PROCESSING, PRODUCTS, AND FOOD SAFETY
Evaluation of radiation-induced compounds in irradiated raw
or cooked chicken meat during storage
J.-H. Kwon,* K. Akram,* K.-C. Nam,† E. J. Lee,‡§ and D. U. Ahn‡§1
*Department of Food Science and Technology, Kyungpook National University, Daegu 702-701, Korea;
†Department of Animal Science and Technology, Sunchon National University, Suncheon 540-742, Korea;
‡Department of Animal Science, Iowa State University, Ames 50011-3150;
and §Department of Agricultural Biotechnology, Major in Biomodulation, Seoul National University,
599 Gwanak-ro, Gwanak-gu, Seoul 151-921, Korea
ABSTRACT The concentrations of hydrocarbons, 2-alkylcyclobutanones, and sulfur volatiles in irradiated (0
and 5 kGy) chicken meat samples (raw, precooked, and
irradiated-cooked) were analyzed after 0 and 6 mo of
frozen storage (−40°C) under oxygen-permeable packaging conditions. Two hydrocarbons [8-heptadecene
(C17:1) and 6,9-heptadecadiene (C17:2)], two 2-alkylcyclobutanones (2-dodecylcyclobutanone and 2-tetradecylcyclobutanone), and dimethyl disulfide were determined as radiation-induced detection markers in the
irradiated raw and cooked chicken meats. Although ir-
radiated-cooked samples produced fewer hydrocarbons
and 2-alkylcyclobutanones than precooked irradiated
samples, the number of individual hydrocarbons or
2-alkylcyclobutanones was still sufficient to detect radiation treatment even after 6 mo of storage at −40°C.
Among sulfur volatiles, only dimethyl disulfide was
found in meat after 6 mo of storage, indicating it has
potential to be used an irradiation detection marker for
frozen-stored meats under oxygen-permeable packaging
conditions.
Key words: irradiation marker, hydrocarbons, 2-alkylcyclobutanones, sulfur volatiles, chicken meat
2011 Poultry Science 90:2578–2583
doi:10.3382/ps.2010-01237
INTRODUCTION
Irradiation improves the safety and shelf life of food
products by controlling microorganisms. Irradiation of
raw meat or poultry has potential to enhance community health by preventing food-borne diseases (Osterholm
and Norgan, 2004). The Centers for Disease Control
and Prevention estimated that if 50% of the meat in the
United States were irradiated, morbidity and mortality
caused by food-borne illness would decrease by approximately 25% (Eustice and Brubn, 2006). Electrons with
energies up to 10 MV, x-rays with energy up to 5.0
MV, and gamma rays from cobalt-60 and cesium-137
are all allowed by the United States Food and Drug
Administration for food irradiation (Cleland, 2006).
Many other countries have approved irradiation as an
efficient technology to control pathogens and parasites
and to extend the shelf life of products (Robertson and
Holly, 2000). However, most countries have various reg-
©2011 Poultry Science Association Inc.
Received November 15, 2010.
Accepted April 28, 2011.
1 Corresponding author: duahn@iastate.edu
ulations with mandatory labeling requirements for irradiated foods. In this scenario, effective and validated
detection methods for irradiated food products are very
important for the enforcement of laws and regulations
and to facilitate international trade (Molins, 2001).
Along with photostimulated luminescence, thermoluminescence, microbiological screening, electron spin
resonance spectroscopy, and other procedures, the formation of long-chain hydrocarbons and 2-alkylcyclobutanones in irradiated food products was standardized
by the European Committee for Normalization as reference methods for the detection of irradiated foods
(Delincée, 2002).
Irradiation of fats or oils causes loss of an electron
from acyl-oxygen bond in fatty acids, followed by a rearrangement process to produce 2-alkylcyclobutanones
such as 2-dodecylcyclobutanone (DCB) and 2-tetradecylcyclobutanone (TCB) specific to their parent fatty acids (Nawar, 1986; Stewart, 2001). Both DCB and
TCB could be used as radiation-induced markers because of their absence in nonirradiated foods (Meier and
Stevenson, 1993; Stewart et al., 2001). However, some
studies found a higher concentration of 2-(tetradec-5′enyl) cyclobutanone specific to oleic acid in irradiated
foods (Stewart et al., 2000, 2001)
2578
RADIATION-INDUCED COMPOUNDS IN IRRADIATED CHICKEN MEAT
In foods containing fat, the cleavage of chemical
bonds in fatty acids upon irradiation generates hydrocarbons. Hydrocarbons produced by irradiation have 1
fewer carbon atom than the parent fatty acid (Cn-1) or
2 fewer carbon atoms and an additional double bond at
position 1 (Cn-2, 1-ene), which is predominately generated by the breakage of fatty acid moieties of triglycerides, mainly at the α and β positions of carbonyl groups
(Letellier and Nawar, 1972; Spiegelberg et al., 1994).
Irradiation treatments produce very reactive hydroxyl radicals in aqueous (Thakur and Singh, 1994)
or oil (O’Connell and Garner, 1983) emulsion systems
that can initiate lipid oxidation to form a lipid radical
by removing a hydrogen atom from fatty acyl chain of
polyunsaturated fatty acids. After a series of reactions,
the lipid radicals produce lipid hydroperoxides that
break into various volatile compounds including aldehydes, ketones, hydrocarbons, and sulfur compounds
(Gray, 1978; Enser, 1987). Ahn (2002) reported that
sulfur volatile compounds in irradiated meat are mainly
formed by the radiolytic degradation of sulfur-containing amino acids (e.g., Cys and Met).
The objective of this study was to determine irradiation-induced chemical changes in irradiated raw or
cooked chicken meat during frozen storage. The irradiation-induced compounds were evaluated as possible
detection markers for irradiated chicken meat.
2579
then cooked. Cooking was done in an 85°C water bath
to an internal temperature of 75°C. The cooked chicken
meats were repackaged in oxygen-permeable nylon bags
(10.2 × 15.2 cm; Associated Bag Co.) after draining
meat juices. Oxygen-permeable nylon bags were used
to check retention and detection of volatile radiolytic
compounds during storage. Meat samples were irradiated at 5 kGy using a linear accelerator (Circe IIIR,
Thomson CSF Linac, St. Aubin, France). The energy
and power levels used were 10 MV and 10.2 kW, respectively, and the average dose rate was 92.0 kGy/
min. The maximum:minimum ratio was approximately
1.18. The absorbed dose was ensured by 2 Ala dosimeters/cart and read using a 104 Electron Paramagnetic
Resonance Instrument (Bruker Instruments Inc., Billerica, MA). For the irradiated cooked chicken meat,
raw chicken meat was irradiated first and then cooked
immediately after irradiation using the same conditions
as above. Samples were analyzed at 0 d and after 6 mo
of storage at −40°C under oxygen-permeable packaging
conditions.
Fatty Acid Composition
1-Tetradecene (C14:1), pentadecane (C15:0), 1-hexadecene (C16:1), 1,7-hexadecadiene (C16:2), heptadecane
(C17:0), 8-heptadecene (C17:1), eicosane (C20:5) DCB,
TCB, and 2-(5′-tetradecenyl) cyclobutanone standards
(Sigma-Aldrich, St. Louis, MO) were used to identify
hydrocarbons and 2-alkylcyclobutanones. Fresh chicken
thighs were purchased from a local supermarket (Ames,
IA), ground through a 5-mm plate, and vacuum packaged in oxygen-impermeable nylon–polyethylene bags
(~100 g; O2 permeability: 9.3 mL of O2/m2 per 24 h at
0°C; Koch, Kansas City, MO) within 6 h of purchase.
The fat in raw chicken meat was extracted using
Folch’s method (Folch et al., 1957). The fatty acid
composition was analyzed after methylating fats using
BF3-methanol (14% solution; Supelco, Bellefonte, PA).
The fatty acid methyl esters were separated using a gas
chromatograph (GC; model 6890, Agilent Technologies, Wilmington, DE) equipped with a flame ionization detector (Agilent Technologies). A split inlet (split
ratio: 29:1) was used to inject samples into an HP-5
capillary column (0.25 mm × 30 m × 0.25 μm), and a
ramped oven temperature was used (80°C for 0.3 min,
increased to 180°C at 30°C/min, and increased to 230°C
at 6°C/min). Inlet and detector temperatures were 180
and 300°C, respectively. Helium was the carrier gas at a
constant flow of 1.1 mL/min. The flows of detector air,
H2, and makeup gas (He) were 300, 30, and 28 mL/min,
respectively. Fatty acids were identified using the retention times of known standards. Relative quantities were
expressed as weight percentage of total fatty acids.
Cooking and Irradiation of the Chicken Meat
Hydrocarbons and 2-Alkylcyclobutanones
Five treatments were prepared depending on cooking
and irradiation conditions: nonirradiated raw chicken
meat (uncooked–0 kGy), irradiated raw chicken meat
(uncooked–5 kGy), nonirradiated cooked chicken meat
(cooked–0 kGy), precooked irradiated chicken meat
(cooked–5 kGy), and irradiated cooked chicken meat
(5 kGy–cooked). Uncooked meat samples were packaged in oxygen-permeable nylon bags (10.2 × 15.2 cm;
2,300 mL/m2 per 24 h; 2 MIL; Associated Bag Co.,
Milwaukee, WI). For cooked meat, samples were vacuum packaged in nylon–polyethylene bags (O2 permeability: 9.3 mL of O2/m2 per 24 h at 0°C; Koch) and
Thirty grams of chicken meat, 300 mL of solvent
(hexane:isopropanol, 3:2 vol/vol), and 50 g of anhydrous sodium sulfate were added in a 500-mL centrifuge bottle and homogenized using a Polytron (model
PT 10/35, Brinkmann, Westbury, NY) for 1 min at
highest speed to extract fat. Samples were kept overnight and then centrifuged at 2,000 × g for 20 min at
4°C. The supernatant containing fat was collected and
the solvent (hexane–isopropanol mixture) was removed
using a rotary vacuum evaporator at <45°C. The resulting fat was placed in N2-filled vials and stored at
−20°C. Hydrocarbons were separated using a Florisil
MATERIALS AND METHODS
Samples and Chemicals
2580
Kwon et al.
column (200 × 20 mm glass column; Sigma-Aldrich,
St. Louis, MO) packed with 30 g of deactivated Florisil
and a 1-cm layer of anhydrous sodium sulfate on the
top. An aliquot of extracted fat (1 g) was mixed with
an internal standard (1 mL of n-eicosane, 4 μg/mL in
n-hexane) and loaded to the column. Hexane (120 mL)
was used to elute hydrocarbons. The eluent was collected and concentrated to 2 mL in a rotary vacuum
evaporator (model R200, Buchi Labortechnik, Flawil,
Switzerland) and further concentrated to 0.5 mL under N stream. For 2-alkylcyclobutanones, extracted fat
(0.5 g) was mixed with an internal standard (1 mL
of 2-cyclohexylcyclohexanone, 1 μg/mL in n-hexane)
and applied to a Florisil column, washed with 150 mL
of hexane, and then eluted with 120 mL of diethyl
ether:hexane (2:98 vol/vol) at a flow rate of 3 mL/min.
The eluent was concentrated to 2 mL using a rotary
vacuum evaporator and further concentrated to 0.2 mL
using N gas.
A GC–mass spectrometer (MS; Agilent Technologies) was used to analyze hydrocarbons and 2-alkylcyclobutanones. Ten milligrams per liter of standard
solution (5 μL) and samples (10 μL) was injected to a
splitless inlet of a GC, separated using a DB-5 column
(30.0 m × 0.32 mm i.d., 0.25 m film thickness), and
identified using a mass selective detector. A ramped
oven temperature was used to separate hydrocarbons.
The initial oven temperature was 120°C and was increased to 175°C at 10°C/min and to 275°C at 25°C/
min. A constant column flow at 1.5 mL/min was used
and the temperature of inlet was set at 250°C. The
ionization potential of mass selective detector (model
5973, Agilent Technologies) was 70 eV and the scan
range was 30.1 to 350 m/z. Identification of hydrocarbons and 2-alkylcyclobutanones was achieved by
comparing the retention time and mass spectral data
of samples with those of the authentic hydrocarbons
and 2-alkylcyclobutanones standards from the Wiley
Library (Agilent Technologies). The concentration of
each hydrocarbon in fat was determined using n-eicosane (4 μg/mL) or 2-cyclohexylcyclohexanone (1 μg/
mL) as the internal standards.
Sulfur Volatile Compounds
A dynamic headspace analysis for sulfur volatiles was
performed using a Solartek 72 Multimatrix-Vial Autosampler/Sample Concentrator 3100 (Tekmar-Dohrmann,
Cincinnati, OH) connected to a GC–MS (HP 6890–HP
5973, Agilent Technologies) according to the method of
Ahn et al. (2001). A minced sample (3 g) was placed
in a 40-mL vial, flushed with He (275 kPa) for 3 s, and
capped airtight with a Teflon (DuPont, Wilmington,
DE) fluorocarbon resin–silicone septum. The maximum
waiting time in a loading tray (4°C) was less than 2
h to minimize oxidative changes before analysis. The
chicken meat sample was purged with He (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 column for 60 s at 225°C. An HP-624 column
(7.5 m, 0.25 mm i.d., 1.4 μm nominal), HP-1 column
(52.5 m, 0.25 mm i.d., 0.25 μm nominal), and HP-Wax
column (7.5 m, 0.25 mm i.d., 0.25 μm nominal) were
connected using zero dead-volume column connectors
(J&W Scientific, Folsom, CA). A ramped oven temperature was used to improve volatile separation. The
initial oven temperature of 0°C was held for 1.5 min.
The oven temperature was then increased to 15°C at
2.5°C/min, to 45°C at 5°C/min, to 110°C at 20°C/min,
and to 170°C at 10°C/min and held for 2.25 min at that
temperature. Constant column pressure at 141 kPa was
maintained. The ionization potential of MS was 70 eV
and the scan range was 19.1 to 350 m/z. Identification
of volatiles was achieved using retention time match
plus Wiley Library (Agilent Technologies). The area of
each peak was integrated using ChemStation software
(Agilent Technologies) and the total peak area (total
ion counts × 104) was reported as an indicator of volatiles generated from the samples.
Statistical Analysis
The experiments, performed in 3 replications, were
designed to monitor the radiation-induced markers,
such as fat-derived hydrocarbons and 2-alkylcyclobutanones, along with production of sulfur volatiles from
irradiated chicken meat. An ANOVA was performed
using the GLM procedure of SAS software (SAS Institute Inc., 1995). The Student–Newman–Keul’s multiple
range test was used to compare the mean values of the
treatments. Mean values and SEM were reported (P <
0.05).
RESULTS AND DISCUSSION
Fatty Acid Compositions
Effect of irradiation before or after cooking on fatty
acid composition of chicken is exhibited in Table 1. The
oxidation rates of lipids and cholesterol in a meat are
influenced by the composition of fats, where polyunsaturated fatty could be oxidized by free radicals (Li et
al., 1996). In this study, the 5-kGy irradiation before
or after cooking did not significantly change the fatty
acid composition of chicken meat. Hau et al. (1992) also
reported that irradiation induced little change in the
fatty acid composition of raw or cooked meats. 8-Heptadecene (C17:1) and 6,9-heptadecadiene (C17:2) are derived from oleic acid and linoleic acids, respectively,
and are found in foods containing irradiated fat (Spiegelberg et al., 1994). Palmitic, stearic, and oleic acids
are the major fatty acid precursors that generate radiolytic products of DCB, TCB, and 2-(tetradec-5′-enyl)
cyclobutanone, respectively, upon irradiation (Kim et
al., 2004).
2581
RADIATION-INDUCED COMPOUNDS IN IRRADIATED CHICKEN MEAT
Table 1. Effect of irradiation before or after cooking on fatty acid composition (relative %) of chicken meat
Raw meat
Cooked before irradiation
Cooked after irradiation
Fatty acid1
0 kGy
5 kGy
0 kGy
5 kGy
5 kGy
Myristic acid (C14:0)
Palmitic acid (C16:0)
Palmitoleic acid (C16:1)
Heptadecanoic acid (C17:0)
10-Heptadecenoic acid (C17:1, n-10)
Stearic acid (C18:0)
Oleic acid (C18:1, n-9)
Linoleic acid (C18:2, n-6)
Gamma-linolenic acid (C18:3, n-6)
Alpha-linolenic acid (C18:3, n-3)
Arachidic acid (C20:0)
Gondoic acid (C20:1, n-9)
Arachidonic acid (C20:4, n-6)
EPA (C20:5, n-3)
Behinic acid (C22:0)
Adrenic (C22:4, n-6)
DPA (C22:5, n-6)
DHA (C22:6, n-3)
Total
0.72a
25.24a
9.90a
0.12a
0.11a
5.32a
38.64a
16.89a
0.20a
0.72a
0.23a
0.33a
1.00a
0.07a
0.09a
0.20a
0.16a
0.05a
100.00
0.69a
25.19a
9.45a
0.08a
0.10a
5.72a
38.41a
16.33a
0.20a
0.72a
0.27a
0.90a
1.29a
0.12a
0.07a
0.25a
0.13a
0.08a
100.00
0.68a
24.92a
10.51a
0.09a
0.14a
5.19a
37.91a
16.34a
0.18a
0.80a
0.19a
0.82a
1.17a
0.07a
0.05a
0.41a
0.48a
0.06a
100.00
0.67a
24.81a
10.48a
0.15a
0.14a
5.23a
39.35a
15.63a
0.16a
0.75a
0.30a
0.68a
0.99a
0.08a
0.12a
0.34a
0.09a
0.05a
100.00
0.76a
24.29a
10.74a
0.12a
0.37a
5.69a
36.11a
16.12a
0.25a
0.83a
0.50a
1.75a
1.32a
0.06a
0.21a
0.61a
0.21a
0.04a
100.00
aMeans
1EPA
within a row with same superscripts are not significantly different ; n = 3.
= Eicosapentaenoic acid; DPA = docosapentaenoic acid; DHA = docosahexaenoic acid.
Hydrocarbons
ucts such as roasted chicken (Noleau and Toulemonde,
1987). However, 8-heptadecene and 6,9-heptadecadiene
were not detected in any of the nonirradiated chicken meat samples. 8-Heptadecene (C17:1) showed more
storage stability than 6,9-heptadecadiene (C17:2) in all
the irradiated samples. The concentration of 6,9-heptadecadiene (C17:2) decreased in raw and irradiatedcooked samples during storage, but these were still detectable after 6 mo of storage. Merritt et al. (1978) also
reported long-term stability of radiolytic hydrocarbons.
Two hydrocarbons (8-heptadecene and 6,9-heptadecadiene) were found only in irradiated samples (Table
2). Other researchers (Spiegelberg et al., 1994; Lee et
al., 2008) also reported that 8-heptadecene (C17:1) and
6,9-heptadecadiene (C17:2) were found at high concentrations only in the irradiated chicken meat. Therefore,
8-heptadecene and 6,9-heptadecadiene could be used as
markers for irradiated chicken meat. 1-Hexadecene was
found not only in irradiated but also cooked chicken
meat. Thus, 1-hexadecene cannot be used as an irradiation marker for chicken meat.
New long-chain hydrocarbons could be produced
in vegetable oils (Nawar, 1977) and in animal prod-
2-Alkylcyclobutanones
Both DCB and TCB were found in all irradiated
chicken meat samples (Table 3). The concentration
Table 2. Concentration1 (µg/g of fat) of radiation-induced hydrocarbons in irradiated raw and cooked chicken meats during storage
at −40°C
Hydrocarbon
1-Tetradecene (C14:1)
Pentadecane (C15:0)
1-Hexadecene (C16:1)
6,9-Heptadecadiene (C17:2)
8-Heptadecene (C17:1)
n-Heptadecane (C17:0)
a–eMeans
0
6
0
6
0
6
0
6
0
6
0
6
Cooked before
irradiation
Raw meat
Storage
time
(mo)
0 kGy
2.15
0.51
0.54
± 0.81d,x
± 0.01d,y
± 0.02e,x
—2
—
—
—
—
—
—
5.03 ± 0.36a,x
4.49 ± 0.06a,x
5 kGy
8.39
5.69
3.92
2.63
21.63
15.76
3.65
1.77
5.22
3.96
2.29
0.60
±
±
±
±
±
±
±
±
±
±
±
±
0.52b,x
0.23b,y
0.31c,x
0.17b,y
0.58a,x
0.57a,y
0.85a,x
0.63b,x
0.74b,x
0.28b,x
0.62b,x
0.11d,y
0 kGy
4.04
1.43
1.67
0.65
3.36
1.14
0.08c,x
0.00c,y
0.25d,x
0.04c,y
0.05c,x
0.01d,y
±
±
±
±
±
±
—
—
—
—
2.52 ± 0.80b,x
1.90 ± 0.11c,x
5 kGy
10.46
8.39
7.47
4.77
6.52
5.51
4.39
4.35
6.99
6.44
3.66
3.39
within a row with different superscripts are significantly different (P < 0.05).
within a column and hydrocarbon with different superscripts are significantly different (P < 0.05).
1Values are mean ± SD; n = 3.
2Dash indicates not detected.
x,yMeans
Cooked after
irradiation
±
±
±
±
±
±
±
±
±
±
±
±
0.73a,x
0.35a,y
0.30a,x
0.67a,x
0.72b,x
0.17b,x
0.36a,x
0.28a,x
0.49a,x
0.06a,x
0.77b,x
0.20b,x
5 kGy
1.63
0.73
6.43
4.02
3.22
2.5
3.30
1.67
5.16
4.10
2.61
0.47
±
±
±
±
±
±
±
±
±
±
±
±
0.69d,x
0.26d,x
0.89b,x
0.67a,y
0.22c,x
0.83c,x
0.47a,x
0.20b,y
0.65b,x
0.29b,x
0.36b,x
0.19d,y
2582
Kwon et al.
Concentration1
Table 3.
storage at −40°C
Treatment
Raw meat
Cooked
before IR3
Cooked
after IR
(µg/g of fat) of radiation-induced 2-alkylcyclobutanones in irradiated raw and cooked chicken meats during
Irradiation
dose
(kGy)
2-Dodecylcyclobutanone
0 mo
2-(5′-Teradecenyl)
cyclobutanone
2-Tetradecylcyclobutanone
6 mo
0 mo
6 mo
0
5
0
—2
0.08 ± 0.01a,x
—
—
0.07 ± 0.01a,x
—
—
0.13 ± 0.03a,y
—
—
0.10 ± 0.06a,x
—
5
5
0.13 ± 0.13a,x
0.11 ± 0.01a,x
0.075 ± 0.02a,x
0.06 ± 0.02b,x
0.18 ± 0.01a,x
0.10 ± 0.03a,y
0.06 ± 0.05b,x
0.09 ± 0.01a,x
0 mo
6 mo
0.30 ±
0.34 ±
0.41 ±
0.01a,x
0.15a,x
0.11a,x
0.26 ± 0.03b,x
0.35 ± 0.02a,x
0.32 ± 0.06a,x
0.42 ± 0.01a,x
0.24 ± 0.11a,x
0.23 ± 0.11b,x
0.23 ± 0.08a,x
a,bMeans
within a row and compound with different superscripts are significantly different (P < 0.05).
within a column with different superscripts are significantly different (P < 0.05).
1Values are mean ± SD; µg/g of fat; n = 3.
2Dash indicates not detected.
3IR = irradiation.
x,yMeans
of DCB (derived from palmitic acid) was higher than
that of TCB (derived from stearic acid) because of the
relative concentrations of the parent fatty acids in the
samples (Kim et al., 2004). Obana et al. (2007) reported that the DCB concentration in gamma-irradiated beef (5.1 kGy) was about 0.45 μg/g of fat (0.068
mg/kg). Boyd et al. (1991) also found DCB only in
irradiated meats, and DCB and TCB were used as irradiation markers in liquid whole eggs (Stevenson et
al., 1993). Irradiation had little effect on concentration
of 2-(5′-teradecenyl) cyclobutanone, which was detected in nonirradiated samples. In irradiated raw meat
samples, the amounts of 2-alkylcyclobutanones showed
great stability during the storage. The concentration
of DCB and TCB decreased over time, but detectable
amounts of DCB and TCB remained in meat after 6 mo
of frozen storage.
Sulfur Volatile Compounds
Sulfur volatile compounds were detected only in irradiated meat samples, of which precooked samples
showed the highest amounts (Table 4). The results are
in agreement with those of Ahn et al. (2000) who reported that new volatiles produced after irradiation
were mainly sulfur compounds, of which dimethyl di-
sulfide was the highest. This compound was mainly
responsible for the sulfur odor and flavor detected in
irradiated meats during sensory evaluation (Zhu et al.,
2003). The changes in relative composition of sulfur
volatiles in meat during storage also affect the overall sensory characteristics of meat samples (Girard and
Durance, 2000). Sulfur volatiles in irradiated meats are
mainly dependent upon storage conditions and easily
disappear under aerobic storage conditions (Nam and
Ahn, 2003). In this study, only dimethyl disulfide exhibited long-term stability, showing the potential of using it as an irradiation detection marker for chicken
meat stored for 6 mo under oxygen-permeable packaging conditions.
Conclusions
Two hydrocarbons [8-heptadecene (C17:1) and
6,9-heptadecadiene (C17:2)] and two 2-alkylcyclobutanones (DCB and TCB) were detected only in irradiated
chicken meat samples regardless of cooking treatment.
Although the levels of hydrocarbons and 2-alkylcyclobutanone decreased during storage, 8-heptadecene,
6,9-heptadecadiene, 2-dodecylcyclobutanone, and 2-tetradecylcyclobutanone proved to be excellent irradiation
indicators for chicken meat samples. Precooked samples
Table 4. Concentration1 (total ion count × 104) of radiation-induced sulfur compounds in irradiated raw and cooked chicken meats
during storage at −40°C
Treatment
Raw meat
Cooked before irradiation
Cooked after irradiation
SEM
a–cMeans
Irradiation
dose
(kGy)
Dimethyl sulfide
Dimethyl disulfide
Dimethyl trisulfide
0 mo
0 mo
6 mo
0 mo
0
5
0
5
5
—2
—
—
3,443a
1,062b
156
—
—
—
12,027a
7,515b
830
—
723c
—
5,579a
3,428b
534
6 mo
—
—
—
—
—
—
within a column with different superscripts are significantly different (P < 0.05).
represent mean of 3 replications.
2Dash indicates not detected.
1Values
—
—
—
1,545a
673b
5
6 mo
—
—
—
—
—
—
RADIATION-INDUCED COMPOUNDS IN IRRADIATED CHICKEN MEAT
produced large amounts of sulfur volatiles by irradiation. However, only dimethyl disulfide was detectable
after 6 mo of storage under oxygen-permeable packaging conditions, indicating that it could be used as
an irradiation marker for frozen-stored cooked chicken
meat.
ACKNOWLEDGMENTS
This study was supported by the World Class University program (R31-10056) through the National Research Foundation of Korea funded by the Ministry of
Education, Science and Technology (South Korea).
REFERENCES
Ahn, D. U. 2002. Production of volatiles from amino acid homopolymers by irradiation. J. Food Sci. 67:2565–2570.
Ahn, D. U., C. Jo, and D. G. Olson. 2000. Analysis of volatile components and the sensory characteristics of irradiated raw pork.
Meat Sci. 54:209–215.
Ahn, D. U., K. C. Nam, M. Du, and C. Jo. 2001. Effect of irradiation and packaging conditions after cooking on the formation of
cholesterol and lipid oxidation products in meats during storage.
Meat Sci. 57:413–418.
Boyd, D. R., A. V. J. Crone, J. T. G. Hamilton, and M. V. Hand.
1991. Synthesis, characterization and potential use of 2-dodecylcyclobutanone as a marker for irradiated chicken. J. Agric. Food
Chem. 39:789–792.
Cleland, M. R. 2006. Advances in gamma ray, electron beam, and
X-ray technologies for food irradiation. Pages 11–35 in Food Irradiation Research and Technology. 1st ed. C. H. Sommers and
X. Fan, ed. Blackwell Publications, Ames, IA.
Delincée, H. 2002. Analytical methods to identify irradiated food—
A review. Rad. Phys. Chem. 63:455–458.
Enser, M. 1987. What is lipid oxidation? Food Sci. Technol. 1:151–
153.
Eustice, R. F., and C. M. Brubn. 2006. Consumers acceptance and
marketing of irradiated foods. Pages 63–84 in Food Irradiation
Research and Technology. 1st ed. C. H. Sommers and X. Fan, ed.
Blackwell Publications, Ames, IA.
Folch, J., M. Less, and G. M. Sloane-Stanley. 1957. A simple method
for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226:497–509.
Girard, B., and T. Durance. 2000. Headspace volatiles of sockeye and
pink salmon as affected by retort process. J. Food Sci. 65:34–39.
Gray, J. I. 1978. Measurement of lipid oxidation: A review. J. Am.
Oil Chem. Soc. 54:225–229.
Hau, L. B., M. H. Liew, and L. T. Yeh. 1992. Preservation of grass
prawns by ionizing irradiation. J. Food Prot. 55:198–202.
Kim, K. S., H. Y. Seo, J. M. Lee, E. R. Park, J. H. Kim, C. H. Hong,
and M. W. Byun. 2004. Analysis of radiation-induced hydrocarbons and 2-alkylcyclobutanones from dried shrimps (Penaeus
aztecus). J. Food Prot. 67:142–147.
Lee, J., T. Kausar, and J. H. Kwon. 2008. Characteristic hydrocarbons and 2-alkylcyclobutanones for detecting γ-irradiated sesame
seeds after steaming, roasting, and oil extraction. J. Agric. Food
Chem. 56:10391–10395.
Letellier, P. R., and W. W. Nawar. 1972. 2-Alkylcyclobutanones
from the radiolysis of triglycerides. Lipids 7:75–76.
Li, S. X., D. U. Ahn, G. Cherian, T. Y. Chung, and J. S. Sim. 1996.
Dietary oils and tocopherol supplementation on cholesterol oxide
2583
formation in freeze-dried chicken meat during storage. J. Food
Lipids 3:27–42.
Meier, W., and M. H. Stevenson. 1993. Determination of volatiles
and o-tyrosine in irradiated chicken. Results of an intercomparison study. Pages 221–218 in Recent Advances on the Detection
of Irradiated Food. Commission of the European Communities
Report EUR/14315/en. M. Leonardi, J. J. Raffi, and J. J. Belliardo, ed. BCR Information, Brussels, Luxembourg.
Merritt, C., P. Angelini, and R. A. Graham. 1978. Effect of radiation
parameters on the formation of radiolysis products in meat and
meat substances. J. Agric. Food Chem. 26:29–35.
Molins, R. A. 2001. Food Irradiation: Principles and Applications.
Wiley Interscience, New York, NY.
Nam, K. C., and D. U. Ahn. 2003. Combination of aerobic and vacuum packaging to control lipid oxidation and off-odor volatiles of
irradiated raw turkey breast. Meat Sci. 63:389–395.
Nawar, W. W. 1977. Radiation chemistry of lipids. Pages 21–26 in
Radiation Chemistry of Major Food Components. P. S. Elias and
A. J. Cohen, ed. Elsevier Science, Amsterdam, the Netherlands.
Nawar, W. W. 1986. Volatiles from food irradiation. Food Rev. Int.
2:45–78.
Noleau, I., and B. Toulemonde. 1987. Volatile components of roasted
chicken fat.  LWT—Food Sci. Technol. 20:37–41.
O’Connell, M. J., and A. Garner. 1983. Radiation-induced generation and properties of lipid hydroperoxide in liposomes. Int. J.
Radiat. Biol. Relat. Stud. Phys. Chem. Med. 44:615–625.
Obana, H., M. Furuta, and Y. Tanaka. 2007. Detection of irradiated meat, fish and their products by measuring 2-alkylcyclobutanones levels after frozen storage. Shokuhin Eiseigaku Zasshi
48:203–206.
Osterholm, M. T., and A. P. Norgan. 2004. The role of irradiation in
food safety. N. Engl. J. Med. 350:1898–1901.
Robertson, R. E., and J. Holly. 2000. Food Irradiation Available
Research Indicates that Benefits Outweigh Risks. Report to Congressional Requesters. United States General Accounting Office,
Washington, DC.
SAS Institute Inc. 1995. SAS/STAT User’s Guide. SAS Institute
Inc., Cary, NC.
Spiegelberg, A., G. Schulzki, N. Helle, K. W. Boegl, and G. A. Schreiber. 1994. Methods for routine control of irradiated food: Optimization of a method for detection of radiation-induced hydrocarbons and its application to various foods. Rad. Phys. Chem.
43:433–444.
Stevenson, M. H., A. V. J. Crone, J. T. G. Hamilton, and C. H.
McMurray. 1993. The use of 2-dodecylcyclobutanone for the identification of irradiated chicken meat and eggs. Rad. Phys. Chem.
42:363–366.
Stewart, E. M. 2001. An international collaborative blind trial using
2-dodecylcyclobutanone and 2-tetradecylcyclobutanone to detect
irradiated Camembert cheese, salmon, mango and papaya. Report to the Ministry of Agriculture, Fisheries and Food (MAFF),
London, UK.
Stewart, E. M., W. C. McRoberts, J. T. G. Hamilton, and W. D.
Graham. 2001. Isolation of lipid and 2-alkylcyclobutanones from
irradiated food by supercritical fluid extraction. J. AOAC Int.
84:976–986.
Stewart, E. M., S. Moore, W. D. Graham, W. C. McRoberts, and J.
T. G. Hamilton. 2000. 2-Alkylcyclobutanones as markers for the
detection of irradiated mango, papaya, Camembert cheese and
salmon meat. J. Sci. Food Agric. 80:121–130.
Thakur, B. R., and R. K. Singh. 1994. Food irradiation: Chemistry
and applications. Food Rev. Int. 10:437–473.
Zhu, M. J., E. J. Lee, A. Mendonca, and D. U. Ahn. 2003. Effect of
irradiation on the quality of turkey ham during storage. Meat
Sci. 66:63–68.