MEAT
SCIENCE
Meat Science 67 (2004) 643–649
www.elsevier.com/locate/meatsci
Temperature abuse affects the quality of irradiated pork loins
M.J. Zhu a, A. Mendonca b, D.U. Ahn
b
a,*
a
Department of Animal Science, Iowa State University, 2276 Kildee, Ames, IA 50011-3150, USA
Department of Food Science and Human Nutrition, Iowa State University, 2312 Food Science Building, Ames, IA 50011-3150, USA
Received 25 September 2003; accepted 9 January 2004
Abstract
The influence of temperature abuse on the quality of irradiated pork loins was investigated. Pork loins were obtained directly
from a local packing plant, sliced and vacuum-packaged. Pork loins were randomly separated into 3 groups, sliced, and assigned to
receive 0, 1.5, or 2.5 kGy electron-beam irradiation. Then, each chop was further cut into three equal pieces and assigned to three
temperature treatments: Trt I was placed in a refrigerator directly after irradiation; Trt II was left at room temperature for 3 h before
refrigeration; and Trt III was exposed at room temperature for 1 h three consecutive days with intermittent storage at 4 °C between
exposures. Before irradiation, each loin pieces were vacuum-packaged. Color, 2-thiobarbituric acid reactive substances (TBARS),
and volatiles were measured after 0, 14, 28 and 42 days of storage, and water-holding capacity and sensory characteristics of the
loins were measured after 0, 14 and 28 days of storage. Temperature abuse had no significant effect on color, oxidation, and volatiles
of irradiated pork loins. However, temperature abuse improved water-holding capacity of meat, which could be caused by the
accelerated hydrolysis of muscle proteins at higher temperature. Irradiation increased redness, sulfur contents in volatiles and offodor of pork loin. Off-odor and redness induced by irradiation sustained during storage. Among sulfur compounds, the content of
dimethyl disulfide decreased gradually while the level of thiourea remained relatively constant. Irradiation also increased water loss,
which might be related to the structural damage in membrane during irradiation. This study shows that temperature abuse has little
effect on the quality of irradiated pork.
Ó 2004 Elsevier Ltd. All rights reserved.
Keywords: Pork loin; Water-holding capacity; Color; Volatiles; Temperature fluctuation; Irradiation
1. Introduction
During large-scale distribution and handling of meat,
especially in export of meat to foreign markets, there are
numerous opportunities for meat to be temperature
abused. These opportunities include loading and unloading of meat at shipping ports and subsequent
transportation by trucks (refrigerated or unrefrigerated)
to retail outlets where the meat has to be unloaded again
and stacked for storage. Therefore, it is inevitable for
meat products to be exposed to fluctuating temperatures
during irradiation, transportation and subsequent storage, which may promote the growth of microorganism
*
Corresponding author. Tel.: +1-515-294-6595; fax: +1-515-2949143.
E-mail address: duahn@iastate.edu (D.U. Ahn).
0309-1740/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.meatsci.2004.01.005
including pathogens and accelerate quality changes in
meat (Labuza & Fu, 1995).
Reducing the incidence of foodborne pathogens and
decreasing the numbers of microorganisms in meat
products is a major objective of many meat processor in
the United States. Irradiation is an attractive method to
eliminate pathogens in meat products, but changes color
and generates irradiation off-odor (Ahn, Jo, & Olson,
2000). In order to minimize quality change, low irradiation dosage is frequently used in meat processing. The
bacteriocidal action of ionizing irradiation is largely
linked to damage of bacterial DNA from the production
of free radicals during the irradiation process some bacteria in meat products can repair the damage, and recover
and proliferate during product transport and storage,
especially during temperature abuse (Lee, Sebranek,
Olson, & Dickson, 1996). Lucht, Blank, and Borsa (1998)
demonstrated that a temperature of 14–22 °C is optimal
for the recovery of irradiation-injured pathogens.
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M.J. Zhu et al. / Meat Science 67 (2004) 643–649
Our study showed that the temperature abuse greatly
accelerated the growth of Listeria monocytogenesis in
ready-to-eat turkey meat products (Bisha, Mendonca,
Sebranek, & Dickson, 2003). Apart from the proliferation of microorganisms in meat, fluctuating temperature
accelerates a number of enzymatic and chemical reactions that can influence the shelf life of irradiated meat.
Exposure of meat to increased temperature conditions
undoubtedly accelerates proteases activity to breakdown
muscle protein into small molecular weight peptides,
and long term storage of meat is often associated with
extensive softening of meat and color change independent of microorganism (Gill, 1996; Tewari, Jayas, &
Holley, 1999). Lipid oxidation may also be accelerated
under the elevated temperature conditions. However, no
information on quality changes in irradiated meat by
temperature abuse is currently available. Since two most
frequent temperature abuses are delay at room temperature after irradiation and temperature fluctuation
during transporting products from one location to another, meats were treated with a 3-h exposure to room
temperature after irradiation and 1 h per day for three
consecutive days of exposure to room temperature to
simulate temperature fluctuation conditions in industry.
To avoid the quality changes caused by microbial
growth, the pork loins used in this study were directly
purchased from a local packing plant where loins were
dissected under strict hygiene conditions. A great care
was taken to avoid microbial contamination during
transportation and further packing. The objective of this
study was to determine the effect of temperature fluctuation on the quality of irradiated pork loins.
2. Materials and methods
III) were exposed at room temperature for 1 h three
consecutive days with intermittent storage at 4 °C between exposures. In each step of meat handling, care
was taken to avoid microbial contamination.
Loin pieces were vacuum-packaged individually in
low oxygen-permeable bags (nylon/polyethylene, 9.3 mL
O2 /m2 /24 h at 0 C; Koch, Kansas City, MO) before irradiation. The energy and power level used for irradiation were 10 MeV and 10 kW, respectively, and the
average dose rate was 88.3 kGy/min. To confirm the
target dose, 2 alanine dosimeters per cart were attached
on the top and bottom surface of a sample. The alanine
dosimeter was read using a 104 Electron Paramagnetic
Resonance Instrument (Bruker Instruments Inc., Billerica, MA, USA). The range of actual dosage for
1.5 kGy was 1.414–1.810 kGy and the range for 2.5 kGy
was 2.34–3.12 kGy. Color, volatiles and lipid oxidation
were analyzed after 0, 14, 28 and 42 days of storage, and
water-holding capacity and sensory characteristics were
evaluated after 0, 14, and 28 days of storage.
2.2. Water-holding capacity
Measurement of water-holding capacity was performed by centrifugation method (Bertram, Andersen,
& Karlsson, 2001). Samples were cut parallel to the
muscle fiber direction, which is about 2.0 cm long and
0.5 0.2 cm in cross-sectional area. The samples were
weighed and placed in test tubes with a filter paper
(Whatman No. 1) cushion. The tube was sealed with
parafilm then centrifuged at 400g at 4 °C for 60 min.
After centrifugation the sample were weighed again.
Water-holding capacity was calculated as the percentage
of the difference in weight before and after centrifugation. Two meat samples were taken from each loin piece
and the average data was used for statistical analysis.
2.1. Sample preparation
2.3. Color measurement
Twelve pork loins fabricated under strict hygienic
conditions were obtained directly from a local packing
plant. Chops from three different loins were pooled and
used as one replication. The upper portion of each loin
was sliced into 2.5-cm thick chops for water-holding
capacity measurement. The rest was sliced to 1.0-cmthick chops and the chops were used for color, volatiles
and 2-thiobarbituric acid reactive substances (TBARS)
assays. Chops within each replication were randomly
separated into three groups, and each group was
assigned to receive 0, 1.5, or 2.5 kGy electron-beam
irradiation using a Linear Accelerator (Circe IIIR;
Thomson CSF Linac, Saint-Aubin, France). Each chop
within a group was further cut into three equal pieces to
make three sub-groups: one sub-group were refrigerated
(4 °C) immediately after irradiation (Trt I); another subgroup was kept at room temperature (22 °C) for 3 h
before refrigeration (Trt II); and the last sub-group (Trt
The surface color of sliced pork loins was measured
in package using a Hunter LabScan Colorimeter
(Hunter Laboratory, Inc., Reston, VA) that had been
calibrated against black and white reference tiles covered with the same packaging materials as used for
samples. The CIE L (lightness), a (redness), and b
(yellowness) values were obtained using an illuminant A
(light source). Two color readings were taken from each
side of a sliced loin.
2.4. 2-Thiobarbituric acid reactive substances measurement
Five grams of minced loin were weighed into a 40-mL
test tube and homogenized with 50 lL butylated hydroxyanisole (7.2%) and 15 mL of deionized distilled
water (DDW) using a Polytron homogenizer (Type PT
M.J. Zhu et al. / Meat Science 67 (2004) 643–649
10/35, Brinkman Instruments Inc., Westbury NY, USA)
for 15 s at high speed. One milliliter of the meat homogenate was transferred to a disposable test tube
(13 100 mm) and then thiobarbituric acid/trichloroacetic acid (15 mM TBA/15% TCA, 2 mL) was added.
The mixture was vortex mixed and incubated in a boiling water bath for 15 min to develop color. The sample
was cooled in cold water for 10 min, mixed again using a
vortex mixer, and centrifuged for 15 min at 2500g at
4 °C. The absorbance of the resulting supernatant
solution was determined at 531 nm against a blank
containing 1 mL of DDW and 2 mL of TBA/TCA
solution. The amounts of TBARS were expressed as
milligrams of malonaldehyde per kilogram of meat.
2.5. Volatiles analysis
A purge-and-trap dynamic headspace GC/MS system
was used to identify and quantify the volatiles compounds. Three grams of minced loin meat was put in a
40-mL sample vial and flushed with helium gas
(99.999%). After capping with a Teflon-lined, openmouth cap, the vial was placed in a refrigerated (4 °C)
sample tray. Samples were purged at 40 °C with helium
gas (40 mL/min) for 11 min. Volatiles were trapped with
a Tenax/charcoal/silica trap column at 20 °C, desorbed
for 2 min at 220 °C, concentrated using a cryofocusing
unit at –90 °C, then desorbed into a GC column for 60 s
at 220 °C. An HP-624 column (15 m, 250 lm i.d., 1.4 lm
nominal), an HP-1 column (60 m, 250 lm i.d., 0.25 lm
nominal), and an HP-Wax column (7.5 m, 250 lm i.d.,
0.25 lm nominal) were combined using zero-volume
connectors and used for volatiles analysis. A ramped
oven temperature was used: the initial oven temperature
was set at 0 °C for 2.5 min, then increased to 10 °C at 5
°C/min, to 45 °C at 10 °C/min, to 110 °C at 20 °C/min,
to 210 °C at 10 °C/min, and held for 2.5 min. Liquid
nitrogen was used to cool the oven below ambient
temperature. Helium was the carrier gas at constant
pressure of 22 psi. A mass selective detector (MSD) was
used to identify and quantify volatiles compounds in
irradiated samples. The ionization potential of MS will
be 70 eV, scan range was between 19.1 and 350 m=z. The
identification of volatiles was achieved by comparing
mass spectral data with those of the Wiley Library. The
peak area was reported as the amount of volatiles released (Ahn, Jo, Du, Olson, & Nam, 2000).
2.6. Sensory evaluation
sensory characteristics and was assigned a score ranging
from 1 (none) to 9 (extremely strong), respectively. All
samples were labeled with random three-digit numbers
and presented randomly to panelists.
2.7. Statistical analysis
A split-plot design was used in this study. Chops from
different loins were first split into three irradiation dosages, and then individual chops were cut into three
pieces and assigned to three temperature treatments.
Data were processed by the general linear model (GLM)
of statistical analysis system (SAS, 2000). The differences
in the mean values were compared by the Tukey’s
multiple range test, and mean values and standard error
of the means (SEM) were reported (P < 0:05).
3. Results and discussion
3.1. Water-holding capacity
Water-holding capacity is an important quality
characteristic of pork loins. These results demonstrated
that irradiation significantly increased the loss of water
from loins (Table 1). For the control samples with no
temperature abuse (Trt I), both irradiation at 1.5 and
Table 1
Water-holding capacity influenced by irradiation and treatments of
pork loins
Characteristics
Trt I
Trt II
Trt III
0 kGy
1.5 kGy
2.5 kGy
0 day
8.1b
11.3a
10.9a
8.9b
10.2a
10.0a
–
–
–
SEM
0.9
0.9
–
0 kGy
1.5 kGy
2.5 kGy
14 day
8.1bx
9.0ab
10.2ax
8.6x
10.0
9.9x
6.4y
8.6
6.8y
0.5
0.9
0.8
SEM
0.5
0.6
0.4
2.3
0 kGy
1.5 kGy
2.5 kGy
28 day
5.7b
6.4ab
8.0ax
7.4
6.9
6.2y
6.0
6.3
6.4y
0.6
0.7
0.4
SEM
0.6
0.6
0.6
x;y
Twelve trained sensory panelists characterized the
smell of irradiated loins under different temperature
fluctuation. Panelists were trained to familiarize with
irradiation odor, the scale to be used, and the range of
intensities likely to be encountered during the study.
A 9-point category scale was used to describe the
645
SEM
0.5
1.2
0.9
Means within a row with different superscript differ significantly
ðP < 0:05Þ; n ¼ 4.
a–c
Means within a column with different superscript differ significantly
(P < 0:05).
Trt I, refrigerated immediately after irradiation; Trt II, kept at
room temperature for 3 h before refrigerated storage; Trt III, were
exposed at room temperature for 1 h at three consecutive days with
intermittent storage at 4 °C between exposures.
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M.J. Zhu et al. / Meat Science 67 (2004) 643–649
2.5 kGy significantly increased centrifugation loss
compared to that of non-irradiated samples. This result
is in agreement with a previous report about increased
centrifugation loss and reduced water-holding capacity
of pork chops after irradiation (Zhao & Sebranek,
1996). The mechanism for irradiation-induced centrifugation loss in pork loins is not clear, but two possible
theories exist: (1) irradiation may damage the integrity
of membrane structure of muscle fibers (Lakritz, Carroll, Jenkins, & Maerker, 1987) and (2) irradiation may
denature the muscle proteins, thus lowering waterholding capacity (Lynch, Macfie, & Mead, 1991). After
14 days of refrigerated storage, samples from three
consecutive days of exposure to room temperature (Trt
III) had lower centrifugation loss than other treatments
(Table 1). Since the meat used in this study is at postrigor stage, the water-holding capacity of meat is gradually improving during storage due to hydrolysis of
muscle proteins. Therefore, the improved water-holding
capacity observed in this study could be due to accelerated hydrolysis of proteins during temperature abuse,
since high temperature increases protease activity (DeTable 2
Color a of pork loin effected by irradiation and treatments after
storage
Irradiation dose
Trt I
Trt II
Trt III
0 kGy
1.5 kGy
2.5 kGy
0 day
13.0b
14.6a
15.2ay
13.2c
14.3b
15.6ax
–
–
–
SEM
0.4
0.2
–
0 kGy
1.5 kGy
2.5 kGy
14 day
12.8b
15.1ax
15.9a
12.6c
14.1by
16.8a
12.5c
14.5bxy
15.9a
SEM
0.3
0.3
0.4
0 kGy
1.5 kGy
2.5 kGy
28 day
14.4b
15.5a
16.2a
14.6b
15.5a
15.9a
13.3b
16.1a
16.3a
SEM
0.3
0.2
0.4
0 kGy
1.5 kGy
2.5 kGy
42 day
–
14.9b
16.1a
–
15.3
16.0
–
14.7b
16.3a
SEM
0.3
0.4
0.2
a–c
SEM
0.4
0.2
0.1
0.3
0.2
0.3
0.4
0.3
0.3
–
0.3
0.3
Means within a column with different superscript differ significantly
ðP < 0:05Þ; n ¼ 4.
x;y
Means within a row with different superscript differ significantly
ðP < 0:05Þ.
Trt I, refrigerated immediately after irradiation; Trt II, kept at
room temperature for 3 h before refrigerated storage; Trt III, were
exposed at room temperature for 1 h at three consecutive days with
intermittent storage at 4 °C between exposures.
vine, Wahlgren, & Tornberg, 1999). During storage,
water-holding capacity increased for all loins with various irradiation doses and temperature treatments (Table 1). This may also be due to the hydrolysis of muscle
proteins during storage, a continuation of the postmortem changes in muscle (Koohmaraie, 1994).
3.2. Color values and TBARS values
As shown in Table 2, irradiated samples have higher
redness (a value) than control samples, which is in
agreement with the previous results (Ahn et al., 2000).
Temperature abuse had no effect on the redness of pork
loin. No significant changes in redness occurred during
storage. As for lightness (L value) and yellowness
(b value), no changes were observed for both temperature abuses and during storage (data not shown).
Overall, the temperature fluctuations had no effect on
the color values of irradiated pork loins. Temperature
fluctuation, irradiation and storage had little influence
on TBARS of pork loins (data not shown). Minimal
irradiation and temperature fluctuation effects on
TBARS were expected because the loin chops were
vacuumed packaged.
Table 3
Irradiation off-odor as influenced by irradiation and treatments of
pork loins
Irradiation dose
Trt I
Trt II
Trt III
0 kGy
1.5 kGy
2.5 kGy
0 day
1.5b
5.7a
6.0a
1.4b
6.2a
7.0a
–
–
–
SEM
0.4
0.5
–
0 kGy
1.5 kGy
2.5 kGy
14 day
1.3b
6.9a
7.1a
1.5c
5.6b
7.6a
1.7b
6.8a
7.3a
SEM
0.4
0.3
0.5
0 kGy
1.5 kGy
2.5 kGy
28 day
1.4c
6.2b
7.3a
1.2b
5.4a
6.3a
1.7b
4.7a
5.7a
SEM
0.4
0.5
0.6
a;b
SEM
0.3
0.6
0.6
0.3
0.4
0.5
0.4
0.5
0.6
Means within a row with different superscript differ significantly
ðP < 0:05Þ; n ¼ 12.
Trt I, refrigerated immediately after irradiation; Trt II, kept at
room temperature for 3 h before refrigerated storage; Trt III, were
exposed at room temperature for 1 h at three consecutive days with
intermittent storage at 4 °C between exposures.
Twelve trained sensory panelists characterized the smell of irradiated loins stored under different temperature conditions. A 9-point
category scale was used to describe the sensory characteristics and was
assigned a score ranging from 1 (none) to 9 (extremely strong), respectively.
M.J. Zhu et al. / Meat Science 67 (2004) 643–649
50
45
40
35
30
25
20
15
10
5
0
Thiourea contentin volatiles of 0 kGy
irradiated prok loins
10000
Trt 1
Trt 2
Trt 3
0
14
28
Thiourea content (x10 4)
Ion counts (x10000)
Dimethyl disulfide in volatiles of 0 kGy
irradiated pork loins
42
Trt 1
8000
Trt 2
6000
Trt 3
4000
2000
0
-2000
0
Storage (days)
trt1
7000
6000
5000
Trt 2
Trt 3
4000
3000
2000
2000
0
0
14
28
28
42
Thiourea content in volatiles of 2 kGy
irradiated pork loins
30000
Thiourea content (x10 4)
9000
8000
14
Storage (day)
Dimethyl disulfide in volatiles of 1.5 kGy
irradiated pork loins
Ion counts (x10000)
647
Trt 1
25000
Trt 2
20000
Trt 3
15000
10000
5000
0
42
0
Storage (days)
14
28
42
Storage (day)
20000
18000
16000
14000
12000
10000
8000
6000
4000
2000
0
Thiourea content involatiles of 3 kGy
irradiated prokloins
Trt 1
Trt 2
Trt 3
0
14
28
42
Storage (days)
Fig. 1. Effects of temperature fluctuation and storage on dimethyl
disulfide contents (104 counts) in volatiles of pork loins under
different irradiation conditions. Trt I, pork loins were refrigerated (4
°C) immediately after irradiation; Trt II, irradiated pork loins were
kept at room temperature (22 °C) for 3 h before refrigeration; Trt III,
after irradiation, pork loins were exposed at room temperature for 1
h three consecutive days with intermittent storage at 4 °C between
exposures. Pork chops were irradiated at 0, 1.5 or 2.5 kGy. Volatiles
were analyzed after storage at 4 °C for 0, 14, 28, and 42 days. A
purge-and-trap dynamic headspace GC/MS system was used to
identify and quantify the volatiles compounds. A mass selective detector (MSD) was used to identify and quantify volatiles compounds
in irradiated samples. The identification of volatiles was achieved by
comparing mass spectral data with those of the Wiley Library. The
peak area (104 ion counts) was reported as the amount of volatiles
released (n ¼ 4).
60000
Thiourea content (x10 4)
Ion counts (x10000)
Dimethyl disulfide involatilesof 2.5 kGy
irradiated porkloins
Trt 1
50000
Trt 2
40000
Trt 3
30000
20000
10000
0
0
14
28
42
Storage (day)
Fig. 2. Effects of temperature fluctuation during storage on thiourea
content (104 counts) in irradiated pork loins. Trt I, pork loins were
refrigerated (4 °C) immediately after irradiation; Trt II, irradiated pork
loins were kept at room temperature (22 °C) for 3 h before refrigeration;
Trt III, after irradiation, pork loins were exposed at room temperature
for 1 h three consecutive days with intermittent storage at 4 °C between
exposures. Pork chops were irradiated at 0, 1.5 or 2.5 kGy. Volatiles
were analyzed after storage at 4 °C for 0, 14, 28, and 42 days. A purgeand-trap dynamic headspace GC/MS system was used to identify and
quantify the volatiles compounds. A mass selective detector (MSD) was
used to identify and quantify volatiles compounds in irradiated samples. The identification of volatiles was achieved by comparing mass
spectral data with those of the Wiley Library. The peak area (104 ion
counts) was reported as the amount of volatiles released (n ¼ 4).
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M.J. Zhu et al. / Meat Science 67 (2004) 643–649
3.3. Sensory evaluation and volatiles analysis
Irradiation induced strong off-odor (Table 3). After
irradiation, off-odor intensity increased from around 1.5
points to above 5 points on a 9-point scale. This irradiation off-odor was a pungent, cooked corn like odor
that has been reported in previous research (Ahn et al.,
2000; Du, Hur, & Ahn, 2002). Temperature fluctuation
and storage had no significant effect on irradiation
off-odor (Table 3).
Irradiation induces sulfur-containing volatiles, which
are the main compounds for irradiation off-odor (Du
et al., 2002; Kim, Nam, & Ahn, 2002). Dimethyl disulfide was almost undetectable in non-irradiated samples,
but the amount of dimethyl disulfide dramatically increased after irradiation (Fig. 1). During storage, the
content of dimethyl disulfide gradually reduced and
became barely detectable after 28 days of storage
(Fig. 1). This suggested that dimethyl disulfide might not
be the only sulfur volatile contributing to irradiation offodor because strong irradiation off-odor was still apparent by sensory panelists after 28 days of storage
(Table 3). However, no significant amounts of other
sulfur volatiles were detected in this study. In another
study, dimethyl disulfide content was shown constant in
volatiles of irradiated vacuum-packaged pork during
storage (Ahn, Nam, Du, & Jo, 2001).
Irradiation odor seems to be more related to thiourea
content in volatiles than other sulfur compounds
(Fig. 2). After 42 days of storage, significant amounts of
thiourea still remained in meat. This result was in
agreement with the sensory data where a sulfur-like offodor was noted (Table 3). Thiourea content in volatiles
enhanced greatly by irradiation, and increased slightly
after 14 days refrigerated storage before decreasing at
42 days of storage (Fig. 2). There was no overall difference in thiourea content among different temperature
fluctuation. Combining with sensory evaluation data,
this result showed that temperature abuse did not
influence the irradiation off-odor of pork loins.
4. Conclusion
Mild temperature fluctuation had minor effect on
color, oxidation, and volatiles of irradiated pork loins.
However, temperature fluctuation improved waterholding capacity of meat. Irradiation increased redness,
sulfur contents in volatiles and off-odor of pork loins.
During storage, the content of dimethyl disulfide decreased gradually while the level of thiourea remained
relatively constant. Irradiation also increased centrifugation loss that was partly reversed during refrigerated
storage, which could be due to the hydrolysis of muscle
proteins. This result shows that the quality changes induced by temperature abuse are not a major concern.
However, temperature abuse is expected to promote
recovery and proliferation of bacteria in irradiated
meats and extensive microbial growth can affect the
quality of meat, when meats with poor hygienic conditions are used.
Acknowledgements
The research was supported by the Midwest Poultry
Consortium. The NASA FTCSC has funded the purchase of the Solartek 72 Multimatrix-Vial Autosampler
used for the volatile analysis in this study.
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