Meat Science 89 (2011) 202–208
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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
Effect of garlic, onion, and their combination on the quality and sensory
characteristics of irradiated raw ground beef
Han Sul Yang a, b, Eun Joo Lee a, Sun Hee Moon a, c, Hyun Dong Paik a, c, Kichang Nam d, Dong U. Ahn a,⁎
a
Department of Animal Science, Iowa State University, Ames, IA 50011 3150, USA
Department of Animal Science, Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, Gyeongnam 660-701, Republic of Korea
Department of Food Science and Biotechnology of Animal Resources, Konkuk University, Seoul 143 701, Republic of Korea
d
Department of Animal Science and Technology, Sunchon National University, Suncheon 540 742, Republic of Korea
b
c
a r t i c l e
i n f o
Article history:
Received 13 January 2011
Received in revised form 11 April 2011
Accepted 20 April 2011
Keywords:
Ground beef
Irradiation
Garlic and onion
Lipid oxidation
Odor and flavor
a b s t r a c t
Irradiated raw ground beef had lower a*- and b*-values than nonirradiated ones regardless of garlic or onion
treatment at 0 d. Irradiation increased TBARS values of control ground beef, but addition of 0.5% onion or 0.1%
garlic + 0.5% onion reduced oxidative changes during storage. Addition of garlic or onion greatly increased the
amounts of sulfur compounds, but the increase was greater with garlic. With irradiation, the profiles and
amounts of S-volatiles in raw ground beef changed significantly. However, the intensity of irradiation aroma
in irradiated raw ground beef with garlic or onion was similar to that of the nonirradiated control. This
indicated that some of the sulfur compounds unique to garlic or onion interacted with common sulfur
compounds detected in irradiated meat and masked or changed the odor characteristics of irradiated raw
ground beef. It was concluded that N 0.5% onion or b 0.01% garlic would be needed to mask or prevent
irradiation aroma in irradiated raw ground beef.
© 2011 Elsevier Ltd. All rights reserved.
1. Introduction
Ground beef products comprise about 42% of beef consumption
and are also the major cause of foodborne illness in the U.S. (Davis &
Lin, 2005). Ground beef is highly susceptible to microbial contamination because of its nature and method of preparation, and the
elimination of contaminated pathogens such as E. coli O157:H7 and
Salmonella in raw ground beef is a challenge (Morris, Buzby, & Lin,
1997). Irradiation is recognized as the most effective method for
controlling pathogenic microorganisms in ground beef; yet only a
small fraction of ground beef (0.15%) is irradiated (Kume, Furuta, &
Todoriki, 2009). Consumer surveys and research indicated that
decreased meat quality has the greatest impact on consumer rejection
of irradiated meat (Lee, Love, & Ahn, 2003). Therefore, developing
methods to minimize quality changes are critical to increase consumer
acceptance of irradiated ground beef.
The most important quality changes in raw ground beef by
irradiation include color change, off-odor production, and accelerated lipid oxidation. The color changes in irradiated meat vary
depending on irradiation dose, animal species, muscle type, and
packaging conditions (Luchsinger et al., 1996; Nanke, Sebranek, &
Olson, 1998). In general, light meat such as pork loin and poultry
breast meat produced pink color, while dark meat such as beef
⁎ Corresponding author. 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.2011.04.020
became brown or gray after irradiation under aerobic conditions
(Ahn, Olson, Jo, Chen, Wu, & Lee, 1998; Kim, Nam, & Ahn, 2002;
Nanke, Sebranek, & Olson, 1999).
All irradiated meat produced characteristic irradiation odor
regardless of degree of lipid oxidation (Ahn et al., 1998). Hashim,
Resurreccion, and MaWatters (1995) reported that irradiating
uncooked chicken breast and thigh produced a characteristic “bloody
and sweet” aroma, but others described it as a “barbecued corn-like”,
“burned oil” or “burned feathers” odor (Ahn, Jo, Du, Olson, & Nam
2000a; Ahn, Jo, & Olson, 2000b; Heath, Owens, Tesch, & Hannah,
1990). Several off-odor volatile compounds were newly generated or
increased in meat after irradiation (Ahn, Nam, Du, & Jo, 2001;
Pattersin & Stevenson, 1995). Ahn et al. (2000a) and Ahn et al.
(2000b) reported that dimethyl sulfide, dimethyl disulfide and
dimethyl trisulfide were among the most prominent sulfur compounds produced by irradiation and were responsible for irradiation
off-odor in meat. The generation of new volatile compounds by
irradiation suggested that radiolytic degradation of proteins were
much more important than lipid oxidation in irradiation off-odor (Ahn
et al., 2000a; Ahn et al., 2000b; Jo & Ahn, 2000).
Antioxidants are used in fresh and further processed meat to
prevent oxidative rancidity and improve color stability, but the use of
antioxidant in meat products is highly regulated by the Food Safety
Inspection Agency (FSIS). For example, synthetic antioxidants such as
butylated hydroxytoluene (BHT) and butylated hydroxyanisol (BHA)
are only permitted to use in meat at 0.02% of fat content, and their use
should be listed on label of packaged meat. Consumers prefer the use
H.S. Yang et al. / Meat Science 89 (2011) 202–208
of plant-derived natural antioxidants to conventional synthetic
antioxidants (Johnston, Sepe, Brannan, & Alderton, 2005). Research
results showed that many natural antioxidants such as ascorbic acid,
α-tocopherol, sesamol, gallic acid, and quercetin had high potential in
preventing oxidative changes, minimizing off-odor production and
preventing color change in irradiated meat (Chen, Jo, Lee, & Ahn,
1999; Nam & Ahn, 2003). However, only antioxidants approved as
generally recognized as safe (GRAS) substances can be used in meat
products. The seasoning used in meat should be declared as “spice” or
“natural flavor” in the label (Electronic Code of Federal Regulations,
2009).
Garlic (Allium sativum L.) and onion (Allium cepa L.) are two major
spices widely used in cookery to complement and enhance the flavor
of meat products (Tang & Cronin, 2007). Both garlic and onion possess
strong antioxidant and flavor properties because of their
high phenolic and sulfur compounds, respectively (Griffiths, Trueman,
Crowther, Thomas, & Smith, 2002). The organosulfur compounds
and their precursors in garlic such as allicin, diallyl sulfide and diallyl
trisulfide are the key compounds that are involved in garlic odor
and flavor (Kim, Jin, & Yang, 2009; Silagy & Neil, 1994). Therefore,
addition of garlic or onion may change, mask, or improve the
odor/flavor characteristics of irradiated raw ground beef. Currently,
only non-fluid seasonings and dried spices and herbs can be added to
fresh or frozen red meat and irradiated. However, dried garlic and
onion lose most of their sulfur compounds during the drying
processing process, and will be much less effective than using fresh
ones.
The objective of this study was to determine the effectiveness of
fresh ground garlic, onion, and their combination in preventing lipid
oxidation and color changes, and masking irradiation aroma in raw
ground beef after irradiation while not producing excessive onion or
garlic odor.
2. Materials and methods
203
2.2. Ionizing radiation
The aerobically 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
at 22 °C. 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
dose range absorbed in meat samples was 2.48–2.83 kGy (Max/Min
ratio: 1.16). The non-irradiated control (0 kGy) samples were
exposed to ambient temperature (22 °C) of linear accelerator facility
while other samples were irradiated (30 min). There was minimal
temperature change in meat (b2 °C) during the irradiation process.
After irradiation, raw meat samples were immediately returned to a
4 °C cold room. All 8 treatments were analyzed for color, TBARS, and
volatiles at 0, 3 and 7 d, but sensory characteristics were determined
after 2 d storage using only 5 treatments (nonirradiated control and 4
irradiated ground beef with additive treatments).
2.3. Color measurement
Color was measured using a Labscan spectrophotometer (Hunter
Associated Labs Inc., Reston, VA, USA) that had been calibrated against
white and black reference tiles covered with the same film as those used
for meat samples. CIE L⁎ (lightness), a⁎ (redness), and b⁎ (yellowness)
values were obtained using illuminant A (light source). Area view and
port size were 0.64 and 1.02 cm, respectively and observer angle was
10°. An average value from two random locations of sample surface was
used for statistical analysis.
2.4. 2-Thiobarbituric acid-reactive substance (TBARS)
Lipid oxidation was determined using a TBARS method (Ahn,
Kawamoto, Wolfe, & Sim, 1995). The amounts of TBARS were
expressed as mg of malondialdehyde (MDA) per kg of meat.
2.1. Sample preparation
2.5. Microbiological analysis
Eight beef top rounds from different steers were obtained from a
local packing plant 6 d post-slaughter. The animals were 27 months
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
(approximately 8 kg/replication). The beef were of Choice grade,
and eight 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, 6) irradiated added with 0.5% onion, 7) nonirradiated added with 0.1% garlic + 0.5% onion and 8) irradiated added
with 0.1% garlic + 0.5% onion. Skinned fresh garlic and onion were
purchased from a local supermarket, ground until they became semiliquid 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-permeable bags (polyethylene,
10 × 15 cm, 2 mil, 2300 mL/m 2/24 h at 22.7 °C, Associated Bag Co.,
Milwaukee, WI, USA), stored at 4 °C overnight, and irradiated the next
day morning.
Ten grams of ground beef was aseptically removed from the
packages and placed into a stomacher bag (Nasco, Ft. Atkinson, WI,
USA) with 90 mL of 0.1% buffered peptone water. Samples were then
stomached in a Stomacher (400 Circulator, Seward, Bohemia, NY,
USA) for 1 min and serial dilutions were made. Subsequent duplicate
plating were made on tryptic soy agar (Difco Laboratories, Sparks, MD,
USA) supplemented with 0.6% yeast extract (TSA-YE), according to
manufacturer directions. Plates were then incubated at 35 °C for 48 h
in an incubation chamber. Counts were recorded as colony forming
units per gram (CFU/g).
2.6. 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 (Ahn
et al. 2001). The meat sample (3 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
204
H.S. Yang et al. / Meat Science 89 (2011) 202–208
connected using zero dead-volume column connectors (J&W Scientific, Folsom, CA, USA). Ramped oven temperature was used to
improve volatile separation. The 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; HewlettPackard) was 70 eV, and scan range was 19.1–400 m/z. Identification
of volatiles was achieved by comparing mass spectral data of samples
with those of the Wiley Library (Hewlett-Packard). Standards were
used to confirm the identification by the mass-selective detector. The
area of each peak was integrated using the ChemStation (HewlettPackard), and the total peak area (pA ⁎ s) was reported as an indicator
of volatiles generated from the sample.
Table 1
CIE color L*-, a*- and b*-values of irradiated and non-irradiated raw ground beef with
different additives during aerobic storage at 4 °C.
Color
Lightness (L*)
Redness (a*)
2.7. Sensory training and evaluation
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. During training, a
lexicon of aroma and color terms to be used on the ballot were
developed and references that can be used to anchor the rating scale
were identified Final anchor point ratings were decided upon by
training panel after initial evaluation and discussion. They were
trained with ground beef patty products for 2 weeks with the product
characteristics to be evaluated.
For the samples, panelists evaluated the color, irradiation aroma,
ground beef aroma and garlic/onion aroma using a 15-point hedonic
scale as described by Meilgaard, Civille, and Carr (1999), where one 1
was “no aroma” and fifteen 15 was “strong aroma.” Five samples were
provided to each panelists per session and the total number sessions
were 6 (3 sessions per each treatment). The samples were placed in
glass containers (Pyrex ®, Charleroi, PA) with plastic cover before the
sensory test. Panelists evaluated samples in isolated booths fitted with
a breadbox server and red incandescent lighting to make color
differences.
Yellowness (b*)
0 day
Non-IR
IR
SEM
3 days
Non-IR
IR
SEM
7 days
Non-IR
IR
SEM
0 day
Non-IR
IR
SEM
3 days
Non-IR
IR
SEM
7 days
Non-IR
IR
SEM
0 day
Non-IR
IR
SEM
3 days
Non-IR
IR
SEM
7 days
Non-IR
IR
SEM
Control
G0.1%
O0.5%
G0.1 + O0.5%
SEM
39.03
37.35
0.8
40.24
39.9
1.23
39.3
39.36
0.84
39.57
37.25
0.98
0.99
0.98
40.07
39.29
1.19
40.11
39.93
0.98
41.18
40.24
1.08
41.67
40.59
1.32
1.01
1.3
42.05
42.11
0.96
43.07
42.18
1.37
42.26
40.39
0.82
41.71
41.62
0.88
1.04
1.06
16.06x
8.41y
0.58
14.77x
7.25y
0.53
15.55x
7.46y
0.64
14.07x
8.01y
0.42
0.63
0.44
8.17
7.83
0.42
9.01
8.39
0.31
8.53
7.77
0.38
8.48x
7.75y
0.23
0.2
0.41
8.87x
7.37y
0.42
8.53
7.15
0.56
8.86
8.25
0.35
8.18
7.17
0.35
0.47
0.36
16.76x
13.05y
0.47
16.40x
13.05y
0.6
15.81x
11.76y
0.88
15.67x
12.57y
0.35
0.57
0.6
14.9
13.3
0.61
15.58
14.58
0.39
14
12.54
0.65
15.1
13.72
0.48
0.48
0.58
14.46
14.43
0.29
15.46
14.58
0.89
14.72
14.75
0.5
14.55
13.74
0.7
0.69
0.54
x,y
Values with different superscripts within a column at the same storage time are
significantly different (P b 0.05). n = 4. Control: without garlic and onion, G0.1%: 0.1%
garlic, O0.5%: 0.5% onion, G0.1 + O0.5%: 0.1% garlic + 0.5% onion, Non-IR: nonirradiated, IR: 2.5 kGy irradiation. SEM: standard error of the means.
2.8. Statistical analysis
The experiment had four replications. Data was analyzed by the
procedures of generalized linear model (GLM) of SAS (2000) 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 the 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.
3. Results and discussion
3.1. Color values
The CIE color values of non- and irradiated ground beef with added
garlic and/or onion are shown in Table 1. The lightness (L⁎) value of
ground beef was not affected by additives nor irradiation treatment.
During storage, however, L⁎-values of both irradiated and nonirradiated ground beef gradually increased. This findings agree with Kim
et al. (2002) who reported no irradiation effect on L⁎-values of beef
steaks. Also, these results are consistent with those of Ahn and Nam
(2004) who found no irradiation effect on L⁎-values of ground beef
with ascorbic acid and/or sesamol + tocopherol. Treating ground beef
patties with garlic and onion had no effect on L⁎-values.
The redness (a⁎) values of all ground beef at 0 d dramatically
decreased (P b 0.05) by irradiation. The a⁎-values of all irradiated
ground beef remained similar levels during storage, but those of nonirradiated ground beef decreased to the irradiated ground beef levels
after 3 d storage and then remained unchanged after that. There were
significant differences found between irradiated and nonirradiated
ground beef with some additive treatments after 3 d and 7 d storage,
but the differences were not consistent. Addition of garlic and onion
had no effect on the a⁎-values of both irradiated and nonirradiated
ground beef. The changes of color a*-value in irradiated ground beef at
Day 0 were similar to those of others (Kim et al. 2002; Nanke et al.,
1999). Satterlee, Wilhelm, and Barnhart (1971) reported that the red,
oxymyoglobin-like pigment formed from metmyoglobin was greatly
inhibited in oxygen atmosphere. Ahn and Nam (2004) suggested that
the addition of ascorbate increased the reducing power in beef and
increased the red color intensity of ground beef. However, addition of
garlic and onion was not effective in changing color values of irradiated
ground beef during storage.
Irradiation decreased the yellowness (b⁎) values of ground beef at
Day 0. However, there was no irradiation effect on b⁎- values after 3 d
and 7 d storage. Addition of garlic and onion also had no effect on the
b⁎- values of irradiated ground beef. Ismail, Lee, Ko, and Ahn (2008)
also found no irradiation effect on b⁎-values of ground beef after 3 and
7 d storage, but Nam and Ahn (2003) reported that addition of
H.S. Yang et al. / Meat Science 89 (2011) 202–208
Table 2
TBARS values of irradiated and nonirradiated raw ground beef with different additives
during aerobic storage at 4 °C.
(Unit: mg MDA/kg meat)
Control
G0.1%
O0.5%
G0.1 + O0.5%
SEM
O day
Non-IR
IR
SEM
0.15y
0.23x
0.01
0.15y
0.24x
0.02
0.13y
0.20x
0.01
0.15y
0.24x
0.03
0.01
0.02
3 days
Non-IR
IR
SEM
0.34y
0.59abx
0.04
0.38y
0.63ax
0.04
0.33
0.46b
0.04
0.37
0.49b
0.04
0.04
0.04
7 days
Non-IR
IR
SEM
0.69ay
0.97ax
0.11
0.43by
0.91ax
0.08
0.37by
0.60bx
0.06
0.41by
0.64bx
0.07
0.09
0.07
a,b
Values with different superscripts within a row are significantly different (P b 0.05).
n = 4.
x,y
Values with different superscripts within a column of the same storage time are
significantly different (P b 0.05).
Control: without garlic and onion, G0.1%: 0.1% garlic, O0.5%: 0.5% onion, G0.1 + O0.5%:
0.1% garlic + 0.5% onion, Non-IR: non-irradiated, IR: 2.5 kGy irradiation. SEM: standard
error of the means.
ascorbic acid+tocopherol maintained a⁎- values and increased b⁎-values
of irradiated beef during storage.
3.2. Lipid oxidation
The TBARS values of irradiated samples were higher than those of
non-irradiated ones (P b 0.05) throughout storage except for 0.5% onion
and 0.1% garlic + 0.5% onion treatments at 3 d storage (Table 2). TBARS
values of ground beef showed an increasing trend as the storage time
increased. Additives, especially onion and garlic + onion treatments
started to show antioxidant effects in irradiated raw ground beef after
3 d storage. After 7 d storage, 0.5% onion and 0.1% garlic + 0.5% onion
treatments showed significant antioxidant effects in both irradiated and
nonirradiated raw ground beef. The differences in TBARS values
205
between control and 0.5% onion and 0.1% garlic + 0.5% onion treatments
are small, but maintaining the TBARS values of ground beef as low as
possible is important because some sensitive consumers start to
recognize oxidation odor when the TBARS value is greater than 1.0
(Jayasingh, Cornforth, Brennand, & Carpenter, 2002). Several previous
studies indicated that irradiation accelerated lipid oxidation of meat
only under aerobic conditions (Ahn, 2002; Ahn et al., 2000a; Ahn et al.,
2000b; Jo & Ahn, 2000), and the effect of antioxidants in raw ground beef
was more distinct after 7 d storage than at 0 d (Ahn & Nam, 2004).
3.2.1. Volatiles
The production of alcohols, aldehydes, hydrocarbons, and ketones
from irradiated and nonirradiated raw ground beef were not
influenced by additives except for alcohols and aldehydes in
irradiated meat after 7 d storage (Table 3). The amounts of alcohols
produced from 0.5% onion- or 0.1% garlic + 0.5% onion-added
irradiated ground beef were significantly lower than those from
control and 0.1% garlic-added ground beef at Day 7. Irradiation had no
effect on the production of alcohols at Day 0, but the amount of
alcohols dramatically increased in nonirradiated ground beef after 7 d
storage because of the growth of microorganisms in nonirradiated
meat. The total plate counts of irradiated ground beef remained 3–4
log CFU/g meat level while those of nonirradiated meat increased to
7–8 log CFU/g meat after 7 d storage (Table 4). Irradiated ground beef
produced much greater amounts of aldehydes than nonirradiated
meats, especially after storage. In fact, the amounts of aldehydes
produced in irradiated meat were 3–10 times greater than those of the
nonirradiated ground beef depending upon additive treatment and
storage time. Irradiated control beef produced the highest amount of
aldehydes while 0.1% garlic + 0.5% onion-added meat produced the
lowest among the irradiated meats at Day 7 (Table 3). The aldehydes
detected in ground beef were mainly lipid oxidation-related products.
Ahn and Nam (2004) reported that hexanal was a good indicator of
lipid oxidation in meat. Hexanal was the major volatile aldehydes and
the production of aldehydes agreed well with TBARS data (Table 2).
Irradiated ground beef produced higher amounts of hydrocarbons
than nonirradiated ones and the differences between irradiated and
nonirradiated meats became greater after 7 d storage. However,
Table 3
Alcohols, aldehydes, hydrocarbons and ketones compounds of irradiated and nonirradiated raw ground beef with different additives during aerobic storage at 4 °C.
(Unit: Total ion counts × 106)
Non-IR
IR
Control
G0.1%
O0.5%
0 day
Alcohols
Aldehydes
Hydrocarbons
Ketones
219
20
213
532
231
25
267
626
238
18
292
600
3 days
Alcohols
Aldehydes
Hydrocarbons
Ketones
329
50
274
500
460
98
491
483
7 days
Alcohols
Aldehydes
Hydrocarbons
Ketones
2793
68
309
733
2808
40
590
344
G0.1 + O0.5%
SEM
Control
G0.1%
O0.5%
G0.1 + O0.5%
SEM
239
24
408
740
32
7
64
119
335
51
340
561
352
83
656
724
242
48
522
631
265
92
666
728
53
16
89
136
283
29
378
491
405
44
535
556
60
20
83
118
411
285
562
390
534
434
785
724
491
279
656
649
542
436
656
689
45
136
88
87
2222
35
319
466
1477
30
377
131
805
23
133
108
695a
420a
609
616
730a
237ab
979
693
414b
109ab
719
605
310b
93b
660
333
94
80
113
127
a,b,c
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, G0.1 + O0.5%: 0.1% garlic + 0.5% onion, Non-IR: non-irradiated, IR: 2.5 kGy irradiation. SEM: standard error of
the means.
Alcohols (ethanol, 1,2-propanol 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).
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H.S. Yang et al. / Meat Science 89 (2011) 202–208
Table 4
Total plate counts of irradiated raw ground beef with different additives during aerobic storage at 4 °C.
(Unit: log CFU/g)
Treatments
Control
G0.1%
O0.5%
G0.1 + O0.5%
0 day
3 days
7 days
Non-IR
IR
Non-IR
IR
Non-IR
IR
5.27 ± 0.27
5.44 ± 0.24
5.84 ± 0.43
5.28 ± 0.24
+
+
+
+
6.42 ± 0.47a
7.02 ± 0.16a
6.98 ± 0.34a
5.60 ± 0.14a
3.72 ± 0.49b
3.58 ± 0.17b
3.36 ± 0.16b
3.41 ± 0.06b
7.82 ± 0.18a
7.93 ± 0.14a
7.78 ± 0.05a
7.05 ± 0.28a
3.35 ± 0.12b
3.40 ± 0.15b
3.38 ± 0.10b
4.03 ± 0.18b
a,b
Values with different superscripts within a row of the same storage time are significantly different (P b 0.05). n = 4.
Control: without garlic and onion, G0.1%: 0.1% garlic, O0.5%: 0.5% onion, G0.1 + O0.5%: 0.1% garlic + 0.5% onion, Non-IR: non-irradiated, IR: 2.5 kGy irradiation, SEM: standard error of
the means, +: CFU/g meat b 10.
additive treatments had no effect on the production of hydrocarbons
in both irradiated and nonirradiated ground beef.
3.3. Sulfur volatiles
In nonirradiated ground beef, the production of sulfur compounds
(S-volatiles) greatly increased by the addition of 0.1% garlic, 0.5% onion,
or 0.1% garlic + 0.5% onion at Day 0: the sulfur compounds produced
from the nonirradiated ground beef with garlic include methanethiol,
2-propene-1-thiol, dimethyl disulfide, 3,3-thiobis-1-propene, methyl
2-propenyl disulfide, and di-2-propenyl disulfide. Garlic produces
greater number sulfur compounds than those listed here, but the
amounts of minor sulfur compounds were below the limit used here.
2-Propen-1-thiol was the major sulfur compounds of raw ground beef
added with garlic, but very large amounts of dimethyl disulfide,
3,3-thiobis-1-propene, and di-2-propenyl disulfide were also produced.
With 0.5% onion treatment alone, only 2-propene-1-thiol, dimethyl
disulfide, 3,3-thiobis-1-propene and methyl 2-propenyl disulfide were
newly produced. 2-Propen-1-thiol was the major sulfur compounds of
raw ground beef added with onion, but the amount was much smaller
than those with garlic. Carbon disulfide was produced from all ground
beef including control, but the amount was small compared with other
sulfur compounds. Total amount of sulfur compounds produced from
the ground beef containing garlic (0.1% garlic and 0.1% garlic + 0.5%
onion treatments) was over 20 times greater than that with onion alone,
indicating that the amount of sulfur compounds produced from 0.1%
garlic was much greater than that from 0.5% onion. During storage under
aerobic packaging conditions, the amounts of all sulfur compounds in
ground beef decreased rapidly, and 2-propene-1-thiol and dimethyl
disulfide were not detected from the nonirradiated ground beef with
0.5% onion treatment after 7 d storage (Table 5).
With irradiation, the profiles and amounts of S-volatiles in raw
ground beef were significantly different from those of nonirradiated
ground beef: in control beef, carbon disulfide was not detected, but
methanethiol, dimethyl disulfide and dimethyl trisulfide were newly
produced after irradiation (Table 5). Irradiation is reported to produce
various volatile sulfur compounds such as hydrogen sulfide, carbon
disulfide, mercaptomethane, dimethyl sulfide, methylthio ethane
Table 5
Sulfur compounds of irradiated and nonirradiated raw ground beef with different additives during aerobic storage at 4 °C.
(Unit: Total ion counts × 106)
Non-IR
IR
Control
G0.1%
O0.5%
G0.1 + O0.5%
SEM
Control
G0.1%
O0.5%
G0.1 + O0.5%
SEM
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
0b
73
0b
0b
0b
0c
0
0c
554a
71
14,864a
1334a
1553a
500a
0
3195a
0b
98
647b
209b
60b
0c
0
0c
649a
81
18,880a
1474a
543b
380b
0
1969b
45
25
1668
72
175
32
0
184
180ab
0
0b
357b
0b
0
38b
0
329a
0
2631a
1126a
642a
218a
200a
412
22b
0
56b
446b
119b
19b
10b
0b
198ab
0
1109ab
930a
322ab
202a
200a
174a
64
0
62
102
116
26
20
155
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
0b
18
0b
0b
0b
0b
0b
0b
212a
21
10,222a
692a
920a
200a
194a
1124a
0b
36
982
67b
25b
18b
2b
0b
298a
29
9896a
804a
865a
200a
139a
1122a
40
14
493
39
64
16
10
93
0b
0
0c
0c
0c
0b
0b
0b
100a
0
630a
529a
398a
167a
60a
142a
0b
0
97c
50b
0c
20b
8b
0b
90a
0
330b
288b
302b
151a
50a
139a
7
0
64
44
28
13
13
12
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
0
0
0c
0b
0c
0b
0b
0c
118
0
3434a
181a
533a
150a
80a
340a
0
11
0c
0b
23c
25b
10b
0c
52
0
1501b
111a
298b
70b
20b
69b
43
0
107
58
53
30
10
16
0b
0
0c
0c
0c
0c
0c
0c
50a
0
127b
229b
369a
106a
20a
92a
0b
0
0c
0c
0c
0c
0c
0c
0b
0
478a
400a
236b
58b
20b
60b
0
0
25
24
27
10
4
17
a,b,c
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, G0.1 + O0.5%: 0.1% garlic + 0.5% onion, Non-IR: non-irradiated, IR: 2.5 kGy irradiation. SEM: standard error of the means.
H.S. Yang et al. / Meat Science 89 (2011) 202–208
dimethyl disulfide, bis-methylthio-methane, 3-methylthio-1-propene,
ethanoic acid S-methyl ester, methyl thioacetate and dimethyl trisulfide
(Patterson & Stevenson 1995; Ahn et al., 2000a; Ahn et al., 2000b; Fan,
Sommers, Thayer, & Lehotay, 2002) some of which are also produced
from garlic and onion. Most sulfur and carbonyl compounds have low
odor thresholds and important to odor (Wick, Murray, Mizutani, &
Koshik, 1967). The perception of odor from samples containing sulfur
volatiles, however, can be changed depending on the composition and
amounts of sulfur compounds as well as those of other volatiles in the
sample because aroma is not a simple result of sulfur volatile content but
the interactions among sulfur compounds as well as sulfur compounds
with other volatile compounds (Ahn, 2002; Ahn & Lee, 2002). Therefore,
the aroma of onion and garlic are different from irradiation odor, and
high levels of sulfur compounds such as mercaptomethane, dimethyl
sulfide and dimethyl disulfide found in irradiated meat do not necessary
mean strong irradiation aroma.
Sulfur compounds produced in meat by irradiation are via the
radiolytic degradation of the side chains of sulfur-containing amino
acids (methionine and cysteine) and the secondary chemical reactions after the primary radiolytic degradation of side chains (Ahn,
2002). More than one site of amino acid side chains was susceptible to
free radical attack, and many volatiles were produced by secondary
chemical reactions after the primary radiolytic degradation of side
chains (Ahn, 2002).
Methionine and cysteine were the major amino acid sources for
sulfur compounds, but the contribution of methionine to the
production of irradiation-induced sulfur compounds was far greater
than that of cysteine (Ahn & Lee, 2002). The changes in profiles and
amounts of sulfur compounds in raw ground beef after irradiation
confirm the secondary chemical reactions among sulfur compounds
and between sulfur compounds and other volatiles in the meat.
The amount of total sulfur compounds in raw ground beef with
garlic, onion, and garlic + onion treatments decreased dramatically
after irradiation (Table 5). As in irradiated control, carbon disulfide
was not detected in irradiated garlic and/or onion-added ground beef.
In garlic-added raw ground beef, the amounts of 2-propene-1-thiol
and di-2-propenyl disulfide decreased more than 80% after irradiation, but changes of other sulfur compounds were not comparatively
small. In onion-added ground beef, the amount of 2-propene-1-thiol
decreased by 90%, but methanethiol was newly produced. The
amounts of sulfur volatiles in irradiated ground beef decreased
dramatically as in nonirradiated ground beef during storage: only
2-propene-1-thiol, dimethyl disulfide, methyl 2-propenyl disulfide,
and dimethyl trisulfide were detected in 0.5% onion-added ground
beef after 3 d and no sulfur compounds were found in both onion
alone and control ground beef after 7 d storage. In garlic added ground
beef, however, significant amounts of sulfur compounds, which
include 2-propene-1-thiol, dimethyl disulfide, 3,3-thiobis-1-propene,
methyl 2-propenyl disulfide, dimethyl trisulfide and di-2-propenyl
disulfide were produced even after 7 d storage (Table 5). Ahn et al.
(2001) reported that the sulfur compounds produced by irradiation
were highly volatile and readily disappeared during storage under
aerobic conditions. However, approximately 20% of sulfur compounds
207
were still remaining in garlic-added raw ground beef after 7 d storage
in aerobic conditions.
3.4. Sensory characteristics
Sensory results indicated that the intensity of irradiation aroma
was significantly (P b 0.05) higher in irradiated control than nonirradiated control beef. Addition of 0.5% onion treatment had no
effect on the intensity of “irradiation aroma” in irradiated raw
ground beef (Table 6). It seems that the amounts and odor intensity
of sulfur compounds from onion, which include 2-propene-1-thiol,
3,3-thiobis-1-propene, methyl 2-propenyl disulfide, were not large
and strong enough to overcome the odor produced by methanethiol,
dimethyl disulfide, and dimethyl trisulfide (Table 5). Addition of
0.1% garlic or 0.1% garlic + 0.5% onion significantly reduced, and the
intensity of sulfury aroma in irradiated raw ground beef with garlic
and garlic + onion was similar to that of the nonirradiated control
(Table 6), indicating that adding garlic or garlic + onion can mask or
totally change the odor/flavor characteristics of irradiated ground
beef. Ground beef with 0.1% garlic and 0.1% garlic + 0.5% onion
produced very large amounts of sulfur compounds including
mercaptomethane, 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.
Irradiated raw ground beef produced significantly lower “ground
beef aroma” than non-irradiated ones regardless garlic, onion or
garlic + onion treatment and addition of garlic or onion had no effect
on the intensity of “ground beef aroma” in irradiated ground beef.
This suggested that some of the sulfur compounds unique to garlic or
onion (2-propen-1-thiol, 3,3-thiobis-1-propene and di-2-propenyl
disulfide) interacted with common sulfur compounds detected in
irradiated meat (methanethiol, dimethyl disulfide and dimethyl
trisulfide) and masked or changed the odor characteristics of
irradiated raw ground beef. The color of irradiated ground beef
was lighter than nonirradiated beef and addition of garlic or onion
had little effect on the color of irradiated ground beef (Table 6).
The perception of odor from samples containing sulfur volatiles
changed greatly depending upon their composition and amounts
present in the sample (Ahn & Lee, 2002). Garlic and onion both
produce sulfury odor, but their odor in foods is not considered as offodor. The amounts of sulfur compounds produced in irradiated
ground beef by 0.5% onion were similar to those by irradiation, and
the intensity of onion aroma in meat was relatively low and was not
enough to mask or reduce irradiation aroma. Addition of 0.1% garlic or
0.1% garlic + 0.5% onion produced 10 times greater amounts of sulfur
compounds than those produced by 2.5 kGy irradiation, but produced
significant “onion/garlic aroma”. Therefore, we suggest use of N0.5%
onion, b0.1% garlic, or their combination to mask or prevent
irradiation aroma in irradiated raw ground beef. Both dried or freshly
ground onion and garlic are permitted to use in irradiated ground
beef, and use of dried onion and garlic would be more convenient than
freshly ground ones. However, we suggest use of freshly ground onion
Table 6
Sensory evaluation of irradiated and nonirradiated raw ground beef with different additives during aerobic storage at 4 °C (Tukey's HSD 5%).
Nonirradiated
Irradiation aroma
Ground beef aroma
Onion/garlic aroma
Ground beef color
Irradiated (2.5 kGy)
Control
Control
G0.1%
O0.5%
G0.1 + O0.5%
2.57 ± 2.12c
7.75 ± 2.86a
0.60 ± 0.52c
12.22 ± 2.08a
7.96 ± 4.85a
4.19 ± 2.92b
0.83 ± 0.70c
7.44 ± 3.97bc
4.21 ± 3.77bc
3.63 ± 2.75b
7.24 ± 3.30a
6.19 ± 3.27c
6.21 ± 4.13ab
4.07 ± 2.86b
3.25 ± 3.02b
8.34 ± 2.79b
3.13 ± 3.05c
3.69 ± 3.02b
7.99 ± 3.62a
6.50 ± 3.66bc
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), and ground beef color
(0: light and 15: dark). Control: without garlic and onion, G0.1%: 0.1% garlic, O0.5%: 0.5% onion, G0.1 + O0.5%: 0.1% garlic + 0.5% onion.
208
H.S. Yang et al. / Meat Science 89 (2011) 202–208
and garlic because they contain greater amounts of sulfur compounds
than dried ones (unpublished data) and are more efficient in masking
irradiation aroma.
4. Conclusion
Addition of 0.5% onion showed some antioxidant effect, but had no
effect on the color of irradiated raw ground beef. Adding garlic, onion,
and their combination produced large amounts of sulfur compounds
in non-irradiated ground beef, but their amounts decreased and
profiles changed after irradiation. Addition of 0.1% garlic in ground
beef was effective, but 0.5% onion was not enough to mask irradiation
aroma. Onion at 0.5% produced weak onion aroma, but garlic at 0.1%
level produced very strong garlic aroma in irradiated raw ground beef.
Therefore, N0.5% onion but b0.1% garlic would be needed to mask or
prevent irradiation aroma in irradiated raw ground beef.
Acknowledgment
This study was supported jointly by the Iowa State University, and
WCU (World Class University) program (R31-10056) through the
National Research Foundation of Korea funded by the Ministry of
Education, Science and Technology.
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