Meat Science 51 (1999) 355±361
Lipid oxidation, color changes and volatiles production in irradiated
pork sausage with di€erent fat content and packaging during
storage$
C. Jo, J.I. Lee, D.U. Ahn*
Department of Animal Science, Iowa State University, Ames, IA 50011-3150, USA
Abstract
E€ects of irradiation on lipid oxidation, color and volatiles production in pork sausages with di€erent fat content and packaging
were determined. Sausages (with 4.7, 10.5 and 15.8% fat content) were sliced and vacuum-packaged either in oxygen-permeable or
impermeable bags, irradiated (0 or 4.5 kGy) and stored at 4 C for 7 days. Lipid oxidation, color and volatiles productions were
analyzed at 0, 3 and 7 days of storage. TBARS (2-thiobarbituric acid reactive substances) values of cooked pork sausages increased
with the increase of fat content regardless of storage, irradiation or packaging types. Irradiated samples had higher TBARS than
nonirradiated at 0 day but the di€erence disappeared during storage in both packaging types. Lightness of sausages (Hunter Lvalue) increased with the increase of fat content and storage time but was not a€ected by irradiation. In aerobic packaging, irradiation reduced Hunter a-values of pork sausages at 0 day but irradiation e€ect on a-value disappeared during storage. In vacuum
packaging, however, irradiated samples had higher Hunter a-values than nonirradiated samples. Irradiation increased 1-heptene
and total volatiles, but the amount of 1-heptene was not associated well with TBARS values of pork sausages. In both irradiated
and nonirradiated pork sausages, aerobic packaging produced more volatiles than vacuum packaging during storage. It was concluded that irradiation and fat content had signi®cant e€ects on lipid oxidation, color and volatiles production of cooked pork
sausages during storage but that oxygen availability had a stronger e€ect than irradiation and fat content. # 1999 Elsevier Science
Ltd. All rights reserved.
1. Introduction
Low-dose (<10 kGy) irradiation can kill at least
99.9% of salmonella in poultry and an even higher percentage of Escherichia coli 0157:H7 (Olson, 1998). But,
irradiation is known to generate hydroxyl radicals that
can initiate chain reactions of lipid oxidation in aqueous
and oil emulsion systems. Irradiation could produce a
large amount of hydroxyl radicals in meat because over
75% of muscle cells are composed of water (Thakur &
Singh, 1994). Thayer, Boyd, and Jenkins (1993) reported
that irradiation-induced chemical changes are dose
dependent and the generation of characteristic o€-odor
and color changes in meat is almost instantaneous after
irradiation. Both raw and cooked meats produce o€-odor
after irradiation but the sources and mechanisms of o€odor production in irradiated meats are not yet known.
* Corresponding author. Tel.: +1-515-294-6595; fax: +1-515-2942401; e-mail: duahn@iastate.edu
$
Journal paper no. J-17966 of the IA Agriculture and Home Economics Experiment Station, Ames, Iowa 50011-3150, USA. Project
no. 3322, and supported by Hatch Act and the Food Safety Consortium.
Ahn et al. (1998b) observed that aerobic-packaged
irradiated raw pork had signi®cantly higher TBARS
values than those of control. Less stable displays of
color were noted for samples irradiated in aerobic
packaging (Luchsinger et al., 1996). Akamittath,
Brekke, and Schanus (1990) suggested that discoloration and lipid oxidation are interrelated and pigment
oxidation may catalyze lipid oxidation. However, irradiation had no detrimental e€ects on the color or ¯avor
of cured meat with nitrite or a nitrite-free curing system.
Polyphosphates had a bene®cial e€ect on lipid oxidation
but a detrimental e€ect on color stability in irradiated
meat (Shahidi, Pegg, & Shamsuzzaman, 1991).
Lynch, Mac®e, and Mead (1991) reported that irradiated turkey breast ®llets produced unpleasant odor
notes when stored in oxygen-impermeable ®lm and the
odor notes were di€erent from those developed from
corresponding nonirradiated samples. Heath, Owens,
Tesch, and Hannah (1990) and Hashim, Resurreccion,
and MacWatters, (1995) also showed that irradiating
uncooked chicken meat produced a characteristic
bloody and sweet aroma that remained after the meat
was cooked. Reineccius (1979) suggested that carbonyl
compounds are important for irradiation odor and that
0309-1740/99/$Ðsee front matter # 1999 Elsevier Science Ltd. All rights reserved
PII: S0309 -1 740(98)00134 -X
356
C. Jo et al./Meat Science 51 (1999) 355±361
Table 1
E€ect of fat content and irradiation on lipid oxidation of cooked pork sausages with di€erent packaging a
Fat content
0 day
0 kGy
Aerobic packaging
(%)
4.7
10.5
15.8
SEM
Vacuum packaging
(%)
4.7
10.5
15.8
SEM
a
b
c
d
4.5 kGy
3 day
SEM
0 kGy
4.5 kGy
7 day
SEM
0 kGy
4.5 kGy
SEMb
mg Malondialdehyde equivalents/kg Meat
1.6
1.6 bc
1.8 b
0.07
1.8
2.2 a
2.2 a
0.07
0.08
0.07
0.07
±
3.3 d
5.1 c
4.4 c
0.36
3.9 d
4.9 c
4.4 c
0.17
0.41
0.11
0.18
±
6.6
6.5
5.9
0.30
5.8
5.9
5.7
0.35
0.21
0.21
0.44
±
1.1 dd
1.4 bc
1.5 bc
0.04
1.2
1.6 ac
1.7 ac
0.04
0.05
0.04
0.03
±
1.2 e
1.5 d
1.7 c
0.04
1.3 e
1.6 d
1.8 c
0.04
0.04
0.04
0.05
±
1.4 d
1.6 c
1.7 ac
0.05
1.2
1.6
1.5 b
0.10
0.12
0.03
0.05
±
Irradiated at 0 or 4.5 kGy dose. n=4.
SEM: standard error of mean.
Di€erent letters within a row are signi®cantly di€erent ( p < 0.05).
Di€erent letters within a column are signi®cantly di€erent ( p < 0.05).
Fig. 1. Color changes of cooked pork sausages with aerobic packaging during storage (&), nonirradiated pork sausage with 0% fat added; (^),
nonirradiated pork sausage with 10% fat added; (*), nonirradiated pork sausage with 20% fat added; (&), irradiated pork sausage with 0% fat
added; (^), irradiated pork sausage with 10% fat added; (*), irradiated pork sausage with 20% fat added). a±c Di€erent letters within a storage
day are signi®cantly di€erent ( p < 0.05). NonIR, nonirradiated; IR, irradiated.
C. Jo et al./Meat Science 51 (1999) 355±361
357
Fig. 2. Color changes of cooked pork sausages with vacuum packaging during storage (&), nonirradiated pork sausage with 0% fat added; (^),
nonirradiated pork sausage with 10% fat added; (*), nonirradiated pork sausage with 20% fat added; (&), irradiated pork sausage with 0% fat
added; (^), irradiated pork sausage with 10% fat added; (*), irradiated pork sausage with 20% fat added). a±c Di€erent letters within a storage
day are signi®cantly di€erent ( p < 0.05). NonIR, nonirradiated; IR, irradiated.
Table 2
E€ect of fat content on the production of volatiles in irradiated aerobic-packaged pork sausages after 0 day of storage at 4 C a
Volatiles
1-heptene
Propanal
2-methylpropanal
2-methylbutanal
Pentanal
3-pentanone
Hexanal
1-butanol
1-pentanol
Nonanal
Decanal
1-heptanol
Aldehydes + ketones
Alcohols
Total volatiles
a
b
c
d
Nonirradiated
4.7%
10.5%
15.8%
1.0 b
9.6 c
19.8
16.8
25.7
98.6 a
157.8
7.8
11.7
1.0
nd d
1.0
329.1
20.5
350.5
5.6 a
12.7 b
14.1
21.0
27.5
81.7 ab
141.2
5.1
12.5
1.0
nd
1.0
299.2
18.6
323.4
9.0 a
17.6 a
17.8
12.7
25.2
54.5 b
157.6
4.5
13.0
1.0
nd
1.0
286.5
18.4
313.9
Irradiated at 0 or 4.5 kGy dose.
SEM: standard error of mean.
Di€erent letters within a row are signi®cantly di€erent ( p < 0.05). n =12.
nd: n=Not detected.
Irradiated
SEMb
4.7%
Area (pA s)
1.1
57.8
0.9
15.7 c
1.7
24.6
3.3
32.4
2.5
30.9
9.9
107.7 a
7.7
201.4 a
1.4
6.2
0.5
15.1 a
ÿ
6.2 a
ÿ
0.8
ÿ
1.0
16.6
419.5 a
1.5
22.3 a
17.2
499.6 a
10.5%
15.8%
SEM
44.0
20.5b
32.7
26.4
32.5
61.8 b
177.0 ab
7.4
14.8 a
3.3 b
nd
0.5
354.2 b
22.3 a
420.5 b
60.2
26.0 a
23.6
28.5
34.3
47.2 b
144.6 b
5.1
10.1 b
1.0 b
nd
0.3
305.2 b
15.4 b
380.8 b
6.0
1.5
3.6
2.5
3.0
11.9
13.0
1.4
1.0
0.8
0.1
0.2
19.3
1.6
22.6
358
C. Jo et al./Meat Science 51 (1999) 355±361
O2/m2/24 h at 0 C; Koch, Kansas City, MO) and stored
in a 4 C refrigerator overnight. Irradiation was conducted the next day at 0 or 4.5 kGy dose (97 kGy/min)
using a Linear Accelerator (Circe IIIR, Thomson CSF
Linac, France). For the aerobic packaging treatment,
vacuum packaging bags were opened before irradiation.
Samples were stored in a 4 C refrigerator immediately
after irradiation and 0-day samples were analyzed 3 h
after storage.
the intensity of irradiation odor is dependent upon
oxygen content during irradiation. El Magoli, Laroia,
and Hansen (1996) indicated that 2-butanone, 2-pentanone and 3-hydroxy-2-butanone increased with the
increase of fat content from 11 to 22% in beef patties,
and Ahn et al. (1998b) reported that propanal, pentanal, hexanal, 1-pentanol and total volatiles correlated
highly ( p < 0.01) with TBARS values of cooked meat.
Although lipid is the most important substance for
quality changes in meat, the e€ect of fat content on the
development of lipid oxidation, color changes and
volatiles production in irradiated meat is limited.
The objective of the present research was to determine
the in¯uence of irradiation on lipid oxidation, color
change and volatile production in cooked pork sausages
with di€erent fat content and packaging during storage.
2.2. Measurements of lipid oxidation, color and fat
content
Lipid oxidation was determined using a spectrophotometer (Gilford Instrument Laboratories, Oberlin,
OH) as described in detail by Jo and Ahn (1998a).
TBARS values were expressed as mg malondialdehyde
(MDA) equivalents per kg meat. A CIE Lab color
[lightness (L), redness (a) and yellowness (b)] of sausages
was measured using a Hunter Colorimeter (Hunter
Associates Laboratories, Reston, VA). Total fat content
was determined by the Folch's extraction method
(Folch, Less, & Sloane-Stanley, 1957).
2. Materials and methods
2.1. Sample preparation
Lean pork was obtained from a local packer and
ground twice through a 9-mm plate. Pork sausages batters were prepared with the lean ground meat, back fat
(0, 10 or 20% of meat weight), NaCl (2%) and ice water
(10%). The batters were stu€ed into cellulose casings (3
cm thickness) and cooked in a smoking chamber to an
internal temperature of 72 C. After cooling by a cold
water shower, the sausages were sliced to 2 cm-thick
pieces (approximately 30 g), vacuum-packaged into
oxygen-impermeable nylon/polyethylene bags (9.3 ml
2.3. Volatiles analysis
Precept II and a Purge-and-Trap concentrator
(Model 3000, Tekmar-Dohrmann, Cincinnati, OH)
were used to purge and trap volatiles, and a gas chromatography (GC) (Hewlett Packard, Model 6890, Wilmington, DE) equipped with a ¯ame ionization detector
(FID) was used to analyze volatiles from pork sausages.
Table 3
E€ect of fat content on the production of volatiles in irradiated vacuum-packaged pork sausages after 0 day of storage at 4 C a
Volatiles
1-heptene
Propanal
2-methylpropanal
2-methylbutanal
Pentanal
3-pentanone
Hexanal
1-butanol
1-pentanol
Nonanal
Decanal
1-heptanol
Aldehydes + ketones
Alcohols
Total volatiles
a
b
c
d
Non irradiated
4.7%
10.5%
15.8%
4.1
12.1
13.8
17.4
24.5
73.3
136.3
2.4
12.0
1.0
nd d
1.0
303.3
15.4
297.8 bc
6.3
13.7
15.7
18.5
27.0
75.4
156.3
2.3
13.5
1.0
nd
1.0
307.6
16.8
331.1 a
8.2
16.1
13.0
17.1
26.3
72.2
143.2
6.2
10.1
1.0
nd
1.0
288.8
17.3
314.3 ab
Irradiated at 0 or 4.5 kGy dose.
SEM: standard error of mean.
Di€erent letters within a row are signi®cantly di€erent ( p < 0.05). n=12.
nd: not detected.
Irradiated
SEMb
4.7%
Area (pA s)
1.3
59.3
1.1
17.6 b
0.7
17.8
2.4
25.8
1.4
26.1 b
6.2
55.1
8.1
224.9 a
1.5
7.6
1.5
14.1 a
ÿ
6.8 a
ÿ
nd
ÿ
nd
15.2
374.2 a
1.7
22.6 a
8.2
456.1 a
10.5%
15.8%
SEMb
63.8
22.2 a
18.0
32.1
33.6 a
55.4
171.9 b
5.6
12.6 ab
1.0 b
nd
nd
334.3 ab
18.2 ab
416.3 ab
50.2
23.9 a
16.3
26.4
32.7 a
38.9
149.7 b
2.9
11.1 b
1.0 b
nd
nd
289.0 b
14.0 b
353.2 b
4.8
0.9
0.6
1.7
1.6
11.3
7.0
1.4
0.7
0.1
ÿ
ÿ
20.1
2.0
21.3
C. Jo et al./Meat Science 51 (1999) 355±361
359
Meat (2 g) was sampled into a vial (40 ml) and analyzed
using the conditions described in detail by Ahn et al.
(1998a). The area of each peak was integrated and
reported as an indicator of volatiles generated from the
meat samples.
15.8% fat content in vacuum packaging. The TBARS
values of vacuum-packaged pork sausages were very
similar throughout storage indicating that oxygen
availability is the most critical factor in the development
of lipid oxidation.
2.4. Statistical analysis
3.2. Color
Experimental design was constructed to determine the
e€ect of irradiation and fat content on lipid oxidation,
color changes and volatile production in cooked sausages stored in two packaging conditions. Analyses of
variance (SAS Institute, 1988) were used to ®nd di€erences and the Student±Newman±Keul's multiple range
test was used to compare di€erences among mean
values. Mean values and standard errors of the mean
(SEM) were reported.
Irradiation had no e€ect on Hunter L-values of sausages both with aerobic and vacuum packagings (Figs. 1
and 2). Pork sausages with high fat produced lighter
color than low-fat sausages. Storage increased Hunter
L-values of pork sausages with both packagings but, the
changes of Hunter L-values in vacuum-packaged sausages were smaller than those of the aerobic-packaged.
Irradiation reduced a-values of aerobic-packaged pork
sausages at day 0 but had no e€ect on those at day 3.
Nonirradiated pork sausages with 10% backfat added
had higher a-value than that of the irradiated sausages
with 20% backfat added at day 7. However, there were no
di€erences in a-values between irradiated and nonirradiated sausages within a same backfat treatment at
day 7. The Hunter a-values of aerobic-packaged pork
sausage gradually decreased in all treatments as storage
time increased. The a-values of all pork sausage were the
highest in vacuum-packaged irradiated sausages and the
lowest in aerobic-packaged nonirradiated sausages.
Therefore, packaging type (oxygen availability) was again
an important factor for maintaining the color of sliced
pork sausages during storage. Irradiation reduced Hunter
b-values of vacuum-packaged sausages but had no e€ect
on Hunter b-values of the aerobic-packaged product.
3. Results and discussion
3.1. Lipid oxidation
Regardless of storage time, irradiation or packaging
types, TBARS values in sausages increased with the
increase of fat content (Table 1). Fat content of sausages prepared with 0, 10 and 20% backfat added were
4.7, 10.5 and 15.8%, respectively. Irradiation increased
the lipid oxidation of sausages with 10.5 and 15.8% fat
content in both aerobic and vacuum packaging at day 0.
However, the irradiation e€ect on lipid oxidation disappeared during storage except for the sausages with
Table 4
E€ect of fat content on the production of volatiles in irradiated aerobic-packaged pork sausages after 7 days of storage at 4 C a
Volatiles
1-heptene
Propanal
2-methylpropanal
2-methylbutanal
Pentanal
3-pentanone
Hexanal
1-butanol
1-pentanol
Nonanal
Decanal
1-heptanol
Aldehydes + ketones
Alcohols
Total Volatiles
a
b
c
d
Nonirradiated
4.7%
10.5%
15.8%
9.6
16.0
68.8
9.9
33.3 a
93.8
369.6 a
8.2
29.8 a
7.0 a
4.7
6.8 a
602.9 a
41.8 a
654.3 a
9.9
20.2
63.5
13.4
26.9 a
79.0
228.7 b
7.5
25.3 a
3.8 b
3.9
4.3 b
439.5 b
37.1 b
486.5 b
13.5
13.4
120.0
15.3
20.1 b
60.3
200.7 b
7.1
21.5 b
3.0 c
5.5
2.9 c
138.0 b
31.5 c
483.0 b
Irradiated at 0 or 4.5 kGy dose.
SEM: standard error of mean.
Di€erent letters with in a row are signi®cantly di€erent ( p < 0.05). n=12.
nd: not detected.
Irradiated
SEMb
4.7%
Area (pA s)
1.6
60.1 a
2.3
26.9 b
19.0
60.8 c
1.6
22.1 a
2.1
35.5 a
9.8
81.8
9.4
349.7 a
0.3
7.6
0.6
24.6 a
0.2
6.1 a
1.1
1.0 a
0.2
5.4 a
24.6
583.8 a
0.9
37.6 a
24.0
681.5 a
10.5%
15.8%
SEMb
21.3 b
21.2 c
152.7 a
18.1 b
18.9 b
50.7
202.3 b
7.7
18.1 b
3.6 b
0.3 b
3.2 b
467.7 b
29.0 b
518.0 b
55.3 a
34.6 a
89.8 b
24.9 a
35.6 a
54.8
195.8 b
6.7
15.0 b
2.9 b
nd d
2.2 c
437.8 b
24.0 c
517.2 b
2.6
1.3
4.5
1.0
1.6
9.3
14.9
0.5
1.1
0.3
0.1
0.3
25.2
1.2
27.1
360
C. Jo et al./Meat Science 51 (1999) 355±361
3.3. Volatiles
hydrocarbons. The Cnÿ1 has one carbon atom less than
the parent fatty acid, and the Cnÿ2:1 has a double bond
in position 1 and is two carbon atoms less than the
parent fatty acid. Therefore, 1-heptene (C7:1) would be
a product from nonane (C9:0) that oxidized and cleaved
from oleic or other n ÿ 9 fatty acids during irradiation
and storage. The productions of nonanal, decanal or 1heptanol in vacuum-packaged pork sausages (both
irradiated and nonirradiated) were very small. The
amount of total volatiles in irradiated cooked pork
products was signi®cantly higher than the amount in the
nonirradiated products. In addition to the amount of
identi®ed volatiles, many unknown volatiles with short
retention time also were found in irradiated samples.
This means that irradiation increased not only volatiles
production but also the number of volatile compounds.
Most probably, these volatiles would be nonpolar small
hydrocarbons and could be important for irradiation
odor but were excluded from the calculation of total
volatiles.
More volatiles were produced as the development of
lipid oxidation in pork sausages progressed during
storage (Tables 2±5). Shahidi and Pegg (1994) observed
that the content of hexanal, an index of lipid oxidation
and meat ¯avor deterioration, declined markedly upon
extended storage of meat. They indicated that the reactions of hexanal with meat components or its further
oxidation to hexanoic acid were responsible for the
reduction of hexanal in meat during storage. The present study showed decrease of hexanal in pork sausages
after 7-day storage only in vacuum packaging. The
reason for hexanal change in vacuum-packaged pork
sausages during storage cannot be explained.
High-fat sausages produced more propanal but less 1pentanol, nonanal and 1-heptanol than low-fat products
(Tables 2±5). The amounts of aldehydes, ketones and
alcohols were the highest in pork sausages with 4.5% fat
and the lowest in sausages with 15.8% fat. Among
individual volatile compounds, only propanal showed
the same trend as TBARS values, which increased with
the increase of fat content (Table 1). This indicated that
there would be certain interactions between fat content
and production of volatiles in pork sausages. Recently,
Ahn et al. (1998b) reported that cooked pork patties
from L. dorsi, which had about 2.5 to 3 times higher fat
content than those from R. fermoris, produced less hexanal and total volatiles than those from R. fermoris at
the same TBARS value. Jo and Ahn (1998b) con®rmed
this trend using an oil emulsion study. Their results
suggested that if the amount of volatiles is used as an
indicator of lipid oxidation or o€-¯avor generation in
cooked pork products, the fat content of samples should
be taken into consideration.
Irradiation increased the amount of 1-heptene in pork
sausages signi®cantly but storage or packaging type
did not (Tables 2±5). Although very small amounts of
1-heptene were found in nonirradiated pork sausages,
1-heptene was an excellent indicator for irradiation
treatments. Villavicencio, Mancini-Filho, Hartmann,
Ammon, and Delincee (1997) suggested the use of
hydrocarbons to detect radiation treatment in the processing of beans. Nawar et al. (1996) reported that irradiation breaks chemical bonds in triacylglycerides and
produces carbonyl compounds such as Cnÿ1 and Cnÿ2:1
Table 5
E€ect of fat content on the production of volatiles in irradiated vacuum-packaged pork sausages after 7 days of storage at 4 C a
Volatiles
1-heptene
Propanal
2-methylpropanal
2-methylbutanal
Pentanal
3-pentanone
Hexanal
1-butanol
1-pentanol
Nonanal
Decanal
1-heptanol
Aldehydes + ketones
Alcohols
Total volatiles
a
b
c
d
Nonirradiated
4.7%
10.5%
5.3 b
7.5 c
14.4
15.1
18.2
51.3
109.3
6.3
10.2
0.5
nd d
0.5
216.3
17.1
238.7
6.9 ab
11.5 b
13.2
18.1
18.2
59.9
100.7
5.3
10.2
0.3
nd
0.3
221.9
15.7
244.5
15.8%
9.1 a
15.1 a
14.3
19.4
22.9
57.4
103.9
4.6
9.5
nd
nd
nd
233.0
14.0
256.1
Irradiated at 0 or 4.5 kGy dose.
SEM: standard error of mean.
Di€erent letters within a row are signi®cantly di€erent ( p < 0.05). n=12.
nd: not detected.
Irradiated
b
4.7%
10.5%
15.8%
Area (pA s)
0.7
53.5
0.7
11.5 b
0.6
17.6
6.0
28.1 c
3.4
23.3 b
5.7
79.9
4.6
131.9 a
0.6
6.0
0.3
9.7 a
0.2
2.2 ab
ÿ
nd
0.2
1.4 a
16.2
294.5
1.0
17.0 b
16.8
365.1
50.5
16.8 a
17.6
42.4 a
29.5 a
82.7
122.7 ab
6.8
10.9 a
1.7 ab
nd
1.0 a
313.4
18.7 a
382.6
55.2
20.1 a
16.4
36.3 b
30.6 a
66.8
102.3 b
5.4
7.5 c
1.2 b
nd
0.3 b
267.2
12.4 c
341.9
SEM
SEMb
1.7
1.1
0.4
1.9
1.7
10.1
7.3
0.4
0.3
0.2
ÿ
0.2
19.0
0.5
19.4
C. Jo et al./Meat Science 51 (1999) 355±361
Ahn et al. (1998b) observed that oxygen exclusion
from meat after cooking was more important in preventing lipid oxidation of cooked meat than raw meat
treatments. The authors reported that lipid oxidation
was not catalyzed by the cooking process but by subsequent oxygen contact with cooked meat during storage. Packaging types had the most in¯uence on the
production of volatiles, lipid oxidation and color changes in cooked pork sausages during storage. It was
concluded that keeping oxygen from meat was more
important than irradiation and fat content in maintaining a high quality of meat after cooking.
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