Meat Science 81 (2009) 467473

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Meat Science
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Colour of ground beef as inuenced by raw materials, addition of sodium

chloride and low oxygen packaging
O. Srheim a,*, F. Westad a,b, H. Larsen a, O. Alvseike c
a
Matforsk AS Noma Food, Osloveien 1, NO-1430 s, Norway
b
ABBON AS, P.O. Box 155, NO-1325 Lysaker, Norway
c
Animalia Meat and Poultry Research Centre, P.O. Box 396, kern, NO-0513 Oslo, Norway

a r t i c l e i n f o a b s t r a c t

Article history: The study aimed at examining the effects of freezing of raw materials, holding time for fresh raw mate-
Received 12 June 2008 rials post mortem and addition of 0.51.0% NaCl on the colour of ground beef under low oxygen (O2)
Received in revised form 19 September modied atmosphere storage. The samples were exposed to 0.13.0% O2 at 4 C for up to 10 days, and
2008
analysed for O2 concentrations, instrumental and visual colour. Residual O2 in the headspace of the pack-
Accepted 25 September 2008
ages oxidizes myoglobin and discolours the meat. Meat may have the ability to scavenge residual O2, and
ground beef differs from intact muscles by having a much higher capacity for O2 consumption. In this
experiment, the use of frozen/thawed raw materials and addition of NaCl both decreased the rate of
Keywords:
Ground beef
O2 consumption and increased discolouration. Using raw materials from 2 days rather than 7 days post
Freezing mortem greatly increased the rate of removal of O2 and improved redness. In low O2 packaging, ground
Holding time post mortem beef preferably should be stored for at least 2 days in an atmosphere with less than 0.1% residual O2 to
Sodium chloride produce a purple pigment predominantly consisting of deoxymyoglobin.
Modied atmosphere packaging 2008 Elsevier Ltd. All rights reserved.
Residual oxygen
Colour

1. Introduction
Obtaining a stable red or purple colour of ground beef is a chal-
lenge, since the colour is inuenced by a number of internal and
external factors. Raw materials of meat vary considerably in their
ability to produce and maintain colour. The grinding of meat can
be detrimental to the colour by causing tissue disruption and
incorporation of oxygen (O2), thereby altering the inherent reduc-
ing system (Kropf, Hunt, & Piske, 1985; Madhavi & Carpenter,
1993).
The level of O2 in the modied atmosphere packages has a di-
rect impact on the colour of the muscle pigment myoglobin. High
concentrations of O2 produce the bright red oxygenated oxymyo-
globin (OMB), low concentrations of O2 the gray/brown oxidized
metmyoglobin (MMB), and anaerobic conditions the reduced pur-
ple deoxymyoglobin (DMB). Wrapping of meat in a highly O2 per-
meable lm gives an initial bright red, but unstable colour and
short time available for retail display. High O2 packaging increases
the colour stability, but has several detrimental quality effects,
including premature browning of cooked meat, lipid oxidation
and reduced tenderness (Lund, Lametsch, Hviid, Jensen, & Skibsted,
* Corresponding author. Tel.: +47 64970100; fax: +47 64970333.
E-mail address: oddvin.sorheim@matforsk.no (O. Srheim).
2007; Mancini & Hunt, 2005; Srheim, 2006). The recent knowl-
edge about the disadvantages of high O2 packaging for meat has di-
rected more interest and research towards low O2 packaging with
atmospheres consisting mainly of mixtures of carbon dioxide (CO2)
and nitrogen (N2). The colour of meat in low O2 atmospheres can
be stabilized with the addition of low concentrations (<0.5%) of
carbon monoxide (CO) (Lanier, Carpenter, Toledo, & Reagan,
1978; Srheim, 2006). In markets where CO is not allowed or desir-
able to use, meat in low O2 atmospheres is often adversely discol-
oured, due to formation of MMB by the oxidizing effect of residual
O2 that inevitably is present in the headspace.
Keeping meat in low concentrations of residual O2 for an ex-
tended time increases the formation of MMB and produces thick
layers of this pigment form, which eventually may hinder the
desirable reduction to DMB. Maximum formation of MMB in beef
semitendinosus muscles stored in CO2 atmospheres occurred with
approximately 1.0% residual O2 present (Ledward, 1970). However,
O2 concentrations as low as 0.010.15% can cause myoglobin oxi-
dation and discolouration in beef (Gill & McGinnis, 1995a; Mancini
& Hunt, 2005; OKeeffe & Hood, 1980; Penney & Bell, 1993). Discol-
ouration initiated by residual O2 is similar in beef and lamb (Pen-
ney & Bell, 1993), while pork can tolerate 0.51.0% O2 (Penney &
Bell, 1993; Srheim, Erlandsen, Nissen, Lea, & Hyem, 1997). In
commercial packaging, obtaining the low levels of O2 needed for

0309-1740/$ - see front matter 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.meatsci.2008.09.010
468 O. Srheim et al. / Meat Science 81 (2009) 467473
dark meats are difcult, in particular for ground beef, where O2 is
incorporated in the batches during grinding (Kropf et al., 1985).
The colour of fresh meat is affected by enzymes responsible for
oxygen consumption rate (OCR) and metmyoglobin reductase
activity (MRA). High OCR internally in the meat can reduce the
time that the meat is exposed to detrimental levels of residual O2
during storage in low O2 atmospheres (OKeeffe & Hood, 1980).
Grinding increased the OCR of beef (Madhavi & Carpenter, 1993).
The internal O2 consumption activity in meat is gradually lost by
time post mortem, due to depletion of substrates and enzymes in-
volved in mitochondrial respiration (OKeeffe & Hood, 1982). As an
alternative to the internal O2 consumption of the meat, O2 scaveng-
ers can be placed inside low O2 packages or incorporated in lm
laminates, but the scavengers are often removing O2 too slowly
to prevent beef muscle surface discolouration (Beggan, Allen, &
Butler, 2006; Gill & McGinnis, 1995b). In addition to the utilization
of rapid O2 consumption, undesirable MMB can be transformed to
DMB by a high internal MRA. The process of MMB reduction re-
quires nicotinamide adenine dinucleotide (NADH) (Mancini &
Hunt, 2005). When the reductant pool of NADH is depleted,
MMB is rapidly formed. High storage temperatures accelerated
MRA, but the total MRA was depleted faster (Kropf et al., 1985).
The MRA of beef muscles was only reduced to approximately
90% of its original level at 7 days storage, and was not affected
by grinding (Madhavi & Carpenter, 1993). Freezing is expected to
further reduce MRA and OCR by decreasing enzymatic activities.
Frozen meat is commonly used in ground beef production to regu-
late the meat temperature during grinding and to avoid fat
smearing.
The temperature during grinding can also be controlled by add-
ing ice. In Norway, it is permitted to add up to 5% water or ice to
ground meat, as well as 1% sodium chloride (NaCl) for the purpose
of binding excess water. Unfortunately, NaCl is known to be a pro-
oxidant to heme pigments (Brooks, 1938). Hemoglobin is autooxi-
dized under the presence of chloride ions (Wallace, Houtchens,
Maxwell, & Caughey, 1982). Trout (1990) added 0.53.0% NaCl to
ground beef, and found that 1% NaCl doubled the MMB formation
compared to no NaCl. Accordingly, Torres, Pearson, Gray, Booren,
and Shimokomaki (1988) found increasing MMB levels with addi-
tion of NaCl in the range 0.54.0%.
The aim of the present study was to examine the effects of using
frozen/thawed raw materials, different holding times for fresh raw
materials post mortem, addition of NaCl and level of residual O2 in
CO2/N2 packaging on the colour of ground beef.
2. Materials and methods
2.1. Experimental set-up
The study was divided in two: part A was fully performed at
Matforsk AS Noma Food, and in part B the ground beef was pro-
duced and packaged at a commercial abattoir, followed by storage
and analyses at Matforsk AS Noma Food. Beef trimmings, ex-
cised mainly from the forequarter, and containing 14% fat, 19% pro-
tein and 67% water according to plant specications, were used in
both studies. The meat for part A was packaged 7 days post mor-
tem, and for part B 2 days post mortem.
In part A, the following six series were produced:
 fresh, unfrozen meat without NaCl or water (A1);
 fresh, unfrozen meat with 0.5% NaCl and 2.5% water (A2);
 fresh, unfrozen meat with 1.0% NaCl and 5.0% water (A3);
 frozen/thawed meat without NaCl or water (A4);
 frozen/thawed meat with 0.5% NaCl and 2.5% water (A5);
 frozen/thawed meat with 1.0% NaCl and 5.0% water (A6).
In part B, two series were produced:
 fresh, unfrozen meat without NaCl or water (B1);
 fresh, unfrozen meat with 1.0% NaCl and 5.0% water (B2).
2.2. Processing, packaging and storage
In part A, a batch of 60 kg beef trimmings was divided in two
batches of 30 kg each: one for immediate processing (series A1,
A2 and A3), and one was vacuum packaged in polyamide bags
and frozen at 20 C for 3 weeks (series A4, A5 and A6). The frozen
meat was thawed at 3 C for 3 days before processing. The pH of
the fresh meat was 5.65. The meat was rst ground (Seydelman
ME 130 Grinder, Stuttgart, Germany) through a plate with 8 mm
openings, followed by manual blending of a brine with NaCl and
water for series A2, A3, A5 and A6 only. Thereafter, the meat was
ground for the second time through a plate with 4 mm openings.
Within 1 h after the nal grinding, 400 g portions of ground beef
in part A were placed on polystyrene trays and ushed with a gas
mixture of 55% CO2/45% N2 (Yara International, Oslo, Norway) in
25  40 cm pouches on a Webomatic C 50-D chamber machine
(Webomatic, Bochum, Germany). The pouches with an ethylenevi-
nylalcohol barrier layer had an O2 transmission rate (OTR) of
3 cm3/m2/24 h at 23 C and 75% relative humidity (RH) (Nordlm
B 206, Nordpak OY, Valkenkoski, Finland). The gas to meat product
ratio was approximately 2.5:1. The initial concentrations of resid-
ual O2 in the packages varied, but were as low as 0.1%. Twenty
packages were produced per series by adjusting residual O2 con-
centrations in the range 0.11.5% by injecting appropriate volumes
of air by using needles and syringes of 10 and 50 cm3. The level of
O2 varied in intervals of approximately 0.05% in the 0.10.5% range
and in approximately 0.15% intervals in the 0.51.5% range. The
ranges for O2 concentrations were equal for fresh (series A1, A2
and A3) and frozen/thawed (series A4, A5 and A6) samples. The
needles were inserted through selfadhesing and selfsealing rubber
septas on the packages (Toray TO 125, Toray Engineering, Osaka,
Japan). The ground beef packages were all stored in darkness at
4 C for 9 days. At the end of storage, no off-odour or spoilage were
detected in the meat.
The processing and packaging conditions for part B differed a
little from part A. In part B, complete packages of ground beef were
collected at a commercial abattoir Nortura, Tnsberg, Norway). The
series B1 and B2 were typical for the production at the abattoir.
The meat was ground twice, and the second time though a plate
with 3 mm openings. The pH of the meat before packaging was
5.75. Within 1 h after the last grinding, portions of 500 g (series
B1) and 400 g (series B2) were packaged on a CFS Tiromat thermo-
forming machine (Convenience Food Systems, Bakel, The Nether-
lands). The upper and lower lms had OTRs of <30 cm3/m2/24 h
at 23 C and 75% RH. The gas mixture consisted of 55% CO2/45%
N2 (Yara International). The gas to product ratios were 0.8:1 and
1.1:1 for series B1 and B2, respectively. For each series, 20 packages
with residual O2 concentrations of 0.13.0% were produced by
injecting air, as for part A. Residual O2 intervals were closer in
the lower than then upper parts of the range. After adjustment of
the residual O2 levels at the abattoir, the packages were trans-
ported to Matforsk AS Noma Food, and stored in darkness at
4 C for 10 days. At this time, the meat had no detectable off-odour
or spoilage.
2.3. Analyses
The concentrations of O2 in the headspace of all packages were
analysed at packaging and after 1, 2, 3, 6 and 9 days of storage (part
 O. Srheim et al. / Meat Science 81 (2009) 467473 469

A), and 1, 2, 4, 7 and 10 days of storage (part B). CO2 concentrations

were analysed as 510 spot tests at all sampling times. O2 was
determined by using a Toray LC 700-F zirconium cell instrument
(Toray Engineering, Osaka, Japan), calibrated against air and a
0.103% O2 gas standard (Yara International). CO2 was measured
on a Toray PG-100 infrared instrument (Toray), calibrated against
air and a 100% CO2 gas standard (Yara International). The threshold
levels for the O2 and CO2 analyses were 0.05% and 1%, respectively.
Gas samples of 5 cm3 were collected with a syringe through self-
sealing septas (Toray TO 125).
Instrumental colour CIE a* redness values were measured with
a Minolta Chroma Meter CR-300 (Minolta Camera Co., Osaka, Ja-
pan) with a 8 mm viewing port, 2 viewer angle and illuminant
D65. The instrument was calibrated against a white tile
(L* = 97.16, a* = 0.25 and b* = 2.09). The samples were measured
in intact packages at the meat surface through the transparent
lms (AMSA, 1991). The a* measurements were performed in four
replicates per sample at the same sampling times as the gas
analyses.
Fig. 1. Oxygen concentrations (%) in packages of ground beef with different levels of
Visual colour evaluation was performed by a three member NaCl (0%, 0.5% and 1.0%) (a) and use of fresh or frozen/thawed raw materials (b) in
trained panel. The meat surface colour in intact packages was as- the small scale experiment (part A).
sessed on a scale of 1 = bright dark red, 2 = purple or dark red,
3 = slightly brown or gray, 4 = moderately brown or gray and The average O2 concentrations during storage of the packages as
5 = extremely brown or gray (adapted from AMSA (1991)). The related to level of NaCl and the use of fresh or frozen/thawed meat
sampling times for the visual colour evaluation equalled the times are shown in Fig. 1 a and b, respectively. The initial average O2 con-
for instrumental colour analyses and O2 analyses. centrations in all six series were approximately 0.55%. A more ra-
pid decline in O2 concentrations occurred for the 0% than the
2.4. Statistics 0.5% and 1.0% NaCl treatments. A multiple comparisons test
showed signicant differences for O2 concentrations at the three
The collected data from the two experimental designs were levels of NaCl (p < 0.05). The O2 concentration of the treatments
analysed with analysis of variance (ANOVA). The responses of without NaCl decreased from day 0 to days 9 storage, reaching a
interests were O2 concentration, CIE a* value and visual colour critical level below 0.1% at 9 days. For the 0.5% and 1.0% NaCl treat-
score. Detailed analyses including individual packages and repli- ments, O2 concentrations were stable between days 0 and 3, fol-
cates were performed as well as on averaged data. The conclusions lowed by a decrease. The reduction in O2 concentrations was
regarding the importance of the experimental factors were consis- faster in samples made from fresh than frozen raw materials
tent, thus, only the results from the averaged data are given below. (p < 0.05). The samples of fresh meat reached an average O2 con-
Multiple comparisons tests (Tukey) were also conducted. The soft- centration of 0.1% after 9 days storage.
ware packages SAS (SAS Institute Inc., Cary, NC, USA) and The To demonstrate the impact of raw materials with both high and
Unscrambler 9.6 (Camo Software, Oslo, Norway) were used for low capability to remove detrimental O2, four examples of the
the ANOVA. development in O2 concentrations are shown in Fig. 2. Two sam-
ples of fresh meat, without NaCl added and with initial O2 concen-
3. Results and discussion trations of 0.15% and 0.4%, passed the level of 0.1% O2 after

3.1. Small scale experiment part A

A summary for the results of part A is given in Table 1 as an AN-

OVA table. In addition to the p values, the amount of variance due
to the experimental factors and their interactions are presented.

Table 1
ANOVA results on ground beef samples from the small scale experiment in part A. The
samples were made from fresh or frozen/thawed raw materials and with different
levels of NaCl (0%, 0.5% and 1.0%).

Effect a* redness Visual colour Oxygen

p Exp. p Exp. p Exp.
value variance value variance value variance
(%) (%) (%)
Fresh/ 0.006 7 <0.001 35 <0.001 9
frozen
(A)
Salt conc. <0.001 56 0.015 12 <0.001 18
(B)
Day (C) 0.005 17 0.604 2 <0.001 66
AB 0.295 1 0.436 2 0.001 3 Fig. 2. Examples from the small scale (part A) experiment of rapid and slow
AC 0.107 6 0.128 8 0.059 1 reduction in O2 levels (%) in packages of ground beef by use of fresh raw materials
BC 0.091 10 0.016 34 0.266 1 without addition of NaCl compared to frozen/thawed raw materials with addition
of 1.0% NaCl.
470 O. Srheim et al. / Meat Science 81 (2009) 467473

approximately 1 and 4 days of storage, respectively. In contrast,

two samples of frozen meat with 1% NaCl added and with similar
initial O2 concentrations, did not pass the level of 0.1% O2, even
after 9 days storage. These examples clearly illustrate how a rapid
removal of residual O2 in the headspace can be achieved by using
fresh raw materials without addition of NaCl.
The concentration of CO2 was reduced from an initial level of
55% to approximately 47% after 9 days storage in all series (results
not shown). A rapid decrease in CO2 concentrations was noted dur-
ing the rst 3 days of storage, due to absorption of the gas in the
meat. There were no differences in CO2 concentrations between
the series (p > 0.05).
The visual colour evaluation, as shown in Fig. 3a, demonstrated
that samples without NaCl had a lower colour score (more red and
less discoloured) than samples with 0.5% and 1.0% NaCl at days 6
and 9 of storage (p < 0.05). At the same storage times, samples with
0.5% NaCl were less discoloured than with 1.0% NaCl (p < 0.05).
Data in Fig. 3b show that samples of fresh meat were redder than
samples of frozen meat between days 2 and 9 of storage (p < 0.05).
The instrumental colour analyses conrmed the results of the
visual colour evaluation. Fig. 4a and b demonstrates that ground
beef without NaCl, as well as use of fresh meat increased a* values
(redness) during the 9 days of storage, particularly at the last phase
Fig. 4. a* redness values of ground beef packaged in CO2/N2 with residual O2 with
of the storage. The a* values were signicantly different for the different levels of NaCl (0%, 0.5% and 1.0%) (a) and use of frozen/thawed raw
three NaCl levels (p < 0.05). materials (b) in the small scale experiment (part A).
An example of details of the visual colour evaluation of all 20
samples of frozen raw materials without NaCl (series A4) is shown Table 2
in Table 2. Values with an acceptable score of 3 or less are printed Visual colour evaluation of individual ground beef samples made of frozen/thawed
in bold numbers. The data demonstrated that only samples with an meat without addition of salt (series A4) from the small scale experiment (part A)
initial O2 concentration of 0.32% or lower had an acceptable colour during storage at 4 C from 1 to 9 days. Colour scale: 1 = bright dark red, 2 = purple or
dark red, 3 = slightly brown or gray, 4 = moderately brown or gray, and 5 = extremely
after 9 days storage. These samples gradually improved in colour
brown or gray. Acceptable colour scores at or below 3.0 are in bold numbers.
scores during the storage period. Samples with initial O2 concen-
trations in the range 0.380.68%, seemed to improve in colour up Initial O2 concentration (%) Day 1 Day 2 Day 3 Day 6 Day 9
to day 6, but later were more discoloured again. For samples in 0.07 4.5 4.0 3.5 2.5 3.0
the range 0.841.53% initial O2, a gradual discolouration was ob- 0.14 4.5 4.0 3.5 3.0 2.0
0.15 4.5 4.0 3.5 2.5 2.5
served throughout storage. It is interesting to notice that the two
0.18 4.5 4.0 3.5 3.0 3.0
samples with the highest initial O2 concentrations of 1.37% and 0.20 4.5 4.0 3.5 2.5 1.5
1.53%, both had acceptable colour scores at day 1, but not at later 0.25 4.5 4.0 3.5 3.0 1.5
0.28 4.5 4.0 3.5 2.5 2.0
0.32 4.5 4.0 3.5 3.5 1.5
0.38 4.5 4.0 3.5 3.5 4.0
0.43 4.5 4.0 3.5 3.5 4.0
0.45 4.0 4.0 3.5 3.5 4.0
0.46 4.0 3.5 3.5 3.5 4.0
0.60 4.0 3.5 3.5 3.5 4.0
0.68 4.0 3.5 3.5 3.5 4.5
0.84 3.5 3.5 3.5 m m
0.94 3.5 3.5 3.5 4.0 4.5
1.02 3.5 3.5 3.5 4.0 4.5
1.11 3.5 3.5 3.5 4.0 4.5
1.37 3.0 3.5 3.5 4.0 4.5
1.53 2.5 3.5 3.5 4.0 4.5

m = missing values because of leakages.

storage. The cause for the relatively low colour scores and accept-
able redness at day 1 is probably a slow transformation of OMB,
which still partly remained at the meat surface at that time as a
consequence of O2 inclusion by the grinding. The high colour score
and severe discolouration at day 1 of samples with initial O2 con-
centrations of 0.070.43% was probably due to release of O2 from
the ground meat and the pigment being in a transient state of
metmyoglobin.

Fig. 3. Visual colour evaluation of ground beef packaged in CO2/N2 with residual O2
with different levels of NaCl (0%, 0.5% and 1.0%) (a) and use of frozen/thawed raw
materials (b) in the small scale experiment (part A). Colour scale: 1 = bright dark
red, 2 = purple or dark red, 3 = slightly brown or gray, 4 = moderately brown or gray,
and 5 = extremely brown or gray.
3.2. Industrial experiment part B
Table 3 shows the results of the ANOVA analysis for part B of the
study. Only the main effects are given, as there were no degrees of
 O. Srheim et al. / Meat Science 81 (2009) 467473 471

Table 3
ANOVA results of ground beef samples from the industrial experiment in part B. The
samples were all made of fresh raw materials and with different levels of NaCl (0% or
1.0%).

Effect a* redness Visual colour Oxygen

p Exp. variance p Exp. variance p Exp. variance
value (%) value (%) value (%)
Day 0.104 20 0.100 30 0.442 37
Salt 0.002 75 0.004 63 0.119 31

freedom left for estimating the error for a model with interaction
terms in this case.
The results for the average O2 concentrations of part B are
shown in Fig. 5. Initial O2 concentrations were as expected higher
in part B than A, approximately 0.90% and 0.55%, respectively.
However, O2 concentrations in part B dropped sharply within the
rst day of storage, reaching the critical level of 0.1% O2 in 1 day
for samples without NaCl and in 4 days for samples with 1% NaCl
added. Levels of O2 were lower for the non-salted than the salted Fig. 6. Visual colour evaluation of fresh ground beef packaged in CO2/N2 with
samples at 1 and 2 days of storage (p < 0.05). The CO2 concentra- residual O2 and without or with 1.0% NaCl in the industrial experiment (part B).
tions in packages of part B were reduced rapidly from the initial Colour scale: 1 = bright dark red, 2 = dark red or purple, 3 = slightly brown or gray,
4 = moderately brown or gray, and 5 = extremely brown or gray.
55% to approximately 35% at day 10 of storage with no differences
between the two treatments (results not shown). The gas to meat
ratio was lower in part B than A, causing more reduction in CO2
percentage.
The visual colour evaluation for part B in Fig. 6, showed that the
average colour score was below 3 and thus acceptable as early as at
day 1 of storage for unsalted samples. The treatment with 1% NaCl
obtained an acceptable colour score after 4 days. The instrumental
redness values of part B, as shown in Fig. 7, conrmed the results of
the visual colour evaluation with higher a* redness for the treat-
ment without NaCl.
By comparing visual colour scores and instrumental a* values
for individual samples in both parts A and B, an acceptability level
of a* > 12 was established. The correlation between visual colour
evaluation and a* redness values in this study was high with r of
0.93. Details of a* values for all samples with addition of 1.0%
NaCl of part B (series B2) are shown in Table 4. Interestingly, there
was a general increase in a* values for all samples with increasing
storage time, probably reecting the decrease in O2 level of the
headspace. A sample with a high initial O2 concentration of 1.94%
had an acceptable a* value of 12.8 at 10 days storage. Samples with

Fig. 7. a* redness values of ground beef packaged in CO2/N2 with residual O2 and
without or with 1.0% NaCl in the industrial experiment (part B).

initial O2 concentrations at or below 0.41% all had acceptable

instrumental colour values after 2 days storage. At day 1, the sam-
ple with an initial O2 concentration of 1.03% had the lowest a* va-
lue and was most discoloured. Higher or lower O2 concentrations
at this time resulted in higher a* values as related to less formation
of metmyoglobin.

3.3. Interactions between raw materials, NaCl levels, O2 concentrations

and colour

The two experiments A and B clearly demonstrated that the col-

Fig. 5. Oxygen concentrations (%) in packages of fresh ground beef without or with
1.0% NaCl in the industrial experiment (part B).
our of ground beef is highly affected by the level and rate of inter-
nal consumption of O2 by the meat. Grinding of beef muscles
substantially increased the OCR compared to intact muscles
(Madhavi & Carpenter, 1993). In support of these ndings, beef
steaks were not able to reduce the level of residual O2 in the head-
space of a CO2/N2 atmosphere over a storage period of 7 days (Beg-
gan et al., 2006). Our results, particularly in part B, showed that the
472 O. Srheim et al. / Meat Science 81 (2009) 467473

Table 4 residual O2 that has to be consumed by the meat. Other require-

a* redness values of individual ground beef samples made from fresh meat with ments include using packaging lms with a high O2 barrier, and en-
addition of 1% NaCl (series B2) from the industrial experiment (part B) during storage
at 4 C from 1 to 10 days. Acceptable a* values above the value of 12 are in bold
sure that leakages do not occur in the packages during storage.
numbers. As demonstrated in both parts A and B of the study, addition of
NaCl to the ground beef was detrimental to its colour, because NaCl
Initial O2 concentration (%) Day 1 Day 2 Day 4 Day 7 Day 10
slowed down the rate of O2 consumption. The 1% NaCl addition,
0.09 14.4 16.0 15.2 13.6 m but also the 0.5% level, had a clear negative effect on O2 removal
0.10 14.2 15.2 14.5 15.7 16.5
0.15 13.6 15.9 13.7 m m
and colour. Trout (1990) showed that in ground beef stored for
0.21 13.1 15.1 14.8 m m 24 h the concentrations of MMB was approximately 50% and
0.25 12.4 12.7 12.5 m m 100% higher with 0.5% and 1.0% NaCl compared to unsalted meat.
0.33 11.0 14.1 m m m When the concentration of NaCl increased from 1.0% to 3.0%, the
0.38 11.1 13.4 14.8 15.6 15.6
level of MMB increased further by only 20%. Torres et al. (1988)
0.41 10.4 13.4 15.1 14.5 15.9
0.59 10.3 12.0 13.7 14.4 15.4 used 0.5% and 2.0% NaCl addition to post-rigor ground beef, and
0.68 10.0 9.7 13.5 14.6 15.7 demonstrated that MMB levels increased with both NaCl levels at
0.95 9.9 9.4 11.9 14.2 15.1 4 days storage. The pH decline of the meat with these two NaCl lev-
1.03 8.7 8.7 11.3 12.7 15.4 els was 0.08 and 0.20, respectively. NaCl also has the ability to
1.29 9.6 10.6 11.1 12.6 14.9
accelerate lipid oxidation, which may trigger myoglobin oxidation
1.34 9.7 9.3 10.3 11.9 15.2
1.62 9.8 8.2 10.2 12.3 13.7 of ground beef (Torres et al., 1988).
1.94 9.3 9.7 9.0 11.8 12.8 The samples with salt contained up to 1% NaCl and 5% water.
2.35 9.7 8.8 8.9 9.4 11.4 The sum of these two components created a diluting effect of the
3.04 10.2 8.3 8.5 9.3 10.1
myoglobin in the samples, probably causing a slight decrease in vi-
m = missing values because of leakages. sual and instrumental redness. However, the magnitude of this
myoglobin dilution is much smaller than the effect of NaCl as a
prooxidant on the colour of the ground beef.
ground meat contributed considerably to the removal of O2 from Part A of the study showed that freezing was another factor to
the headspace. In a low O2 packaging system, it is benecial to uti- retard the rate of O2 consumption, and therefore made the meat
lize meat sources with a high OCR for obtaining a rapid and com- more discoloured. Freezing probably reduced the activity of en-
plete removal of O2. In contrast, for a high O2 packaging system, zymes involved in O2 consumption. Frozen meat is used to control
a low OCR is desirable for improving blooming and binding of large temperature during grinding of meat. Considering enhancement of
amounts of O2 to myoglobin (Mancini & Hunt, 2005). the colour of ground beef, using solid CO2 as a processing aid is
The O2 consumption of the ground beef in part B was much likely to be a better approach for temperature adjustment
more rapid than in part A, probably caused by using meat raw (Srheim, Uglem, Lea, Claus, & Egelandsdal, 2006).
materials of 2 days compared to 7 days post mortem. The develop- In a successful low O2 packaging for ground beef, the pigment
ment in percentage residual O2 in the headspace in our study can typically changes rapidly from initial OMB, through transient
be seen as a direct expression of OCR. In a previous study, the MMB to the nal DMB, depending on the exposure to different lev-
OCR was substantially reduced in ground beef longissimus dorsi els of O2 throughout the process (Mancini & Hunt, 2005). The time
and psoas major muscles between 1 and 7 days storage, with a par- that the meat is in the transient state of MMB could be shortened
ticular high decline before 3 days (Madhavi & Carpenter, 1993). In by increasing the temperature, but is not recommendable due to
mitochondria and cardiac tissue of beef, the OCR was lowered with risk of increased growth of bacteria.
3040% between 2 h and 4 days post mortem (Tang et al., 2005b). By evaluating the results on O2 consumption and colour for all
These authors added several chemical compounds to the sub- individual samples in parts A and B of the study, a storage time
strates for increasing the OCR, among which rotenone was the of at least 2 days in a CO2/N2 atmosphere with less than 0.1% resid-
most efcient. Using the same substrates of mitochondria and car- ual O2 in the head space is required to obtain a purple colour with
diac tissue, the MRA also decreased at 4 days storage, but to a the myoglobin predominantly in the form of DMB. This require-
smaller extent than the OCR (Tang, Faustman, Mancini, Seyfert, & ment is valid for all types of ground beef tested in this study,
Hunt, 2005a). The MRA of beef muscles was only marginally re- including fresh, frozen/thawed, salted and unsalted meat. The rule
duced at 7 days storage, and grinding did not alter the MRA (Madh- applies for any 2 day period during storage, except when the en-
avi & Carpenter, 1993). These data indicate that MRA is lost very zyme systems OCR and MRA are severely depleted. Another excep-
slowly prior to and during processing of fresh ground beef. In this tion from the general rule is under circumstances where a large
system, OCR is likely to be more important than MRA, because the fraction of MMB has been formed under highly oxidizing condi-
OCR is increased temporarily by grinding, and is rapidly reduced tions, at which a full reduction back to DMB can be difcult to
during the rst 24 days post mortem. In low O2 packaging sys- achieve. Furthermore, if the amount of O2 transported into the
tems, efforts should be made to use and maintain raw materials package is higher than what is consumed by the meat, the colour
with a high OCR, ensuring a rapid reduction to the purple pigment will deteriorate.
form DMB. Packaging of ground beef in low O2 is a very dynamic system,
In the present study, the gas to meat ratio of part A was approx- where the O2 consumption capacity of the meat itself is a more
imately 2.5 times higher than in part B. On the other hand, the ini- important factor than external factors related to the packaging.
tial level of residual O2 was almost double as high in part B as in Our results are in disagreement with the established rule of a max-
part A, 0.90% versus 0.55%. These external factors contributed to imum of 0.050.15% initial O2 to avoid discolouration of beef (Gill
the total amount of O2 in the packages and affected the results of & McGinnis, 1995a; Mancini & Hunt, 2005; Penney & Bell, 1993).
the changes in residual O2 of the headspace, but the main factor Provided that sufcient O2 consumption capacity is present in
was still the age of the meat post mortem and the ability of the the ground beef, initial O2 concentrations of 0.51.5% can be
ground beef to consume O2. In optimising low O2 packaging it is acceptable. We hypothesize that the large surface of the meat ob-
benecial to lower the gas to meat ratio as much as possible with- tained by grinding facilitates the enzymatic reactions for rapid re-
out compromising the antimicrobiological effect of CO2 on spoilage moval of O2. In contrast to ground meat, for whole muscle meat the
(Jakobsen & Bertelsen, 2002), thereby reducing the amount of internal O2 consumption seems to be of minor importance and
 O. Srheim et al. / Meat Science 81 (2009) 467473
external factors must contribute to the removal of O2 (Beggan
et al., 2006). The present study demonstrated that with knowledge
of raw material quality, processing and packaging conditions, it is
possible to produce ground beef in low O2 atmospheres with a pre-
dominantly purple colour of DMB. The main advices to the industry
for a successful application of the low O2 system are to utilize fresh
raw materials shortly after slaughter, avoid addition of NaCl, de-
crease headspace volumes and reduce initial levels of residual of
O2 in packages. Furthermore, the exposure of the meat to O2 during
handling before packaging should be minimized (Kropf et al.,
1985).
The concept of low O2 packaging for ground beef is currently
used by the Norwegian meat industry, and low O2 packages are
generally well perceived in the domestic market where meat in
high O2 packages is not sold. In markets in other countries where
both low and high O2 ground beef packages would be available,
the rst choice of the consumers based on colour is likely to be
high O2. However, low O2 packaging in CO2/N2 atmospheres has
many quality and safety benets compared to high O2 (Mancini
& Hunt, 2005; Srheim, 2006). Informing and educating the con-
sumers to understand and accept the different colours and forms
of myoglobin in low O2 packaging systems at retail display should
be an aim for processors and distributors of meat. A better scien-
tic knowledge of the consumer choices of the colour of meat at
the point of purchase is needed.
4. Conclusions
In order to present ground beef in low O2 atmospheres of CO2/
N2 with a predominantly purple colour, a rapid removal of residual
O2 by the meat itself from the headspace is crucial. Fresh raw
materials had a higher rate of O2 consumption than frozen/thawed
raw materials. Moreover, fresh raw materials obtained at 2 days
post mortem consumed O2 much faster than at 7 days post mor-
tem. Addition of 1% NaCl to ground beef decreased the O2 con-
sumption rate considerably and caused discolouration.
Acknowledgements
The authors are very grateful to Hans-Arne Rnningen and
Bjrn Vidar Bjnnes at Nortura in Tnsberg, Norway, for their assis-
tance in the industrial experiment. Aud Espedal, Karin Solgaard
and Hans Sundell, all at Matforsk AS Noma Food, are thanked
for excellent technical assistance in the study.
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