
MAP4
4334
±
0.91`
A
43.59±1.14
b
A
43.02
±
1.79
b
`
A
4338
±
0.49
a
A
44.48
±
1.65
a
A
4332
±
0.13
a
A
43.88
±
0.88
a
A
MAPS
43.07
±1.55
,
`
A
42.22
±
0.02
ab
A
43.79±
1.42`
A
4235
±
0.63
a
A
41.96
±
2.67
a
A
42.16±
1.51a
A
44.29
±
0.23
a
A
a*
AP
27.20
±
1.16
a
E
24.57
±
0.78
ab
DE
21.50±139
b
CD
19.56±2.05`
BC
14.41
±
3A2
b
A
15.67
±
3.72
a
AB
17.97
±2.22
b
ABC
MAP1
28.10
±
0.79
a
E
22.69
±
1.2V
"
13.14
±
0.03
a
c
11.14±0.62
a
B
8.14
±
0.28
a
A
NA
NA
MAP2
28.81
±
0.81
a
E
25.71
±
1.59
b
"
20.26
±
0.05
b
c
13.92
±
0.92
b
B
9.43
±
0.68
a
A
NA
NA
MAP3
28.92
±
0.65
a
D
26.44
±
(lo
b
C
26.13
±
1.25`
C
23.61
±
1.12c
B
22.76
±
0.45`
B
20.45
±
1.2V
A
18.29
±
0.00
b
A
MAP4
2832
±
0.81
a
F
26.03
±
0.66
b
E
24.53
±
0.42`
D
22.49
±
035
Bc
C
2035
±
033`
B
19.93
±
0.42
a
B
16.81
±0.07
b
A
MAPS
29.09
±
1.4?
D
25.79±1A2
b
D
21.55
±
1.28
b
C
20.22
±
1.72
c
d
C
14.48
±
2.75
b
B
12.22
±
4.95
a
B
8.22
±
0.59
a
A
b*
AP
23.42
±
0.61a
b
D
22.55
±
0A8
b
CD
20.78
±
0.76`
BC
20.01
±
1.42bc
B
16.73
±
1.69a
A
16.84
±
2.26a
A
17.77
±1.26
b
A
MAP1
22.27
±
0.60
a
D
20.88
±
0.56
a
c
16.82
±
1.03
a
B
16.53
±
0.10
a
"
15.29±
0.03
a
A
NA
NA
MAP2
22.75
±
0A2
a
D
22.20±
0.04
ab
D
18.14
±
035
b
c
17.23
±
0.09
a
B
15.56±
0.54
a
A
NA
NA
MAP3
22.93
±
03V
C
22.89±
0.13
b
C
21.82±
0.21
c
d
C
19.65±
0.117
1
8
1638
±1.19a
A
16.45
±
0.25a
A
16.45
±0.59a
b
A
MAP4
24.13
±
0.59
ab
E
22.84
±
0.66
b
D
2235
±
032
d
D
21.49±
0.18`
C
20.41
±
0A1
b
B
20.03
±
0.04
a
B
18.20
±
0.06
b
A
MAPS
24.89
±
0.76"
E
22.76±
0.91
b
D
20.97
±
0.92`
C
20.17
±
1.03
b
`
C
17.25
±
0.65
a
B
16.62
±
1.79a
.B
15.45
±
0.81a
A
TBA
AP
1.14
±
0.07V
A
2.09
±
0.23a
B
2.62
±
039a
C
2.50±0.00a
BC
234
±
0.00a
BC
2.73
±
0.16a
b
CD
3.12
±
0.00"
D
MAP1
1.85
±
0.078
C
A
234
±
0.16
ab
B
3.43
±
aoo
b
C
3.93
±
0.16`
"
632
±
0.23
d
E
NA
NA
MAP2
1.97
±
0.078
C
A
2.57
±
ale
B
2.73
±
0.00
a
B
3.67
±
0.00
c
C
5.93
±
0.16`
"
NA
NA
MAP3
1.93
±
0.078
C
A
237
±
0.16
ab
B
2.41
±
0.078
a
B
2.96
±
aoo
b
C
3.59±
0.078
b
D
3.67
±
0.23
1
'
D
3.98
±
0.078
C
E
MAP4
1.40
±
0.078
b
A
238
±
0.16a
b
B
2.56±0.23a
BC
2.89±
0.16
b
C
2.65
±
0.16a
Bc
2.57
±
0.00a
Bc
2.73
±
0.078a
BC
MAPS
1.25
±
0.078
ab
A
2.28
±
0.00
ab
B
2.64
±
0.16
a
B
2.57
±
0.078
a
B
2.65
±
0.078
a
B
3.27
±
0A7
b
C
3.40
±
0.31
b
C
aEach
value
is
the
mean
of
two
batch
production
with
two
samples
analyzed
per
batch
(n=4).
Means
with
different
lowercase
letters
in
the
same
column
are
significantly
different
(p<0.01).
Means
with
different
capital
letters
in
the
same
line
are
significantly
different
(p<0.01).
-
*-AP
-
0-1111AP1
-A-1111AP2
-x-IIIIAP3
-x-IIIIAP4
-•-MAP5
1.day
3
5
7
9
11
14
1.day
3
5
7
9
11
14
time
after
packaging,
days
time
after
packaging,
days
Fig.
1.
(a)
Lactic
acid
bacteria,
(b)
Enterobacteriaceae,
(c)
Pseudomonas
spp,
(d)
B.
thermosphacta
counts
of
minced
beef
meat
samples
packaged
under
different
modified
atmosphere
packaging
conditions
during
storage
at
4
°C.
O.K.
Esmer
et
al.
/
Meat
Science
88
(2011)
221-226
225
numbers
of
Pseudomonas
spp.
and
B.
thermosphacta
were
very
close
to
the
microbial
load
of
AP
samples.
The
lowest
numbers
were
obtained
in
MAP2(0
2
/CO
2
/N
2
:50/50/0)
and
MAP4(0
2
/CO
2
/N
2
:50/30/20)
combina-
tion
for
LAB.
Until
the
7th
day
of
storage
LAB
counts
increased
and
then
started
to
decrease
for
these
two
MAP
combination,
whereas
for
MAP1
(0
2
/CO
2
/N
2
:30/70/0)
and
MAP5(0
2
/CO
2
/N
2
:30/30/40)
combinations
they
slightly
increased
and
for
MAP3
(02/CO2/N2:70/30/0)
the
increase
was
higher
by
the
end
of
the
storage
period.
Enterobacteriaceae
family
were
completely
inhibited
on
the
14th
day
of
storage
in
MAP4(02/CO2/
N
2
:50/30/20)
combination.
MAP3
(0
2
/CO
2
/N
2
:70/30/0)
and
MAP4(0
2
/CO
2
/N
2
:50/30/20)
gas
combinations
restricted
the
growth
of
Pseudomonas
spp.
whereas
Pseudomonas
spp.
were
completely
inhibited
in
MAP1
(0
2
/CO
2
/N
2
:30/
70/0)
and
MAP2(0
2
/CO
2
/N
2
:50/50/0)
combinations
after
five
days
of
storage
The
growth
of
B.
thermosphacta
was
completely
inhibited
in
MAP1
(0
2
/CO
2
/N
2
:30/70/0)
and
MAP2(0
2
/CO
2
/N
2
:50/50/0)
gas
com-
binations
after
three
days
and
after
five
days
of
storage
respectively,
while
MAP4(0
2
/CO
2
/N
2
:50/30/20)
restricted
the
growth
of
it.
As
seen
from
our
results,
high-CO
2
concentration
sample
groups
as
70%CO
2
and
50%CO
2
inhibited
the
growth
of
B.
thermosphacta
and
Pseudomonas
spp.
Although
the
effect
of
carbon
dioxide,
higher
than
20%,
was
specified
in
the
literature
for
inhibition
of
Pseudomonas
spp.
(Koutsoumanis
et
al.,
2008;
Soldatou
et
al.,
2009;
Giatrakou,
Kykkidou,
Papavergou,
Kontominas,
&
Savvaidis,
2008;
Ntzimani,
Paleologos,
Sawaidis,
&
Kontominas,
2008;
Ravi
Sankar,
Lalitha,
Jose,
Manju,
&
Gopal,
2008;
Chouliara,
Karatapanis,
Sawaidis,
&
Kontominas,
2007;
Cutter,
2002;
Skandamis
&
Nychas,
2002;
Kennedy
et
al.,
2004;
Sheridan
et
al.,
1997;
Patsias,
Chouliara,
Badeka,
Sawaidis,
&
Kontominas,
2006),
there
are
some
controversial
results
for
inhibition
of
B.
thermosphacta
in
carbon
dioxide
atmospheres.
Koutsoumanis
et
aL
(2008),
expressed
that
packaging
with
low
permeability
films
(LPF)
lowered
the
growth
rate
of
B.
thermosphacta
and
Pseudomonas
spp.
due
to
the
higher
inhibitory
effect
of
carbon
dioxide
and
they
observed
a
significant
reduction
in
the
growth
rates
of
both
microorganisms
in
minced
pork
packaged
in
LPF.
Soldatou
et
aL
(2009),
Ercolini
et
al.
(2006)
and
Sheridan
et
al.
(1997)
found
that
under
high
carbon
dioxide
atmosphere
of
70%,
40%
and
50%
respectively,
growth
of
B.
thermosphacta
and
Pseudomonas
spp
was
restricted.
However,
Berruga,
Vergara,
and
Gallego
(2005);
Skandamis
and
Nychas
(2002);
Gill
and
Harrison
(1989)
and
Patsias
et
aL
(2006)
determined
an
important
growth
of
B.
thermosphacta
in
carbon
dioxide
atmospheres.
It
was
explained
that
the
behaviors
of
LAB
were
fully
anticipated
considering
the
fact
that
LAB
are
facultative
anaerobic
and
are
able
to
grow
both
in
the
presence
and
absence
of
oxygen
(Patsias,
Badeka,
Savvaidis,
&
Kontominas,
2008).
According
to
our
results,
while
LAB
counts
for
AP
control
samples
increased
throughout
the
storage,
LAB
counts
of
MAP2(0
2
/CO
2
/N
2
:50/50/0)
and
MAP4(0
2
/CO
2
/N
2
:50/30/
20)
samples,
with
the
amount
of
oxygen
as
50%,
began
to
decrease
after
the
7th
day
of
storage
and
by
the
end
of
the
14th
day
of
storage,
there
was
a
decrease
of
about
1.48
log
cfu/g
and
0.30
log
cfu/g
for
each
samples
respectively.
LAB
counts
of
MAP1(0
2
/CO
2
/N
2
:30/70/0)
and
MAP5
(0
2
/CO
2
/N
2
:30/30/40)
samples,
in
which
the
amount
of
oxygen
started
as
30%,
increased
slightly
until
the
end
of
storage
period,
whereas
there
was
an
increase
of
about
0.42
log
cfu/g
for
MAP1
(02/CO2/
N2
:3
0/70/0
)
sample
and
an
increase
of
135
log
cfu/g
for
MAP5
(02/CO2/
N2
:3
0/3
0/40
)
sample.
However,
for
MAP3
(0
2
/CO
2
/N
2
:70/30/0)
sample,
which
contains
high
amounts
of
oxygen,
LAB
counts
increased
by
about
2.88
log
cfu/g
until
the
end
of
storage
period.
In
agreement
with
our
results,
Kennedy
et
al.
(2004)
found
that
LAB
counts
increased
throughout
the
storage
period
with
different
MAP
combinations
that
have
high
oxygen
and low
carbon
dioxide,
but
the
MAP
combinations
that
have
the
higher
oxygen
content
gave
slightly
higher
LAB
counts.
Koutsoumanis
et
al.
(2008)
found
that
until
the
8th
day
of
storage,
LAB
counts
increased
and
then
started
to
decrease
in
LPF
samples,
where
the
produced
carbon
dioxide
is
maintained
in
the
headspace.
Skandamis
and
Nychas
(2002)
found
that
100%
CO
2
decreased
the
growth
rate
of
LAB
compared
with
40%CO
2
/30%0
2
/30%N
2
at
5
°C.
Ercolini
et
al.
(2006)
found
lower
counts
for
MAP
applications
containing
different
amounts
of
oxygen,
carbon
dioxide
and
nitrogen
with
respect
to
air
packaged
samples.
In
the
study
of
Patsias
et
al.
(2006),
high-CO
2
MAP
application
lowered
the
LAB
counts
compared
to
aerobic
packaging.
Aksu,
Kaya,
and
Ockerman
(2005)
also
showed
the
effects
of
high-CO
2
MAP
application
compared
to
aerobic
packaging
for
inhibition
of
LAB
counts.
Contrary
of
our
results,
it
was
determined
by
some
researchers
that
LAB
can
grow
under
high
concentrations
of
CO
2
in
MAP
products
as
facultative
anaerobic
bacteria
(Giatrakou
et
aL,
2008;
Ntzimani
et
aL,
2008;
Arkoudelos,
Stamatis,
&
Samaras,
2007;
Chouliara
et
al.,
2007;
Franzetti,
Martinoli,
Piergiovanni,
&
Gali,
2001).
MAP
applications
limited
the
growth
of
Enterobacteriaceae
in
comparison
to
AP
samples
in
all
groups
irrespective
of
gas
combina-
tions
applied.
However,
it
was
completely
inhibited
in
MAP4
(02/CO2/
N
2
:50/30/20)
samples
on
the
14th
day
of
storage.
Compatible
with
our
results,
Berruga
et
al.
(2005)
found
that
Enterobacteriaceae
counts
in
lamb
meat
increased
throughout
the
storage
period
and
the
presence
of
CO
2
levels
over
40%
in
packs
limited
the
growth
of
Enterobacteriaceae.
Soldatou
et
al.
(2009)
found
the
same
trend
for
Enterobacteriaceae
counts
in
lamb
meat
throughout
the
storage
period
in
comparison
with
air
packaging.
Compatible
with
our
results,
Chouliara
et
al.
(2007)
determined
that
Enterobacteriaceae
grew
under
MAP
conditions
at
a
slower
rate
than
under
aerobic
packaging.
However,
in
contrast
to
our
results
Ravi
Sankar
et
al.
(2008)
found
higher
counts
for
the
gas
combination
of
40%CO
2
+
30%0
2
+
30%N
2
than
five
gas
combinations,
which
contain
CO
2
concentration
between
40-70%
and
0
2
concentration
between
60-30%.
They
also
found
that
the
behavior
of
Enterobacteriaceae
was
different
in
MAP
combinations
with
the
same
carbon
dioxide
concentration
as
we
found
for
MAP3
(0
2
/CO
2
/N
2
:70/30/0),
MAP4(
0
2
/CO
2
/N
2
:50/30/20)
and
MAPS
(0
2
/
CO
2
/N
2
:30/30/40).
Patsias
et
al.
(2008)
did not
find
any
difference
for
Enterobacteriaceae
counts
in
chilled
precooked
chicken
product
between
air
packaging
and
MAP
applications
of
30%CO
2
+
70%N
2
,
60%CO
2
+
40%N
2
and
90%CO
2
+
10%N
2
.
Goulas,
Chouliara,
Nessi,
Kontominas,
and
Savvaidis
(2005)
also
did
not
find
any
effect
of
MAP
application
on
Enterobacteriaceae
counts
in
mussels
stored
under
modified
atmospheres
of
50%CO
2
+
50%N
2
,
80%CO
2
+
20%N
2
,
40%CO
2
+
30%0
2
+
30%N2.
4.
Conclusion
Increasing
the
concentration
of
CO
2
in
modified
atmosphere
applications
resulted
with
a
decrease
in
oxidation
stability
and
loss
of
redness
due
to
the
metmyoglobin
formation,
which
means
a
decrease
in
the
a*
and
b*
values
of
samples,
whereas
the
lightness
of
samples
were
not
affected.
The
oxidation
stability
and
the
color
of
minced
beef
meat
packaged
in
modified
atmospheres
were
best
preserved
in
atmospheres
containing
low
CO
2
concentrations
(30%)
rather
than
high
(70-50%)
concentrations
although
high-CO
2
con-
centrations
inhibited
the
growth
of
spoilage
microorganisms.
However,
the
oxygen
concentration
is
also
an
important
factor
in
the
shelf-life
of
fresh
red
meat.
High
concentrations
of
oxygen
(50-70%)
are
effective
in
maintaining
and
prolonging
the
redness
of
meat,
whereas
it
also
leads
to
the
decrease
in
lipid
stability.
When
we
keep
the
carbon
dioxide
concentration
as
30%,
we
determined
that
keeping
the
oxygen
concentration
as
low
as
30%
was
not
enough
to
maintain
the
redness
of
minced
beef
meat
throughout
the
storage
period.
When
we
compare
the
MAP
groups
having
50%
and
70%
oxygen
concentration,
we
determined
that
oxidation
stability
is
better
with
50%
than
in
70%
as
well
as
microbial
growth,
whereas
there
was
no
significant
difference
in
the
redness
of
samples.
As
a
result,
we
concluded
that,
the
best
preservation
for
minced
beef
meat
was
in
MAP4
gas
combination
maintaining
acceptable
color
together
with
oxidation
stability
and
acceptable
microbial
loads
until
the
end
of
storage
period
of
fourteen
days.
0.K
Esmer
et
al.
/
Meat
Science
88
(2011)
221
-
226
226
Acknowledgements
Acknowledgements
are
BANVIT
A.S.
Bandirma
Balikesir
for
their
support
in
to
this
project.
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