ARTICLE IN PRESS
Radiation Physics and Chemistry 71 (2004) 149–154
Effects of ascorbic acid and antioxidants on color, lipid
oxidation and volatiles of irradiated ground beef
D.U. Ahn*, K.C. Nam
Animal Science Department, Iowa State University, 2276 Kildee, Ames, IA 50011-3150, USA
Abstract
Beef loins with 3 different aging times after slaughter were ground, added with none, 0.1% ascorbic acid, 0.01%
sesamol+0.01% a-tocopherol, or 0.1% ascorbic acid+0.01% sesamol+0.01% tocopherol. The meats were packaged
in oxygen-permeable bags, irradiated at 2.5 kGy, and color, oxidation–reduction potential (ORP), lipid oxidation and
volatile profiles were determined. Irradiation decreased the redness of ground beef, and visible color of beef changed
from a bright red to a green/brown depending on the age of meat. Addition of ascorbic acid prevented color changes in
irradiated beef, and the effect of ascorbic acid became greater as the age of meat or storage time after irradiation
increased. The ground beef added with ascorbic acid had lower ORP than control, and the low ORP of meat helped
maintaining the heme pigments in reduced form. During aerobic storage, S-volatiles disappeared while volatile
aldehydes significantly increased in irradiated beef. Addition of ascorbic acid at 0.1% or sesamol+a-tocopherol at each
0.01% level to ground beef prior to irradiation were effective in reducing lipid oxidation and S-volatiles. As storage time
increased, however, the antioxidant effect of sesamol+tocopherol in irradiated ground beef was superior to that of
ascorbic acid.
r 2004 Elsevier Ltd. All rights reserved.
Keywords: Irradiated ground beef; Color and volatiles; Ascorbate; Antioxidants
1. Introduction
Ground beef comprises over 40% of beef consumption in the US (AMI, 1998), and is the most susceptible
form of meat to microbial contamination during
processing and handling. Therefore, prevention of
pathogens from ground beef is the most demanding.
Irradiation is the most effective technology in controlling pathogenic microorganisms in ground beef, but can
influence color, lipid oxidation and odor of beef
significantly.
Meat color is a prime quality parameter that
determines the consumer acceptance of meat. Liu et al.
(1995) indicated that the loss of value due to discolora*Corresponding author. Tel.: +1-515-294-6595; fax: +1515-294-9143.
E-mail address: duahn@iastate.edu (D.U. Ahn).
tion in beef at the retail level in the US could be over 700
million dollars per year. The color changes induced by
irradiation are different depending on animal species,
muscle type, irradiation dose, and packaging type (Ahn
et al., 1998). In general, light meat such as pork loin and
poultry breast meat produced pink color, while dark
meat such as beef became brown or gray after
irradiation (Millar et al., 1995; Nanke et al., 1998;
Kim et al., 2002a). The pink color compounds in
irradiated light meat was characterized as a carbon
monoxide-heme pigment complex (Nam and Ahn,
2002a, b), but the mechanisms and cause of color
changes in irradiated beef is not known yet.
The major volatile compounds responsible for offodor in irradiated meats are mainly sulfur compounds
(Ahn et al., 1999, 2000, 2001). The volatile sulfur
compounds were produced from the radiolytic degradation of the side chains of sulfur-containing amino acids,
0969-806X/$ - see front matter r 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.radphyschem.2004.04.012
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methionine and cysteine (Ahn, 2002; Ahn and Lee,
2002). Unlike popular belief, ground beef oxidized faster
than ground pork or poultry (Nam et al., 2001; Kim
et al., 2002a). Despite the intrinsic antioxidant activities
in fresh meat, irradiation accelerated lipid oxidation in
raw pork and beef patties under aerobic conditions (Ahn
et al., 1998; Kim et al., 2002b).
Ascorbic acid is a reducing agent, which inhibits
myoglobin oxidation and brown color development in
nonirradiated beef (Sanchez-Escalante et al., 2001). The
combinations of phenolic antioxidants such as gallate,
sesamol, and tocopherol, were effective in reducing the
oxidative reactions and the production of sulfur volatiles
in irradiated pork by scavenging free radicals produced
by irradiation (Nam and Ahn, 2003).
The objective of this study was to determine the effect
of ascorbic acid and selected antioxidants on the color
and off-odor volatiles of beef with different postmortem
aging time before irradiation and storage time after
irradiation.
2. Materials and methods
2.1. Sample preparation
Beef loins (Longissimus dorsi) with 3 different aging
times after slaughter were used. The freshest loins were
obtained from 4 animals 2 d after slaughter. One group
of the loins purchased 2 week before sample preparation
was further aged at 4 C and the other group was
purchased 1 d before preparation. For convenience, the
three loins were named ‘‘pre-aged’’, ‘‘aged’’, and ‘‘longterm-aged’’, respectively. Each meat block was ground
separately through a 3-mm plate. Five treatments were
prepared: (1) nonirradiated control, (2) irradiated
control, (3) 0.1% (w/w) l-ascorbic acid-added and
irradiated, (4) 0.01% sesamol+0.01% a-tocopheroladded and irradiated, and (5) 0.1% ascorbic
acid+0.01% sesamol+0.01% tocopherol-added and
irradiated. Each additive was added to the ground beef
and then mixed for 1 min in a bowl mixer. Ground beef
was individually packaged in oxygen-permeable bags
(polyethylene), stored at 4 C overnight, and irradiated
next day morning.
2.2. Ionizing radiation
The aerobically packaged ground beef were irradiated
at 2.5 kGy using a Linear Accelerator Facility with
10 MeV energy and 10.2 kW power level. After irradiation, the irradiated and nonirradiated meat samples were
immediately returned to a 4 C cold room and stored for
7 d. Color, ORP values, lipid oxidation and volatile
profiles of the samples were determined on 1, 4, and 7 d
of storage.
2.3. Chemical analyses
CIE color values were measured on the surface of
meat samples using a LabScan colorimeter. Oxidationreduction potential was measured using a pH/ion meter
equipped with a platinum electrode. Lipid oxidation was
determined using a TBARS method (Ahn et al., 1999).
Volatiles of samples were analyzed using a Solatek 72
Multimatrix-Vial Autosampler/Sample Concentrator
3100 connected to a GC/MS according to the method
of Ahn et al. (2001).
3. Results and discussion
3.1. Color values
Color L value increased as the aging time of beef
increased. During storage after irradiation, L values of
ground beef also showed an increasing trend as the
storage time increased, and the increase in L value was
more apparent in meat from ‘‘long-term-aged’’ beef than
other ones. Irradiation did not influence the L values of
beef from all stages of aging. Addition of ascorbic acid
and/or sesamol+tocopherol had no effect on the L
values of irradiated ground beef. Irradiation reduced the
redness (a value) of ground beef significantly, but with
varying degree depending on aging time (Table 1).
Immediately after irradiation, the color of ground beef
changed from a bright red to a greenish brown, which
would be unattractive beef color for consumers. The
color of irradiated beef was totally different from that of
irradiated pork or poultry breast, which was pink or red.
Nam and Ahn (2002a) reported that the complex of
heme pigments with carbon monoxide produced by
irradiation was responsible for the increased redness in
irradiated turkey breast. The formation of CO-heme
complex, however, could not explain the color changes
in beef after irradiation because, while the production of
carbon monoxide in beef by irradiation was similar to
those of light meats (Kim et al., 2002a), the pigment
content in beef is >10-fold higher than that in light
meats. Thus, the contribution of CO-heme pigment to
the color of ground beef was much smaller than that of
light meats.
Ascorbic acid incorporated to beef at the level of
0.1% (w/w) was very effective in maintaining redness (a
values) of irradiated ground beef. Satterlee et al. (1971)
reported that the formation of red, MbO2-like pigment
formed from MbFe3+ was greatest in a nitrogen
atmosphere, slightly inhibited in air and greatly inhibited in an oxygen atmosphere. Oxygen is an effective
scavenger of aqueous electrons (e
aq). Therefore, in the
absence of oxygen, a reducing environment is established in the irradiated meat, which converts MbFe3+ to
MbFe2+ (Giddings and Markakis, 1972). Addition of
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151
Table 1
CIE color a values of irradiated ground beef treated with different additives during aerobic storage at 4 C
Storage
Nonir
Irradiated
Control
Control
Ascorbic1
S+E2
A+S+E3
SEM
Pre-aged
Day 1
Day 4
Day 7
SEM
22.0ax
20.1cy
20.1cy
0.4
17.4bx
17.0ex
14.8ey
0.3
21.3ay
24.5ax
25.6ax
0.4
17.4by
18.6dx
16.6dy
0.3
21.0a
22.3b
22.3b
0.4
0.3
0.4
0.4
Aged
Day 1
Day 4
Day 7
SEM
19.7bx
19.4cx
15.4dy
0.3
17.3cx
16.9dx
15.3dy
0.3
22.7ay
25.9ax
26.1ax
0.4
19.4b
18.4c
18.2c
0.4
23.2a
23.3b
22.8b
0.4
0.3
0.4
0.4
Long-term-aged
Day 1
Day 4
Day 7
SEM
19.8ax
8.1ey
8.4ey
0.2
17.6bx
12.5dy
11.9dy
0.3
19.0ay
23.0ax
23.2ax
0.4
14.7cy
15.7cxy
16.2cx
0.4
17.2by
19.7bx
20.0bx
0.3
0.3
0.3
0.3
SEM: standard error of the mean.
1
Ascorbic acid 0.1%; 2Sesamol 100 ppm+a-tocopherol 100 ppm; 3Ascorbic acid 0.1%+sesamol 100 ppm+a-tocopherol 100 ppm.
n ¼ 4:
a–d
Values with different letters within a row are significantly different (Po0:05).
x–z
Values with different letters within a column of the same sample are significantly different (Po0:05).
ascorbate further increased the reducing power in beef
and increased the red color intensity of ground beef. On
the other hand, sesamol + tocopherol had no effect in
preventing color changes, and did not show any
synergistic effect between ascorbic acid and sesamol +
tocopherol in ground beef by irradiation.
The a values of ‘‘pre-aged’’ beef was not changed
much during the storage, and the redness was higher in
nonirradiated than irradiated beef. ‘‘Long-term-aged’’
beef, however, showed drastic decreases in a values
during storage and nonirradiated ground beef had lower
a values than irradiated beef. Therefore, in ‘‘long-termaged’’ ground beef, the color of irradiated meat looked
better than nonirradiated meat during storage. This
difference in color between fresh and old meats could be
related to the loss of reducing power in old meat (‘‘longterm-aged’’).
Ascorbic acid increased the a values of irradiated
ground beef and the color stabilizing effects of ascorbic
acid was more distinct in ‘‘long-term-aged’’ than in ‘‘preaged’’ irradiated ground beef. Only the ground beef
added with ascorbic acid produced higher a values than
the meat with ascorbate+sesamol+tocopherol. Thus,
the use of ascorbic acid was more effective in stabilizing
irradiated beef color than using it with other antioxidants. However, addition of strong antioxidants along
with ascorbic acid would be more beneficial in control-
ling lipid oxidation in irradiated ground beef during
storage.
The addition of ascorbic acid with or without sesamol
+ tocopherol significantly lowered the ORP values of
irradiated ground beef regardless of the age of meat. The
lowered ORP values by ascorbic acid maintained heme
pigments in ferrous status and stabilized the color of
irradiated ground beef. With increased storage time after
irradiation, ORP values of meat increased steadily in all
treatments but ascorbic acid-added ground beef still
maintained lower values than others over the storage
time.
3.2. Lipid oxidation of irradiated beef
Irradiation increased TBARS values of ‘‘pre-aged’’
and ‘‘aged’’ ground beef but the difference between
irradiated and nonirradiated ‘‘long-term-aged’’ beef was
small (Table 2). Both ascorbic acid (0.01%, w/w) and
sesamol+a-tocopherol combination (100 ppm each)
showed significant antioxidant activities in irradiated
ground beef. As the storage time increased overall lipid
oxidation increased, and the rate of lipid oxidation was
faster in irradiated than nonirradiated beef. The effect of
antioxidants in ground beef was more distinct after 7 d
of storage than at Day 0. TBARS of irradiated ground
beef added with ascorbic acid was 40% lower than that
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152
Table 2
TBARS values of irradiated ground beef treated with different additives during aerobic storage at 4 C
Storage
Nonir
Irradiated
Control
Control
Ascorbic1
S+E2
A+S+E3
SEM
Pre-aged
Day 1
Day 4
Day 7
SEM
0.44bz
0.66by
0.88bx
0.05
0.58az
0.96ay
1.90ax
0.10
0.28cy
0.29cy
0.39cx
0.02
0.20c
0.17d
0.18c
0.01
0.23c
0.23cd
0.27c
0.02
0.03
0.02
0.08
Aged
Day 1
Day 4
Day 7
SEM
0.65by
0.91by
1.94bx
0.18
1.27az
1.79ay
2.81ax
0.08
0.44cy
0.57cy
0.76cx
0.05
0.35c
0.36d
0.31c
0.02
0.33c
0.41cd
0.37c
0.03
0.05
0.05
0.14
Long-term-aged
Day 1
Day 4
Day 7
SEM
4.13ay
5.05ay
6.87ax
0.42
4.40ay
4.54ay
7.23ax
0.14
1.15by
1.42by
2.85bx
0.12
0.81bz
0.93by
1.06cx
0.03
0.81bz
0.92by
1.07cx
0.02
0.11
0.30
0.17
SEM: standard error of the mean.
1
Ascorbic acid 0.1%; 2Sesamol 100 ppm+a-tocopherol 100 ppm; 3Ascorbic acid 0.1%+sesamol 100 ppm+a-tocopherol 100 ppm.
n ¼ 4:
a–c
Values with different letters within a row are significantly different (Po0:05).
x–z
Values with different letters within a column of the meat are significantly different (Po0:05).
of irradiated control, but sesamol+tocopherol had
stronger antioxidant effect than ascorbic acid. The
incorporation of ascorbic acid prevented color changes
while sesamol+a-tocopherol showed a very strong
antioxidant effect in irradiated beef during storage. This
suggested that the combined use of these additives could
prevent color changes and lipid oxidation in ‘‘long-termaged’’ irradiated ground beef during storage.
3.3. Volatiles of irradiated beef
Irradiation increased the amounts of sulfur compounds (Fig. 1). The S-volatiles newly generated or
greatly increased by irradiation were ethanethioic acid Smethyl ester, dimethyl disulfide, and dimethyl trisulfide.
Ahn et al. (2000) reported that S-containing volatiles
were highly dependent upon irradiation dose and the
off-odor in irradiated pork was produced by the
compounding effects of volatiles from lipid oxidation
and radiolytic degradation of various amino acid side
chains. Both ascorbic acid and sesamol+tocopherol
lowered the amounts of dimethyl disulfide in irradiated
ground beef. Aging time of beef was an important factor
influencing volatile production by irradiation. Irradiation of ‘‘long-term-aged’’ ground beef produced greater
amounts of total and S-volatiles than ‘‘pre-aged’’ and
‘‘aged’’ beef. This could be related to more severe
structural disintegration in ‘‘long-term-aged’’ than ‘‘preaged’’ and ‘‘aged’’ beef, and the structural damage
should have made the meat susceptible to the attacks of
free radicals produced by irradiation.
When irradiated ground beef were stored for 7 d
under aerobic conditions, the profiles of volatile
compounds were totally different from those at day 1.
Almost all volatile compounds produced in ground beef
after 7-d storage under aerobic conditions were lipid
oxidation-related products such as hydrocarbons and
volatile carbonyl compounds. Ketones such as 2propanone, 2-butanone, and 2,3-butadione were the
predominant compounds in ground beef after 7-d
storage, irrespective of irradiation. Hexanal, a good
indicator of lipid oxidation, was the most predominant
aldehyde compound and was significantly detected at
even ‘‘pre-aged’’ beef at day 7. As aging time before
irradiation increased, many more volatile aldehydes
(propanal, pentanal, hexanal, and heptanal) were found
and their amounts also increased. As storage time after
irradiation increased, considerable amounts of ethanol
were produced in ‘‘aged’’ and ‘‘long-term-aged’’ nonirradiated beef, which could be attributed to microbial
growth. The S-volatiles predominant immediately after
irradiation were not found in irradiated ground beef
after 7 d of aerobic storage. Although aerobic packaging
was very effective in eliminating the S-volatiles produced
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D.U. Ahn, K.C. Nam / Radiation Physics and Chemistry 71 (2004) 149–154
the heme pigments of beef red. The S-volatiles produced
by irradiation had characteristic odor, but the intensity
of irradiation off-odor in ground beef diminished over
storage period because S-volatiles disappeared during
aerobic storage. As storage time increased, ‘‘long-termaged’’ irradiated ground beef developed severe lipid
oxidation unless antioxidant was added. Sesamol+tocopherol was highly effective in reducing lipid oxidation,
and ascorbic acid stabilized color of irradiated beef.
Therefore, the combined use of ascorbic acid and
sesamol+tocopherol was recommended to control
overall quality changes in irradiated ground beef during
storage.
2.E+08
Total ion counts
a
1.E+08
Sulfur-volatiles
b
c
5.E+07
d
0.E+00
0
3
6
a
Aldehydes
3.E+07
Total ion counts
153
References
2.E+07
b
a
1.E+07
b
c
c
0.E+00
0
3
d
6
Storage time (d)
Fig. 1. Changes of the amounts of sulfur-volatiles and
aldehydes of ‘‘aged’’ ground beef treated with different
additives during the aerobic storage at 4 C. (K) Nonirradiated
control; (J) irradiated control; (’) irradiated ascorbic acidadded; (&) Irradiated sesamol+tocopherol-added; (~) irradiated ascorbic acid+sesamol+tocopherol-added. (a–d) Different letters within a storage time shows that the means are
significantly different (Po0:05). n ¼ 4:
by irradiation, the amounts of volatile aldehydes in
irradiated ground beef significantly increased during
storage unless antioxidant additives were added.
Addition of antioxidant was very effective in inhibiting not only a few hydrocarbons but volatile aldehydes
also in irradiated beef at day 7. Especially, volatile
aldehydes were not detected in ground beef incorporated
with sesamol+tocopherol, while ascorbic acid produced
some aldehydes. Therefore, when irradiated beef is
aerobically stored, the generation of lipid oxidation
products is of more concern than S-volatiles.
4. Conclusion
As in nonirradiated beef, addition of ascorbic acid at
0.1% (w/w) to ground beef prior to irradiation stabilized
the color of ground beef during aerobic storage. The
color stabilizing effect of ascorbic acid was derived from
the reducing power of ascorbic acid, which maintained
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