Addition of garlic or onion before irradiation on lipid oxidation,... characteristics of cooked ground beef

Meat Science 88 (2011) 286–291
Contents lists available at ScienceDirect
Meat Science
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / m e a t s c i
Addition of garlic or onion before irradiation on lipid oxidation, volatiles and sensory
characteristics of cooked ground beef
Han Sul Yang a, Eun Joo Lee a,c, Sun Hee Moon a,b, Hyun Dong Paik a,b, Dong U. Ahn a,c,⁎
a
b
c
Department of Animal Science, Iowa State University, Ames, IA 50011-3150, USA
Department of Food Science and Biotechnology of Animal Resources, Konkuk University, Seoul 143-701, Republic of Korea
Department of Agricultural Biotechnology, Major in Biomodulation, Seoul National University, Seoul 151-921, Republic of Korea
a r t i c l e
i n f o
Article history:
Received 17 September 2010
Received in revised form 17 December 2010
Accepted 9 January 2011
Keywords:
Cooked ground beef
Irradiation
Garlic and onion
Lipid oxidation
Odor and flavor
a b s t r a c t
Addition of 0.5% onion was effective in reducing lipid oxidation in irradiated cooked ground beef after 7 day
storage. Addition of garlic or onion greatly increased the amounts of sulfur volatiles from cooked ground beef.
Irradiation and storage both changed the amounts and compositions of sulfur compounds in both garlic- and
onion-added cooked ground beef significantly. Although, addition of garlic and onion produced large amounts
of sulfur compounds, the intensity of irradiation odor and irradiation flavor in irradiated cooked ground beef
was similar to that of the nonirradiated control. Addition of garlic (0.1%) or onion (0.5%) to ground beef
produced a garlic/onion aroma and flavor after cooking, and the intensity was stronger with 0.1% garlic than
0.5% onion treatment. Considering the sensory results and the amounts of sulfur compounds produced in
cooked ground beef with added garlic or onion, 0.5% of onion or less than 0.1% of garlic is recommended to
mask or change irradiation off-odor and off-flavor.
© 2011 Elsevier Ltd. All rights reserved.
1. Introduction
Irradiation has been approved for use in beef since 2000 and is the
best known method in controlling pathogens in raw ground beef.
However, the amount of irradiated beef sold in the U.S. is less than 1%
of total beef consumption because irradiation of meat changes quality,
which negatively influences consumer acceptance (Lee, Love, & Ahn,
2003). Huskey (1997) reported that both safety (84%) and taste (83%)
of meat are very important for the meat industry and consumers.
Although consumer surveys and market analysis indicated that about
70% of consumers were willing to pay a premium price for irradiated
chicken breast (Hayes, Shogren, Fox, & Kliebenstein, 1995), the major
concerns in irradiating meat are its effect on meat quality. The primary
changes in irradiated meat are mainly related to the generation of offodor, color change, and lipid oxidation. Color and odor of meat at the
time of opening packaging bag, and subsequent cooking and eating
determine whether consumers will purchase the meat again next
time.
Irradiated meat, regardless of packaging methods, produced more
volatiles than non-irradiated ones and developed a characteristic
aroma (Ahn, Olson, Jo, et al., 1998). Sulfur compounds produced by
irradiation are responsible for irradiation off-odor (Jo, Lee, & Ahn,
1999). Volatile sulfur compounds can be produced in two different
ways: one is a direct radiolytic cleavage of the side chains of sulfur
⁎ Corresponding author. Department of Animal Science, Iowa State University, Ames,
IA 50011-3150, USA. Tel.: +1 515 294 6595; fax: +1 515 294 9143.
E-mail address: duahn@iastate.edu (D.U. Ahn).
0309-1740/$ – see front matter © 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.meatsci.2011.01.002
containing amino acids such as methionine and cysteine (Ahn, 2002),
and the other is by secondary reactions of primary sulfur compounds
with surrounding compounds (Jo & Ahn, 2000). Significant amino
acid–lipid interactions are also involved (Ahn, Nam, Du, & Jo, 2001).
Among the sulfur compounds, dimethyl sulfide, dimethyl disulfide
and dimethyl trisulfide were the most prominent sulfur compounds
produced by irradiation and are responsible for irradiation off-odor in
meat (Ahn et al., 1997; Ahn, Olson, Lee, et al., 1998). The perception of
odor from samples containing sulfur volatiles is changed somewhat
depending on the composition of other volatiles in the sample, but the
roles of nonsulfur compounds to the overall odor characteristics of
irradiated liposomes prepared with phosphatidyl choline, phosphatidic acid, amino acid homopolymers were minor (Ahn & Lee, 2002).
Irradiation is expected to accelerate oxidative changes in meat
significantly, but increases TBARS only in aerobically packaged raw
meat (Ahn et al., 1997). Exposure to oxygen after cooking was the
most important factor in oxidative changes of cooked pork, and
hexanal concentrations represented the lipid oxidation status of
cooked meat better than any other volatile components (Ahn et al.,
1997; Ahn, Olson, Lee, et al., 1998). Dietary vitamin E at N200 IU/kg
feed decreased lipid oxidation and reduced total volatiles of raw
turkey meat, but has not been shown to be effective in cooked turkey
meat stored under aerobic conditions (Ahn, Kawamoto, Wolfe, & Sim,
1995). The addition of tocopherol + gallate and tocopherol + sesamol
is highly effective in reducing lipid oxidation and off-odor volatiles in
irradiated cooked turkey and pork patties (Nam & Ahn, 2003b), but
has only minor effects on the production of sulfur compounds and
off-odor intensity (Nam & Ahn, 2003a).
H.S. Yang et al. / Meat Science 88 (2011) 286–291
Sensory analyses of irradiated pork indicated that approximately
70% of sensory panels characterized irradiation odor as “barbecuedcorn-like” odor (Ahn, Jo, Du, Olson, & Nam, 2000; Ahn, Jo, & Olson,
2000; Nam, Ahn, Du, & Jo, 2001). Sulfury odor in ready-to-eat (RTE)
turkey hams increases as irradiation dose increases, and the contents
of sulfur compounds in irradiated hams are higher than those in
nonirradiated samples. Irradiation increases the production of
acetaldehyde, which could be related to a “metal-like” flavor in
irradiated hams (Zhu, Lee, Mendonca, & Ahn, 2004). Masking or
preventing off-odor/off-flavor production in irradiated meat is among
the most critical factors for consumer acceptance of irradiated ground
beef. Garlic (Allium sativum L.) and onion (Allium cepa L.) are two
major food ingredients widely used in cookery to complement and
enhance the flavor of meat products (Tang & Cronin, 2007). Garlic and
onion both produce many sulfur compounds, which provide their
unique flavor and odor. Therefore, addition of garlic or onion may
change, mask, or improve the odor/flavor characteristics of irradiated
cooked meat. Nonfluid seasonings such as garlic and onion are
permitted for use in irradiated ground meat and meat byproducts
(Electronic Code of Federal Regulation, 2009). Extensive work has
been done to determine irradiation effects on raw meat quality, but
little information on the quality changes or improvement for
irradiated cooked meat is available.
The objective of this study was to determine the effect of garlic and
onion on lipid oxidation volatile profiles, and masking or preventing
off-odor/off-flavor in irradiated cooked ground beef.
2. Materials and methods
2.1. Sample preparation
Eight beef top rounds from different steers were obtained from a
local packing plant 6 days post-slaughter. The animals were 27 month
old steers finished on a ration containing grain, by-products, and hay for
4 months. Two rounds from different steers were pooled and treated as
a replication. Each round was trimmed of any visible fat and connective
tissues. All the muscles from the two rounds were pooled and ground
together through a 3-mm plate twice, and used. Six different treatments
were prepared: 1) non-irradiated control, 2) irradiated control, 3)
non-irradiated added with 0.1% garlic (wt/wt), 4) irradiated added with
0.1% garlic, 5) non-irradiated added with 0.5% onion, and 6) irradiated
added with 0.5% onion. Skinned fresh garlic and onion were purchased
from a local supermarket, ground until they became a semi-liquid form
using a Kitchen Aid food processor (Model KSM 90; Kitchen Aid Inc., St.
Joseph, Mich., USA) immediately before use in a fabrication room of
meat laboratory (4 °C). The entire homogenate of garlic and onion was
used, and the amount of garlic and onion treatments was selected on the
basis of our preliminary study to prevent excessive garlic and onion odor
in ground beef. Each additive was added to the ground meat and then
mixed for 1 min in a bowl mixer (Model KSM 90; Kitchen Aid Inc.,
St. Joseph, Mich., USA). Ground beef patties (approximately 60 g) were
made by hand, packaged individually in oxygen-impermeable bags
(O2 permeability, 9.3 mL O2/m2/24 h at 0 °C), stored at 4 °C overnight,
and irradiated the next day morning. Only four treatments (nonirradiated control, irradiated control, irradiated added with 0.1% garlic,
and irradiated added with 0.5% onion) were used for sensory analysis.
2.2. Ionizing radiation and cooking
The packaged ground beef patties were irradiated at 0 or 2.5 kGy
using a linear accelerator facility (Circe IllR; Thomson CSF Linac, St.
Aubin, France) with 10 MeV energy and 5.6 kW power level. The
average dose rate was 74.1 kGy/min. Alanine dosimeters were placed
on the top and bottom surfaces of a sample and were read using a 104
Electron Paramagnetic Resonance Instrument (Bruker Instruments
Inc., Billerica, MS, USA) to check the absorbed dose. The Max/Min ratio
287
was 1.16. The non-irradiated control (0 kGy) samples were exposed
to an ambient temperature of linear accelerator facility while other
samples were irradiated.
After irradiation, 12 patties per treatment (3 storage times × 4
replications) of the patties were cooked in a 90 °C water bath
(Isotemp®, Fisher Scientific Inc., Pittsburgh, PA, USA) until the
internal temperature of the patties reached 75 °C. After cooling to
room temperature, patties were removed from the cooking bags and
re-packaged in oxygen-permeable bags (polyethylene, 10 × 15 cm, 2
mil, Assoc. Bag Co.), stored for 7 days at 4 °C, and used for TBARS and
volatile analyses. The rest of the patties were cooked in an electric
oven at 175 °C to an internal temperature of 75 °C and used for
sensory analysis. Internal temperatures of meat patties during
cooking were monitored with thermocouples connected to digital
read-out devices. All the cooked meat patties were vacuum-packaged
immediately after cooking to minimize oxidative changes during
storage and handling before the sensory test. The cooked meats were
used for the sensory test without storage.
2.3. 2-Thiobarbituric acid-reactive substance (TBARS)
Lipid oxidation was determined using a TBARS method (Ahn, Olson,
Jo, et al., 1998). The meat sample (5 g) was placed in a 50-mL test tube
and homogenized with 15 mL deionized distilled water for 15 s at high
speed (Type PT 10/35; Brinkman Instrument Inc., Westbury, NY, USA).
The meat homogenate (1 mL) was transferred to a disposable test tube,
and butylated hydroxytoluene (7.2%, 50 μL) and thiobarbituric acid
(TBA)/trichloroacetic acid (TCA) solution (2 mL) were added. The
sample was mixed using a vortex mixer, and then incubated in a 90 °C
water bath for 15 min to develop color. After cooling, the samples were
centrifuged at 3000 ×g for 15 min at 5 °C. The absorbance of the
resulting upper layer was read at 531 nm against a blank prepared with
1 mL deionized distilled water and 2 mL TBA/TCA solution. The amounts
of TBARS were expressed as mg of malondialdehyde (MDA) per kg of
meat.
2.4. Volatile compounds
A purge-and-trap apparatus (Solatek 72 and Concentrator 3100;
Tekmar-Dohrmann, Cincinnati, OH, USA) connected to a gas chromatograph/mass spectrometer (HP 6890/HP 5973; Hewlett-Packard Co.,
Wilmington, DE, USA) was used to analyze volatiles produced. The
meat sample (2 g) was placed in a 40-mL sample vial, and the vial was
flushed with helium gas (40 psi) for 5 s to minimize oxygen content in the
vial. The sample was purged with helium gas (40 mL/min) for 14 min at
40 °C. Volatiles were trapped using a Tenax–charcoal–silica column
(Tekmar-Dohrmann) and desorbed for 2 min at 225 °C, focused in a
cryofocusing module (−80 °C), and then thermally desorbed into a
capillary column for 60 s at 225 °C.
An HP-624 column (15 m×0.25 mm i.d., 1.4 μm nominal), an HP-1
column (60 m×0.25 mm i.d., 0.25 μm nominal; Hewlett-Packard), and an
HP-Wax column (15 m×0.25 mm i.d., 0.25 μm nominal) were connected
using zero dead-volume column connectors (J & W Scientific, Folsom, CA,
USA). Ramped oven temperature was used to improve volatile separation.
An initial oven temperature of 30 °C was held for 6 min. After that, the
oven temperature was increased to 60 °C at 5 °C/min, increased to 180 °C
at 20 °C/min, increased to 210 °C at 15 °C/min, and then was held for
5 min at the temperature. Constant column pressure at 22.5 psi was
maintained. The ionization potential of the mass-selective detector
(Model 5973; Hewlett-Packard) was 70 eV, and the scan range was
19.1–400 m/z. Identification of volatiles was achieved by comparing the
mass spectral data of samples with those of the Wiley Library (HewlettPackard). Standards were used to confirm the identification by the
mass-selective detector. The area of each peak was integrated using the
ChemStation (Hewlett-Packard), and the total peak area (pA* s) was
reported as an indicator of volatiles generated from the sample.
288
H.S. Yang et al. / Meat Science 88 (2011) 286–291
2.5. Sensory training and evaluation
Ten panelists were recruited and trained in 3 training sessions. Ten
panelists were screened from potential panelists (total 16 panelists)
using basic taste identification tests. Panelists were given samples
representing anchor points for each attribute, and training sessions using
non-irradiated control and 1.25, 2.5, and 4.5 kGy irradiated samples
produced in the meat lab. The panelists were trained using a 5-point scale
(“5 extremely intense” and “1 slightly intense”) for irradiation aroma,
ground beef aroma, garlic/onion aroma, irradiation flavor, ground beef
flavor, and garlic/onion flavor. The final anchor point ratings were
decided upon by the training panel after initial evaluation and discussion.
They were trained with cooked ground beef patty products for 2 weeks
with the product characteristics to be evaluated.
For the samples, panelists evaluated irradiation aroma/flavor, ground
beef aroma/flavor and garlic/onion aroma/flavor using a 15-point hedonic
scale as described by Meilgaard, Civille, and Carr (1999), where one (1)
was “no aroma/flavor” and fifteen (15) was “strong aroma/flavor.” Cooked
samples were cut and placed in glass containers (Pyrex, Charleroi, PA)
with a plastic cover while they were still hot and tested immediately.
Panelists evaluated samples in isolated booths fitted with a breadbox
server and red incandescent lighting to make color differences.
2.6. Statistical analysis
Data was analyzed by the procedures of the generalized linear
model (GLM) of SAS (2000). The SNK (Student–Newman–Keuls)
multiple-range test was used to compare the mean values of
treatments. Mean values and standard error of the means (SEM)
were reported. Differences in sensory values were compared using
Tukey's significant differences. For sensory data, mean values and
standard deviations were reported. Statistical significance for all
comparisons was made at P b 0.05.
irradiated samples (Table 1). Griffiths, Trueman, Crowther, Thomas,
and Smith (2002) reported that among vegetables and fruits, onion
contains the highest amount of quercetin, a phenolic antioxidant
(Hertog, Hollman, & Katan, 1992). Over the 7 day storage period, the
TBARS of cooked ground beef increased by about 3 times from 0 day
values in all treatments. Irradiation is reported to accelerate lipid
oxidation of meat under aerobic conditions and oxygen availability
during storage was important than irradiation on the lipid oxidation of
raw and cooked meat (Ahn, Olson, Jo, Love, & Jin, 1999), but little
differences in TBARS values were found between irradiated and
nonirradiated cooked ground beef after 7 day storage under aerobic
conditions.
3.2. Volatiles
Among the volatiles, only the amounts of aldehydes showed
difference by additive treatments in non-irradiated cooked ground
beef (Table 2). Irradiation had minor effects on the production of
alcohols at Day 0, but irradiated cooked ground beef with garlic or
onion produced less amounts of alcohols after 3 day storage. The
amounts of aldehydes in cooked ground beef increased during
storage, but irradiation had little effect except for nonirradiated
cooked ground beef at Day 0 when 0.1% garlic- or 0.5% onion-added
ground beef produced more aldehydes than control. The increase of
aldehydes in both irradiated and non-irradiated cooked meat should
be caused by lipid oxidation under aerobic conditions during storage,
but additive treatments had no effect on the amounts of aldehydes at
3 day and 7 day storage. Hexanal, butanal, heptanal, propanal and
pentanal were detected in the cooked ground beef, but hexanal was
the major volatile aldehyde and the production of aldehydes agreed
well with TBARS data (Table 2). Ahn, Olson, Lee, et al. (1998) reported
that hexanal was a good indicator of lipid oxidation in meat.
Production of hydrocarbons and ketones did not show any consistent
trends by irradiation, additive treatments, and storage.
3. Results and discussion
3.3. Sulfur compounds
3.1. Lipid oxidation
Irradiation had no effect on the TBARS of cooked ground beef at Day 0
regardless of the additive treatments, but irradiated control and 0.1%
garlic-added beef had higher TBARS values than those of non-irradiated
ones at 3 day storage (P b 0.05) (Table 1). At Day 7, additive treatments
had no effect on the oxidation of nonirradiated cooked ground beef, but
0.5% onion-treatment showed a significant antioxidant effect in
Table 1
TBARS values of irradiated and nonirradiated cooked ground beef with different
additives during aerobic storage at 4 °C.
(Unit: mg MDA/kg meat)
0 day
Non-IR
IR
SEM
3 days
Non-IR
IR
SEM
7 days
Non-IR
IR
SEM
a–b
Controlc
G0.1%
O0.5%
SEM
0.34
0.31
0.01
0.33
0.30
0.03
0.29
0.30
0.01
0.02
0.02
0.71y
0.91x
0.05
0.74y
0.89x
0.03
0.65y
0.77x
0.04
0.03
0.05
1.09
1.04a
0.08
0.99
0.99a
0.04
0.88
0.78b
0.03
0.06
0.05
Values with different superscripts within a row are significantly different (P b 0.05).
n = 4.
Values with different superscripts within a column of the same storage time are
significantly different (P b 0.05).
c
Control: without garlic and onion, G0.1%: 0.1% garlic, O0.5%: 0.5% onion, Non-IR: nonirradiated, IR: 2.5 kGy irradiation. SEM: standard error of the means.
x–y
Addition of garlic or onion greatly increased the amount of sulfur
volatiles from irradiated and nonirradiated cooked ground beef
(Table 3). Non-irradiated cooked ground beef produced only carbon
sulfide, which disappeared after 7 day storage (Table 3). The amount of
S-volatiles produced in non-irradiated cooked ground beef with 0.1%
garlic or 0.5% onion treatment was much greater than those of the
control (P b 0.05). The amount of total sulfur volatiles produced from
both irradiated and non-irradiated 0.1% garlic-added cooked ground
beef was more than 10-fold of the 0.5% onion-added samples. Most of
the sulfur compounds in non-irradiated 0.1% garlic-added ground beef
remained in the meat, but only a small portion of 3,3-thiobis-1-propene
was detected in onion-added cooked ground beef after 7 day storage.
Ahn et al. (1999) reported that the sulfur compounds produced by
irradiation were highly volatile and readily disappeared during storage
under aerobic conditions. The organosulfur compounds and their
precursors in garlic such as allicin, diallyl sulfide and diallyl trisulfide
are reported to be involved in garlic odor and flavor. None of them was
detected in this study probably due to their high reactivity and low
stability (Kim, Jin, & Yang, 2009; Silagy & Neil, 1994).
Irradiation produced significant amounts of methanethiol, dimethyl
disulfide and dimethyl trisulfide, which are the main sulfur compounds
involved in irradiation off-odor in meat (Table 3). Irradiation is also
reported to produce various other sulfur compounds such as hydrogen
sulfide, carbon disulfide, mercaptomethane, methylthio ethane dimethyl
disulfide, bis-methylthio-methane, 3-methylthio-1-propene, ethanoic
acid S-methyl ester, and methyl thioacetate (Ahn, Jo, & Olson, 2000; Fan,
Sommers, Thayer, & Lehotay, 2002; Nam, Du, Jo, & Ahn, 2002; Patterson &
Stevenson, 1995). Irradiation changed the compositions and amounts of
sulfur compounds in both garlic- and onion-added cooked ground beef.
H.S. Yang et al. / Meat Science 88 (2011) 286–291
289
Table 2
Alcohols, aldehydes, hydrocarbons and ketone compounds of irradiated and nonirradiated cooked ground beef with different additives during aerobic storage at 4 °C.
(Unit: total ion counts × 106)
Non-IR
0 day
Alcohols
Aldehydes
Hydrocarbons
Ketones
3 days
Alcohols
Aldehydes
Hydrocarbons
Ketones
7 days
Alcohols
Aldehydes
Hydrocarbons
Ketones
IR
Control
G0.1%
O0.5%
SEM
257
427b
558
416
584
786a
825
344
112
918a
512
356
102
89
144
61
250
1743
200b
314
105
1806
1008a
273
111
1950
498b
293
95
1481
175
280
145
1425
816
271
96
1402
326
220
Control
G0.1%
O0.5%
SEM
136
816
945
452
123
733
511
605
81
1029
849
350
17
92
119
66
74
209
122
99
388a
1458
695
374
63b
1786
580
96
181b
1564
1060
372
54
148
140
95
51
222
163
89
241
1130b
285
445
116
1878a
252
113
197
1131b
287
368
86
65
45
110
a–b
Values with different superscripts within a row of the same irradiation treatment are significantly different (P b 0.05). n = 4.
Control: without garlic and onion, G0.1%: 0.1% garlic, O0.5%: 0.5% onion, Non-IR: non-irradiated, IR: 2.5 kGy irradiation. SEM: standard error of the means. Alcohols (ethanol, 1,2propanol and 1-butanol), Aldehydes (hexanal, butanal, heptanal, propanal and pentanal), Hydrocarbons (1-pentane, pentane, 1-hexane, hexane, heptane and octane) and Ketones
(2-propanone, 2,3-butanedione, 2-butanone and 2-heptanone).
In 0.1% garlic added meat, the amounts of 2-propene-1-thiol and di-2propenyl disulfide decreased by 80% and 70%, respectively. In onion
added meat, the amount of methanethiol increased by 2-fold, but 3,3thiobis-1-propene disappeared after irradiation. The amounts and
compositions of sulfur compounds in garlic- and onion-added cooked
ground beef changed dramatically during storage, especially in 0.5%
onion added-meat, and no sulfur compounds were detected in onionadded irradiated beef after 7 days of storage. No sulfur compounds were
detected in irradiated control meat after 3 day storage under aerobic
conditions. Most of sulfur compounds produced in irradiated ground beef
with 0.5% onion disappeared after 3 day storage and completely
disappeared after 7 days (Table 3). After 7 day storage, therefore, the
cooked ground beef with onion may not have irradiation odor/flavor nor
onion odor/flavor because no sulfur compounds were detected. With
0.1% garlic, most of the sulfur compounds still remained and the
composition not changed much even after 7 day storage. Therefore, using
0.1% garlic would be more efficient than 0.5% onion to produce sulfur
compounds to mask or modify irradiation off-odor.
Table 3
Sulfur compounds of irradiated and nonirradiated cooked ground beef with different additives during aerobic storage at 4 °C.
(Unit: total ion counts × 105)
Non-IRfs
0 day
Methanethiol
Carbon disulfide
2-Propen-1-thiol
Dimethyl disulfide
3,3-Thiobis-1-propene
Methyl 2-propenyl disulfide
Dimethyl trisulfide
Di-2-propenyl disulfide
3 days
Methanethiol
Carbon disulfide
2-Propen-1-thiol
Dimethyl disulfide
3,3-Thiobis-1-propene
Methyl 2-propenyl disulfide
Dimethyl trisulfide
Di-2-propenyl disulfide
7 days
Methanethiol
Carbon disulfide
2-Propen-1-thiol
Dimethyl disulfide
3,3-Thiobis-1-propene
Methyl 2-propenyl disulfide
Dimethyl trisulfide
Di-2-propenyl disulfide
a–b
IR
Control
G0.1%
O0.5%
SEM
Control
G0.1%
O0.5%
SEM
0b
26
0b
0b
0b
0b
0c
0b
221a
111
2504a
152a
598a
185a
82a
663a
91ab
75
0b
133a
12b
39b
34b
0b
43
55
54
22
53
14
7
49
203
0
0b
135
0b
0b
40
0b
468
10
524a
233
444a
220a
129
186a
222
18
0b
127
0b
24b
57
0b
115
10
78
38
45
25
27
27
0
0
0b
0b
0
0
0
0c
8
5
1151a
64a
470
104
0
122b
47
6
0b
51a
144
49
0
175a
22
20
41
16
34
31
0
5
0b
0
0b
0b
0b
0b
0b
0b
296a
16
1138a
147a
423a
134a
73a
20a
8b
0
0b
18b
0b
0b
0b
0b
71
9
43
45
15
4
4
11
0b
0
0b
0b
0b
0b
0
0b
31a
0
2756a
64a
483a
109a
0
213a
0b
0
0b
0b
10b
0b
0
0b
8
0
79
9
22
12
0
21
0b
0
0b
0b
0b
0b
0
0b
158a
20
1369a
240a
320a
107a
57
89a
0b
0
0b
0b
0b
0b
0
0
9
11
52
16
18
9
32
11
Values with different superscripts within a row of the same irradiation treatment are significantly different (P b 0.05). n = 4.
Control: without garlic and onion, G0.1%: 0.1% garlic, O0.5%: 0.5% onion, Non-IR: non-irradiated, IR: 2.5 kGy irradiation. SEM: standard error of the means.
290
H.S. Yang et al. / Meat Science 88 (2011) 286–291
Table 4
Sensory evaluation of irradiated and nonirradiated cooked ground beef with different
additives during aerobic storage at 4 °C.
Irradiation aroma
Ground beef aroma
Onion/garlic aroma
Irradiation flavor
Ground beef flavor
Onion/garlic flavor
Non-irradiated
Irradiated
Control
Control
G0.1%
O0.5%
3.18 ± 2.22
8.16 ± 3.06
0.14 ± 0.09c
3.16 ± 3.09
8.36 ± 3.36a
0.00 ± 0.00c
5.22 ± 4.74
6.25 ± 3.53
0.73 ± 0.62c
2.94 ± 2.45
7.31 ± 3.45ab
0.48 ± 0.39c
3.06 ± 2.97
5.71 ± 4.24
6.52 ± 4.00a
2.61 ± 2.71
5.58 ± 3.71b
5.64 ± 3.34a
4.07 ± 3.88
6.39 ± 3.39
3.69 ± 3.19b
3.46 ± 3.16
6.33 ± 3.02ab
3.15 ± 3.05b
a–c
Values with different superscripts within a row are significantly different (P b 0.05).
n = 10.
Irradiation aroma (0: weak and 15: strong intense), ground beef aroma (0: weak and
15: strong intense), onion/garlic aroma (0: weak and 15: strong intense), irradiation
flavor (0: weak and 15: strong intense), ground beef flavor (0: weak and 15: strong
intense), and onion/garlic flavor (0: weak and 15: strong intense). Control: without
garlic and onion, G0.1%: 0.1% garlic, O0.5%: 0.5% onion.
3.4. Sensory characteristics
No differences in the intensities of irradiation aroma and
irradiation flavor between irradiated and nonirradiated cooked
ground beef were found (Table 4). The intensity of ground beef
aroma, however, was the strongest in nonirradiated cooked ground
beef and the lowest in 0.1% garlic treatment, and the differences were
insignificant. Ground beef flavor also showed similar trends to ground
beef aroma, but the intensity was significantly lower with the addition
of garlic.
Huber, Brasch, and Waly (1953) reported that meat sterilized
through irradiation developed a characteristic odor. Most sulfur and
carbonyl compounds had low odor thresholds and are important to odor
(Wick, Murray, Mizutani, & Koshik, 1967). Hashim, Resurreccion, and
MaWatters (1995) reported that irradiating uncooked chicken breast
and thigh produced a characteristic bloody and sweet aroma that
remained after the thighs were cooked. Ground beef with garlic
produced very large amounts of sulfur compounds including methanethiol, dimethyl sulfide, and dimethyl disulfide, which are the main
sulfur compounds produced in meat by irradiation. In addition, garlic
produced even larger amounts of other sulfur compounds that are
responsible for their characteristic odor/flavor than onion. Although the
intensity of irradiated cooked control had higher irradiation aroma than
other treatments, it was not significantly different from other
treatments. The composition and amounts of sulfur compounds found
in irradiated cooked ground beef with 0.5% onion were similar to those
of non-irradiated ones at Day 0 and produced only methanethiol and
dimethyl disulfide after 3 day storage in aerobic packaging conditions
(Table 3). So, the odor/flavor of onion-added irradiated cooked ground
beef was expected to be similar to that of the irradiated cooked control.
Also, the intensities of irradiation aroma and irradiation flavor between
0.1% garlic-added and 0.5% onion-added irradiated cooked meat were
expected to be different because the composition and amounts of sulfur
compounds between the two treatments differ significantly. However,
the intensity of irradiation flavor of irradiated cooked ground beef with
garlic or onion was weak and was not different from that of nonirradiated or irradiated control (Table 4), indicating that cooking
changed or eliminated the irradiation aroma and irradiation flavor.
The perception of odor from samples containing sulfur volatiles can be
changed greatly depending upon their composition and amounts
present in the sample (Ahn, 2002; Ahn & Lee, 2002). Another reason
could be large variations among sensory panelists as shown in Table 4.
The intensities of “onion/garlic aroma” and “onion/garlic flavor” in
ground beef remained strong even after cooking, but ground beef with
onion alone had significantly lower scores than garlic treatment.
Garlic and onion produce sulfury odor and flavor, but they are not
considered as off-odor or off-flavors. However, too strong garlic or
onion odor and flavor can be objectionable to some consumers.
Considering the sensory results and the amounts of sulfur compounds
produced in cooked ground beef with added garlic or onion, 0.5% of
onion would be good enough to mask or change odor of irradiated
ground beef, but b0.1% of garlic is recommended to reduce the
intensity of garlic aroma and garlic flavor.
4. Conclusion
Irradiation accelerated lipid oxidation in cooked ground beef, but
storage of cooked meat under aerobic conditions had stronger effect than
irradiation. Onion at the 0.5% level showed a significant antioxidant effect
in irradiated cooked ground beef after 7 d storage. Addition of garlic or
onion greatly increased the amount of sulfur volatiles from cooked
ground beef, but the increase was greater with 0.1% garlic than 0.5% onion
treatment. Irradiation changed the amounts and compositions of sulfur
compounds in both garlic- and onion-added cooked ground beef. The
amounts and compositions of sulfur compounds in garlic- and onionadded cooked ground beef changed dramatically during storage,
especially in onion added-meat, and no sulfur compounds were detected
in onion-added irradiated beef after 7 days storage under aerobic
conditions. Although, addition of garlic and onion produced large
amounts of sulfur compounds, the intensity of irradiation off-odor and
irradiation off-flavor in irradiated cooked ground beef was similar to that
of the nonirradiated control. Addition of 0.5% of onion or 0.1% of garlic
helped in masking or changing irradiation aroma of cooked ground beef.
Acknowledgements
This study was supported jointly by the Iowa State University, and
the WCU (World Class University) program (R31-10056) through the
National Research Foundation of Korea funded by the Ministry of
Education, Science and Technology.
References
Ahn, D. U. (2002). Production of volatiles from amino acid homopolymers by
irradiation. Journal of Food Science, 67(7), 2565−2570.
Ahn, D. U., Jo, C., Du, M., Olson, D. G., & Nam, K. C. (2000). Quality characteristics of pork
patties irradiated and stored in different packaging and storage conditions. Meat
Science, 56, 203−209.
Ahn, D. U., Jo, C., & Olson, D. G. (2000). Analysis of volatile components and the sensory
characteristics of irradiated raw pork. Meat Science, 54, 209−215.
Ahn, D. U., Kawamoto, C., Wolfe, F. H., & Sim, J. S. (1995). Dietary alpha-linolenic acid
and mixed tocopherols, and packaging influence lipid stability in broiler chicken
breast and leg muscle tissue. Journal of Food Science, 60, 1013−1018.
Ahn, D. U., & Lee, E. J. (2002). Production of off-odor volatiles from liposome-containing
amino acid homopolymers by irradiation. Journal of Food Science, 67(7),
2659−2665.
Ahn, D. U., Nam, K. C., Du, M., & Jo, C. (2001). Volatile production in irradiated normal,
pale soft exudative (PSE) and dark firm dry (DFD) pork under different packaging
and storage conditions. Meat Science, 57(4), 419−426.
Ahn, D. U., Olson, D. G., Jo, C., Chen, X., Wu, C., & Lee, J. I. (1998). Effect of muscle type,
packaging, and irradiation on lipid oxidation, volatile production and color in raw
pork patties. Meat Science, 49, 27−39.
Ahn, D. U., Olson, D. G., Jo, C., Love, J., & Jin, S. K. (1999). Volatiles production and lipid
oxidation on irradiated cooked sausage as related to packaging and storage. Journal
of Food Science, 64, 226−229.
Ahn, D. U., Olson, D. G., Lee, J. I., Jo, C., Chen, X., & Wu, C. (1998). Packaging and
irradiation effects on lipid oxidation and volatiles in pork patties. Journal of Food
Science, 63, 15−19.
Ahn, D. U., Sell, J. L., Jeffery, M., Jo, C., Chen, X., Wu, C., & Lee, J. I. (1997). Dietary vitamin
E affects lipid oxidation and total volatiles of irradiated raw turkey meat. Journal of
Food Science, 62, 954−959.
Electronic Code of Federal Regulation (2009). Title 21: Food and drugs.Part 179: Irradiation
in the production, processing, and handling of food. http://ecfr.gpoaccess.gov
Accessed October 30, 2009.
Fan, X., Sommers, C. H., Thayer, D. W., & Lehotay, S. J. (2002). Volatile sulfur compounds
in irradiated precooked turkey breast analyzed with pulsed flame photometric
detection. Journal of Agricultural and Food Chemistry, 50(15), 4257−4261.
Griffiths, G., Trueman, L., Crowther, T., Thomas, B., & Smith, B. (2002). Onion — A global
benefit to health. Phytotheraphy Research, 16, 603−615.
Hashim, I. B., Resurreccion, A. V. A., & MaWatters, K. H. (1995). Disruptive sensory
analysis of irradiated frozen or refrigerated chicken. Journal of Food Science, 60,
664−666.
Hayes, D. J., Shogren, J. F. Fox, J. A., & Kliebenstein, J. B. (1995). Market tests of irradiated
meat. (Abstract). FSC Annual Meeting. Progress Report p73. Kansas City, MO.
H.S. Yang et al. / Meat Science 88 (2011) 286–291
Hertog, M. G. L., Hollman, P. C. H., & Katan, M. B. (1992). Content of potentially
anticarcinogenic flavonoids of 28 vegetables and 9 fruits commonly consumed in
the Netherlands. Journal of Agricultural and Food Chemistry, 40, 2379−2383.
Huber, W., Brasch, A., & Waly, A. (1953). Effects of processing conditions on
organoleptic changes in foodstuffs sterilized with high intensity electrons. Food
Technology, 7, 109−115.
Huskey, L. (1997). Industry reports. Food Safety Consortium Annual Meeting, Kansas
City, MO.
Jo, C., & Ahn, D. U. (2000). Production of volatiles from irradiated oil emulsion systems
prepared with amino acids and lipids. Journal of Food Science, 65, 612−616.
Jo, C., Lee, J. I., & Ahn, D. U. (1999). Lipid oxidation, color changes and volatiles
production in irradiated pork sausage with different fat content and packaging
during storage. Meat Science, 51, 355−361.
Kim, Y. J., Jin, S. K., & Yang, H. S. (2009). Effect of dietary garlic bulb and husk on the
physicochemical properties of chicken meat. Poultry Science, 88, 398−405.
Lee, E. J., Love, J., & Ahn, D. U. (2003). Effect of antioxidants on the consumer acceptance
of irradiated turkey meat. Journal of Food Science, 68(5), 1659−1663.
Meilgaard, M., Civille, G. V., & Carr, B. T. (1999). Sensory evaluation techniques (3rd Ed.).
Boca Raton, FL: CRC Press 354 pp.
Nam, K. C., & Ahn, D. U. (2003a). Use of antioxidants to reduce lipid oxidation and offodor volatiles of irradiated pork homogenates and patties. Meat Science, 63(1),
1−8.
291
Nam, K. C., & Ahn, D. U. (2003b). Use of double-packaging and antioxidant
combinations to improve color, lipid oxidation, and volatiles of irradiated raw
and cooked turkey breast patties. Poultry Science, 82(5), 850−857.
Nam, K. C., Ahn, D. U., Du, M., & Jo, C. (2001). Lipid oxidation, color, volatiles, and
sensory characteristics of aerobically packaged and irradiated pork with different
ultimate pH. Journal of Food Science, 66(8), 1225−1229.
Nam, K. C., Du, M., Jo, C., & Ahn, D. U. (2002). Quality characteristics of vacuumpackaged, irradiated normal, PSE, and DFD pork. Innovative Food Science and
Emerging Technology, 3(1), 73−79.
Patterson, R. L., & Stevenson, M. H. (1995). Irradiation-induced off-odor in chicken and
its possible control. British Poultry Science, 36, 425−441.
S.A.S. Institute (2000). SAS user's guide. Cary, NC, USA: SAS Institute, Inc..
Silagy, C., & Neil, A. (1994). Garlic as a lipid lowering agent. A meta-analysis. Journal of
Royal College of Physicians of London, 28, 39−45.
Tang, X., & Cronin, D. A. (2007). The effects of brined onion extracts on lipid oxidation
and sensory quality in refrigerated cooked turkey breast rolls during storage. Food
Chemistry, 100, 712−718.
Wick, E. L., Murray, E., Mizutani, J., & Koshik, M. (1967). Irradiation flavor and volatile
components of beef. Radiation preservation of foods. Advanced Chemistry Series.
Washington, DC: American Chemical Society.
Zhu, M., Lee, E. J., Mendonca, A., & Ahn, D. U. (2004). Effect of irradiation on the quality
turkey ham during storage. Meat Science, 66(1), 63−68.