Meat Science 85 (2010) 368–372

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Meat Science
journal homepage: www.elsevier.com/locate/meatsci

Effects of gamma irradiation and electron beam irradiation on quality, sensory,

and bacterial populations in beef sausage patties
J.G. Park a,b, Y. Yoon a, J.N. Park a, I.J. Han a, B.S. Song a, J.H. Kim a, W.G. Kim a, H.J. Hwang b, S.B. Han c,
J.W. Lee a,*
a
Team for Radiation Food Science and Biotechnology, Advanced Radiation Technology Institute, Korea Atomic Energy Research Institute, Jeongeup 580-185, Republic of Korea
b
Graduate School of Food and Biotechnology, Korea University, Chungnam 339-700, Republic of Korea
c
Food and Risk Standardization Team, Korea Food and Drug Administration, Seoul 122-704, Republic of Korea

a r t i c l e i n f o a b s t r a c t

Article history: This study compared effects of gamma ray (GR) and electron beam (EB) irradiation on quality (TBARS
Received 30 June 2009 value, hardness, color), sensory characteristics, and total bacterial populations in beef sausage patties
Received in revised form 11 January 2010 during accelerated storage at 30 °C for 10 days. Beef sausage patties were vacuum-packaged and irradi-
Accepted 13 January 2010
ated by GR and EB at 0, 5, 10, 15, and 20 kGy at room temperature. The results of quality evaluation
showed that the effects of GR irradiation were similar (p P 0.05) to EB irradiation on lipid oxidation,
hardness, color and sensory scores of the beef sausage patties. However, GR-irradiated samples had lower
Keywords:
(p < 0.05) total bacterial counts than EB-irradiated samples after irradiation, and during storage regard-
Gamma irradiation
E-beam irradiation
less of irradiation dose. The results indicate that use of GR irradiation up to 10 kGy on patties should
Beef sausage patties be useful in reducing bacterial populations with no adverse effect on quality and most of sensory char-
Sensory quality acteristics (color, chewiness, and taste).
Crown Copyright Ó 2010 Published by Elsevier Ltd. All rights reserved.

1. Introduction and Development Laboratories required 41.2-kGy irradiation in

A meat industry has grown substantially in recent years, and
the development of new processed meat products has increased
because of the demand for meat products and the excellent nutri-
tional properties of the foods. However, slaughtering, cutting, and
meat processing procedures may increase possibility of microbial
contamination on foods. The studies by Taha (1999), and Wood-
burn and Raob (1997) showed that fresh meat and processed meat
have been related to the transmission of foodborne pathogens such
as Escherichia coli O157:H7, Salmonella, Pseudomonas spp., Listeria
monocytogenes, Staphylococcus aureus, and Bacillus cereus.
One of decontamination technologies for ensuring the microbi-
ological safety of meat is radiation technology. Food irradiation has
been studied to improve food safety since the 1950s, and many sci-
entists have demonstrated that food irradiation at low doses offers
advantages to processors, retailers, and consumers (Thayer, 1993).
Although low dose (<10 kGy) irradiation significantly reduced bac-
terial populations in food, still higher doses are required for ensur-
ing food safety. In South Africa, 45-kGy irradiation is permitted to
shelf-stable meat products such products have been marketed in
recent years (Bruyn, 2000). Moreover, the US Army Natick Research
* Corresponding author. Tel.: +82 63 570 3204; fax: +82 63 570 3207.
E-mail address: sjwlee@kaeri.re.kr (J.W. Lee).
beef to ensure no Clostridium botulinum spore in the product (Anel-
lis, Rowley, & Ross, 1979).
Gamma ray (GR) used in most commercial plants to treat pre-
packaged items because GR irradiation has high penetrating
power, but a major limitation of electron beam (EB) has their lim-
ited penetration depth only up to 8 cm in foods (Miller, 2005).
Thus, EB treatment has been used for products such as grain on a
conveyor or low-density foods (Song, Kim, Yun, Kim, & Jo, 2009).
Mitchell (1994) suggested that although both isotopic and machine
sources have similar effects on foods, consumers would react more
favorable to machine sources compared to isotope sources because
of the association of isotopes with the nuclear industry.
Roberts and Weese (1998) reported that shelf life of ground
beef patties stored at 4 °C may be extended by GR irradiation at
5 and 7 kGy. The studies by Lee, Yook, and Kim (1999) and Giroux,
Ouattara, and Yefsah (2001) showed that GR irradiation (<5 kGy)
with antioxidants reduced bacterial populations (total aerobic bac-
teria, coliforms) with improved qualities (lipid oxidation, color,
sensory characteristics). Wheeler, Shackelford, and Koohmaraie
(1999) also presented there were no differences in sensory charac-
teristics of frozen ground beef patties between GR-irradiated sam-
ples (3 or 4.5 kGy) or non-irradiated samples. In EB-irradiated beef
patties at 10 kGy, no viable aerobic, total coliform, or E. coli was de-
tected, and physicochemical changes of beef patties caused by lipid

0309-1740/$ - see front matter Crown Copyright Ó 2010 Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.meatsci.2010.01.014
 J.G. Park et al. / Meat Science 85 (2010) 368–372
oxidation, and surface discoloration were increased by EB irradia-
tion (Gill, Marsden, & Kropf, 1998; Poon, Dubeski, & Kitts, 2004;
Wong, Wijewickreme, & Kitts, 2005).
In comparison studies for effects of GR and EB irradiation on
various attributes, both GR and EB irradiation were effective to de-
crease total aerobic bacteria (Kim, Chung, & Ko, 1998), E. coli
O157:H7 (Lopez-gonzalez, Murano, Brennan, & Murano, 1999),
Pseudomonas fluorescens and Salmonella typhimurium (Chung, Ko,
& Kim, 2000) in refrigerated beef. GR irradiation had generally bet-
ter radurization effects than EB irradiation in beef (Kim et al.,
1998). Lopez-gonzalez, Murano, and Brennan (2000) also com-
pared effects of GR and EB irradiation on sensory characteristics,
and found that GR-irradiated beef patties had more intense
cardboardy and sour flavors, and salty and sour tastes than EB-irra-
diated beef patties. However, these comparison studies evaluated
effects of GR and EB irradiation either on quality or bacterial
growth in beef patty sample. Therefore, the objective of this study
was to compare the effects of GR and EB irradiation at various
doses up to 20 kGy on quality and sensory characteristics of
the beef sausage patties as well as reduction of microbial
population.
2. Materials and methods
2.1. Beef sausage patty preparation and packaging
Fresh beef chuck (1–2 days post-mortem; 18% fat) was pur-
chased from a local market and ground, using a 4-mm plate.
Ground beef (53 g) was then mixed with various ingredients (pork
back fat: 15 g, ice water: 6 g, onion: 8.5 g, egg white: 4.3 g, isolated
soy protein: 4.1 g, dried bread powder: 4.1 g, NaCl: 0.65 g, flavor
enhancing wine: 0.41 g, black pepper powder: 0.21 g, red color re-
agent: 0.01 g, trisodium phosphate: 0.22 g, sugar: 0.85 g) as de-
scribed by Lee et al. (2005), and 100 g of the meat batter was
used to prepare beef sausage patty (diameter: 100 mm, thickness:
10 mm), using a patty maker (Large Hamburger Press, Tupperware,
Inc., Orlando, FL, USA). The beef sausage patties were then heated
in a preheated oven (NU-VU ES-3, Menominee, MI, USA) at 70 °C
of internal temperature for 30 min. The beef sausage patties were
removed from the cooker and cooled to room temperature
(25 °C) for 50 min, and individually placed into a retort pouch
(laminated with polyester, aluminum and polypropylene,
10  15 cm2), followed by vacuum packaging at 300 mm Hg. The
internal temperature was monitored with a thermocouple
(TES-1300 thermometer, TES, Taiwan).
2.2. Irradiation and storage conditions
One side of vacuum-packaged patties were irradiated at 0 (con-
trol), 5, 10, 15, and 20 kGy by GR, and both sides of beef sausage
patties was irradiated by EB at same doses as GR. GR irradiation
was conducted using a cobalt-60 irradiator (point source AECL,
IR-79, MDS Nordion International Co., Ltd., Ottawa, Ontario,
Canada) in the Advanced Radiation Technology Institute, Korea
Atomic Energy Research Institute (Jeoung-Eup, Korea). The source
strength was approximately 300 kCi with a dose rate of 10 kGy/
h. Dosimetry was applied using 5-mm diameter alanine dosimeters
(Bruker Instruments, Rheinstetten, Germany). EB irradiation was
performed with an ELV-4 Electron-Beam-Accelerator (2.5 MeV) at
the EB-Tech (EB-Tech Co., Daejeon, Korea). The beam currents were
2.5, 5, 7.6, and 10.5 mA for 5, 10, 15, and 20 kGy, respectively. After
irradiation, the patties were stored at 30 °C (10 days) for
accelerated storage, recommended by Oh et al. (2004) as sufficient
conditions to verify change of bacterial populations and physico-
chemical properties.
369
2.3. Quality evaluation
2.3.1. 2-Thiobarbituric acid (TBARS) values
To determine lipid oxidation of patties, TBARS value was mea-
sured on day 0, 2, 5, and 10 according to the method described
by Ahn, Olson, Jo, Love, and Jin (1999). The sample (5 g) was
homogenized in a 50-mL centrifuge tube with 50 lL of butylated
hydroxyanisol (BHA) (7.2% in ethanol) and 15 mL of distilled water,
using a homogenizer (DIAX 900, Heidolph Co., Ltd., Schwabach,
Germany). The 1 mL portions of the homogenates were mixed with
3 mL of 20 mM 2-thiobarbituric acid (15% in trichloroacetic acid
solution), heated in boiling water for 15 min, and centrifuged for
10 min at 2500g, using a centrifuge (UNION 5 KR, Hanil Science
Industrial, Co., Ltd., Incheon, Korea). The absorbance of the super-
natant was measured at 532 nm by a spectrophotometer (UV
1600 PC, Shimadzu, Tokyo, Japan), and it was reported as lg mal-
ondialdehyde/g.
2.3.2. Hardness and Hunter’s color value (L*, a*, and b*)
The hardness of the patties was determined on day 0 using a pe-
netrating test by a texture analyzer system (TA-XT2i, Stable Micro
System, England) equipped with a probe (1.0 cm thickness). To
determine hunter’s color value such as L* (lightness), a* (redness),
and b* (yellowness), color values of the patty surface were mea-
sured on day 0 by a color/color difference meter (Model CM-
3500d, Minolta Co., Osaka, Japan); standard colors: L* (90.5), a*
(0.4) and b* (11.0).
2.3.3. Sensory evaluation
Sensory evaluation of the patties was conducted on day 0 by 21
panelists who were trained according to the method described by
Civille and Szczesniak (1973), Ahn, Jo, and Olson (2000), and Aziz,
Mahrous, and Youssef (2002). Briefly, training sessions were con-
ducted to inform panelists with the products and attributes to be
evaluated, and were followed by an open discussion. Panelists
were trained in three 1 h sessions in which patties were served
to the panelists from a wide variety of treatments to familiarize
them with a wide range of color, chewiness, taste, off-flavor, and
overall acceptance of patties. Sensory scores of patties were re-
ferred to using a seven point descriptive scale where 1 = extremely
dislike or extremely weak to 7 = extremely like or extremely
strong.
After irradiation, patties were removed from pouches and re-
heated in a cooker (NU-VU ES-3 cooker, Menominee, MI, USA) at
130 °C for 10 min for sensory evaluation. The samples were cooled
to 45–55 °C, cut into 2-cm cubes, and served to panelists. Patties
were served randomly to each panelist 15 min after the packages
were opened. Sample order was also randomized to account for
sampling order bias. Water and unsalted crackers were provided,
and panelists were asked to expectorate and rinse their mouths be-
tween each sample. Results were expressed as the predominant
score given by panelists.
2.4. Total aerobic bacteria
Total aerobic bacterial populations in patties were determined
on day 0, 2, 5, and 10. The 10 g portions of patties were placed
aseptically in sterile nylon bag (10  15 cm; Sunkyung Co., Ltd.,
Seoul, Korea) containing 90 mL of 0.1% sterile peptone water (Difco
Laboratories, Detroit, MI, USA) and pummelled for 2 min using a
Lab-blender 400 stomacher (Seward medical, London, UK). The ali-
quots of the pummelled samples were serially diluted with 0.1%
sterile peptone water, and 0.1 mL portions of the diluents were pla-
ted on plate count agar (Difco Laboratories, St. Louis, USA) in trip-
licate. The plates were then incubated at 37 °C for 48 h, and total
aerobic bacterial populations on plates were determined as colony
370 J.G. Park et al. / Meat Science 85 (2010) 368–372

forming units (log CFU) per gram. Spoilage in sample was defined
as results of total bacterial populations (P8 log CFU/g), spoilage
odor, and slim layer as described by Oh et al. (2004).
2.5. Statistical analysis
Samples were analyzed in triplicate and the results were pre-
sented as mean ± standard deviation. All data were analyzed by
the generalized linear model procedures of the SASÒ version 9.2
(SAS Institute, Cary, NC, USA). Tukey’s multiple range tests were
used to compare LS means among treatments at a = 0.05.
3. Results and discussion
3.1. Quality evaluation
3.1.1. Effect of irradiation on lipid oxidation
TBARS values of GR or EB-irradiated patties up to 10 kGy were
not different (p P 0.05) compared to the control, but TBARS values
of the samples which were irradiated more than 15 kGy were high-
er (p < 0.05) than those of control (Table 1). Irradiation induced li-
pid oxidation by hydroxyl radicals generated by ionizing
irradiation in meat and meat products (McMillin, 1996), and this
lipid oxidation adversely affected color, flavor, texture and nutri-
tive value of meat (Smith, Tinsley, & Bubl, 1960). However, the re-
sult from our study showed that GR or EB irradiation caused lipid
oxidation in beef patties only when irradiated more than 15 kGy.
Mattison et al. (2006) also showed that low dose (1 kGy) irradia-
tion on pork loins did not influence cooking loss, TBARS values,
and sensory characteristics. Meanwhile, TBARS values of irradiated
beef patties were increased (p < 0.05) with no general difference
(p P 0.05) between GR and EB irradiation during storage (Table 1).
3.1.2. Hardness and Hunter’s color value
Irradiation of patties did not decrease hardness of the samples
(p P 0.05), and no difference (p P 0.05) in hardness was observed
between GR and EB-irradiated samples (Table 2). Lee et al. (2005)
also reported that gamma irradiation at 20 kGy did not affect hard-
ness, cohesiveness springiness, chewiness and gumminess of pork
patties.
The L* values of patties were not changed (p P 0.05) by GR and
EB irradiation, regardless of irradiation dose, but a* and b* values of
GR and EB-irradiated beef patties decreased (p < 0.05) as irradia-
tion dose increased (Table 2). a* and b* values in GR-irradiated beef
patties were lower (p < 0.05) than those of EB-irradiated beef pat-
ties irradiated at more than 10 kGy (Table 2). In agreement, a study
by Kim, Nam, and Ahn (2002) showed that GR irradiation caused
color change of pork loin, chicken breast redder or pinker, and beef
loin into greenish brown. Thus, further research should be needed
to control discoloration problems of irradiated patties. Nam and
Ahn (2003) reported that antioxidants such as ascorbate, citrate,
tocopherol, garlic esters, and polyphenols may reduce the discolor-
ation of irradiated meat because they either induce reducing con-
ditions or scavenge free radicals. Hence, the combination of
irradiation and antioxidants to minimize color change in beef sau-
sage patties should be studied in further research.
3.1.3. Sensory evaluation
Although irradiation decreased a* and b* values of beef patties,
sensory characteristic (color) of the beef patties was not generally
influenced by both irradiation methods (Table 3). Chewiness and

Table 1
Effects of gamma ray or electron beam irradiation on TBARS values (mean ± standard deviation; lg malondialdehyde/g sample) in vacuum-packaged beef sausage patties during
storage at 30 °C.

Irradiation dose (kGy) Storage period (days)

0 2 5 10
c A
Gamma ray irradiation 0 1.75 ± 0.36 – – –
5 2.35 ± 0.28bc – – –
10 2.54 ± 0.12abc 2.91 ± 0.36a 3.23 ± 0.17b –
15 2.88 ± 0.31ab 2.94 ± 0.16a 3.95 ± 0.51ab 4.69 ± 0.5a
20 3.21 ± 0.25a 3.22 ± 0.43a 4.14 ± 0.28a 5.37 ± 0.41a
Electron beam irradiation 0 1.75 ± 0.36c – – –
5 1.91 ± 0.24c – – –
10 2.18 ± 0.36bc 2.31 ± 0.29a – –
15 2.85 ± 0.29ab 2.99 ± 0.13a – –
20 2.98 ± 0.25ab 3.01 ± 0.67a – –
a–c
Means within the same column with different letters were significantly different (p < 0.05).
A
Bar indicates no determination of TBARS value when samples had obvious spoilage odor and slim layer, and more than 8 log CFU/g of total bacterial populations.

Table 2
Hardness (mean ± standard deviation; g) and Hunter’s color values (mean ± standard deviation) in the gamma ray or electron beam-irradiated beef sausage patties after vacuum
packaging.

Irradiation dose (kGy) Hardness L* a* b*

a a a
Gamma ray irradiation 0 451.26 ± 31.79 40.94 ± 0.91 15.57 ± 0.09 21.65 ± 0.26a
5 421.79 ± 24.09ab 40.65 ± 0.85a 11.84 ± 0.14c 20.95 ± 0.13bc
10 412.67 ± 44.23ab 40.31 ± 0.63a 7.91 ± 0.23e 20.32 ± 0.28cd
15 395.35 ± 11.97ab 39.53 ± 0.41a 5.75 ± 0.19f 19.81 ± 0.19de
20 360.01 ± 19.21b 39.18 ± 0.52a 4.52 ± 0.05g 19.46 ± 0.22e
Electron beam irradiation 0 451.26 ± 31.79a 40.94 ± 0.91a 15.57 ± 0.09a 21.65 ± 0.26a
5 436.04 ± 34.73ab 40.79 ± 0.36a 12.63 ± 0.19b 21.74 ± 0.28a
10 427.83 ± 41.48ab 40.43 ± 0.71a 8.32 ± 0.13d 21.33 ± 0.17ab
15 406.54 ± 15.39ab 40.35 ± 0.52a 5.98 ± 0.07f 20.81 ± 0.23bc
20 380.16 ± 19.05ab 40.14 ± 0.65a 4.89 ± 0.12g 20.63 ± 0.29c
a–g
Means within the same column with different letters were significantly different (p < 0.05).
 J.G. Park et al. / Meat Science 85 (2010) 368–372 371

Table 3
Sensory evaluation (mean ± standard deviation) of gamma ray or electron beam-irradiated beef sausage patties after vacuum packaging.

Irradiation dose (kGy) Color Chewiness Taste Off-flavor Overall acceptance

a a a e
Gamma ray irradiation 0 6.8 ± 0.4 6.6 ± 0.7 6.8 ± 0.6 1.2 ± 0.1 6.8 ± 0.7a
5 6.2 ± 0.6ab 5.9 ± 0.4ab 6.1 ± 0.6ab 2.1 ± 0.2cd 5.8 ± 0.4abc
10 6.1 ± 0.5ab 5.4 ± 0.6abcd 5.7 ± 0.5abc 2.6 ± 0.3abc 5.1 ± 0.6bcd
15 5.5 ± 0.5ab 4.9 ± 0.3bcd 5.2 ± 0.5bcd 2.8 ± 0.3ab 4.6 ± 0.2cd
20 5.3 ± 0.4b 4.1 ± 0.4d 3.9 ± 0.3d 3.2 ± 0.2a 4.1 ± 0.3d
Electron beam irradiation 0 6.8 ± 0.4a 6.6 ± 0.7a 6.8 ± 0.6a 1.2 ± 0.1e 6.8 ± 0.7a
5 6.5 ± 0.5ab 6.1 ± 0.5ab 6.2 ± 0.5ab 1.8 ± 0.3de 6.1 ± 0.5ab
10 6.4 ± 0.5ab 5.5 ± 0.5abc 5.9 ± 0.6ab 2.1 ± 0.3cd 5.3 ± 0.4bcd
15 6.2 ± 0.6ab 5.1 ± 0.3abcd 5.4 ± 0.5abc 2.5 ± 0.2bc 4.9 ± 0.3bcd
20 5.8 ± 0.4ab 4.3 ± 0.3cd 4.3 ± 0.4cd 2.7 ± 0.2abc 4.3 ± 0.4d
a–e
Means within the same column with different letters were significantly different (p < 0.05).

Table 4
Effects of gamma ray or electron beam irradiation on the reduction of total aerobic bacterial populations (mean ± standard deviation; log CFU/g) in vacuum-packaged beef
sausage patties during accelerated storage at 30 °C.

Irradiation dose (kGy) Storage period (day)

0 2 5 10
Gamma ray irradiation 0 3.61 ± 0.06a –A – –
5 <2.00 ± 0.00d 5.54 ± 0.02c – –
10 <2.00 ± 0.00d 3.93 ± 0.05d 6.64 ± 0.04a –
15 <2.00 ± 0.00d 2.68 ± 0.03e 5.83 ± 0.05b 7.38 ± 0.06a
20 <2.00 ± 0.00d <2.00 ± 0.00f 3.79 ± 0.03c 5.87 ± 0.05b
Electron beam irradiation 0 3.61 ± 0.06a – – –
5 3.12 ± 0.05b 7.72 ± 0.03a – –
10 2.48 ± 0.04c 6.52 ± 0.04b – –
15 <2.00 ± 0.00d 6.13 ± 0.05c – –
20 <2.00 ± 0.00d 5.41 ± 0.03c – –
a–f
Means within the same column with different letters were significantly different (p < 0.05).
A
Bar indicates no determination of total aerobic bacterial populations when samples had obvious spoilage odor and slim layer, and more than 8 log CFU/g of total bacterial
populations.

taste of GR and EB-irradiated samples were not changed (p P 0.05)
up to 10 kGy and 15 kGy of irradiation, respectively. Off-flavor of
GR and EB-irradiated samples was continuously increased
(p < 0.05) by irradiation, and overall acceptance was not changed
up to 5 kGy. Lopez-gonzalez et al. (2000) reported that the beef
patties irradiated at 2 kGy of GR had more intense cardboardy
and sour flavors, and salty and sour tastes than the beef patties
irradiated at 2 kGy by EB. However, the result from our study sig-
nificant differences (p P 0.05) of sensory characteristics of GR- and
EB-irradiated samples were not observed. Generally, most chemi-
cal changes such as off-flavor generation in meat are associated
with free radical reactions (Smith et al., 1960). Irradiation can ini-
tiate or promote lipid oxidation, resulting in undesirable off-odors
and flavors (Tappel, Groninger, & Knapp, 1958). However, the gen-
eration of off-flavor in irradiated meat and meat products could be
reduced by various methods such as modified atmosphere packag-
ing, low irradiation temperature (freezing), and addition of antiox-
idants (Brewer, 2009).
3.2. Effect of irradiation on bacterial growth
On day 0, total aerobic bacterial populations in cooked beef pat-
ties (untreated) were about 3.6 log CFU/g. After irradiation, GR irra-
diation decreased more total bacterial populations (p < 0.05) than
EB irradiation, and bacterial populations in GR-irradiated samples
and EB-irradiated samples were below detection limit (2 log CFU/
g) after irradiation more than 5 kGy and 15 kGy, respectively (Ta-
ble 4). This result was also found in studies by Chung et al.
(2000) and Kim, Chung, and Ko (1998) indicating that GR irradia-
tion was more effective than EB irradiation for the destruction of
P. fluorescens, psychrotrophs and mesophiles in refrigerated beef
because EB has lower penetration depth than GR. However, bacte-
ria in the samples which had below detection limit on day 0 were
recovered during accelerated storage at 30 °C, and bacterial popu-
lations in EB-irradiated samples was higher (p < 0.05) than those in
GR-irradiated samples.
4. Conclusions
GR irradiation may be more effective in decreasing bacterial
populations compared to EB irradiation, and both of GR and EB
irradiation did not have adverse effects on lipid oxidation and most
sensory characteristics (color, chewiness, and taste) up to 5 kGy
and 10 kGy, respectively. Therefore, GR irradiation at 5–10 kGy
on patties should be useful in reducing bacterial populations with
no adverse effect on quality and most of sensory characteristics
(color, chewiness, and taste).
Acknowledgement
This work was supported by Nuclear Research and Develop-
ment Program of the Korea Science and Engineering Foundation
(KOSEF) Grant funded by the Korean government (MEST) (Grant
code: KOSEF R01-2008-000-20213-0).
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