Food Control 90 (2018) 113e120

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Food Control
journalhomepage:www.elsevier.com/locate/foodcont

Evaluation of non-thermal hurdle technology for ultraviolet-light to inactivate

Escherichia coli K12 on goat meat surfaces
Hema L. Degala a, Ajit K. Mahapatra a, *, Ali Demirci b, Govind Kannan a
a Food Engineering Laboratory, Agricultural Research Station, College of Agriculture, Family Sciences and Technology, Fort Valley State University, Fort Valley,
GA, 31030, USA
b Department of Agricultural and Biological Engineering, Pennsylvania State University, University Park, PA, 16802, USA

article info abstract

Article history: Non-thermal processes are in demand in the meat industry due to their ability to inactivate foodborne pathogens, such as
Available online 26 February 2018 Escherichia coli O157:H7, at room temperatures. Although ultraviolet-light (UV-C) is a potential process for eliminating
pathogens while preserving the quality of foods, its inefficiency in penetrating solid foods might result in a lower log reduction
Keywords: of pathogens in meat. Thus, it is necessary to look at hurdle technologies. Lemongrass oil (LG), with its antimicrobial,
UV-light antifungal and antioxidant properties, can be an ideal alternative. Therefore, the objective of this study was to evaluate the
Essential oils efficacy of UV-C, LG, and their combination on E. coli K12 inoculated goat meat. Lemongrass oil at 0.25%, 0.5%, and 1%
Non-thermal processing concentrations (w/v) with intensities of 100 and 200 mW cm 2, which provided an energy dose of 0.2 e2.4 mJ cm 2 of UV-C,
E. coli Goat was used to treat goat meat for 2, 4, 6, 8, 10, and 12 min. The top surfaces of LG treated goat meat samples were treated with
meat Meat
quality UV-C by these combinations of treatments. The combi-nation of 1% LG þ UV-C with 200 mW cm 2 treatment for 2 min
resulted in a synergistic microbial reduction of 6.66 log10 CFU mL 1 (below detection levels) of E. coli K12 compared to the
control, the level of which was significantly higher than individual and other hurdle treatments (P 0.05). No significant effect
on the texture, whereas, changes in color and oxidative stability of goat meat was observed with LG þ UV-C treatments.
Although this combination seems to be a better option, treatment conditions need to be optimized and further studies are
required to validate hurdle mechanisms for commercial applications.

© 2018 Elsevier Ltd. All rights reserved.

1. Introduction
Escherichia coli (E. coli) O157:H7 is one of the most harmful foodborne
pathogens (Kaper & Karmali, 2008; Scallan et al., 2011; Zhang, Li, Jadeja,
Fang, & Hung, 2016), and it can result in a se-vere and sometimes fatal
condition called Hemolytic Uremic Syn-drome (HUS), leading to kidney
failure. It is responsible for about 2138 hospitalizations and 20 deaths
annually (Scallan et al., 2011). Although cattle are the major reservoir for E.
coli O157:H7, it also has been isolated from goats, deer, sheep, horses, dogs,
birds, and flies (Chapman, Siddons, Malo, & Harkin, 1997; Hancock et al.,
1998). Goat meat is an important source of animal protein, partic-ularly in
Africa and Asia. Since meat goats are raised and processed by smallholder
producers in most parts of the developing world,
meat hygiene practices may not be ideal due to various reasons. Non-thermal
intervention technologies such as the ones examined in this study can be
easily adopted by processing plants of any size. Besides, the significance of
goat meat in the U.S. has increased in recent years due to the lower fat content
of goat meat compared to beef, pork or lamb, and due to the growing
immigrant population that is traditionally accustomed to goat meat
consumption (APHIS, 2012). As a result, both domestic production and
importation of goat meat from other countries have increased in the U.S.
However, research on foodborne pathogens in goat meat has been very
limited, although there are reports that E. coli O157:H7 is prevalent in goats
as it is in cattle. Since both cattle and goats are ruminants, goat meat can serve
as an ideal model to study meat borne pathogens.

Since meat is usually marketed raw, thermal processes are not preferred
due to their potential effect on the quality of meat. Chemical methods,
especially chlorine-based washing techniques, have been used to
* Corresponding author.
E-mail address: mahapatraa@fvsu.edu (A.K. Mahapatra). decontaminate meat surfaces from foodborne

https://doi.org/10.1016/j.foodcont.2018.02.042
0956-7135/© 2018 Elsevier Ltd. All rights reserved.
114 H.L. Degala et al. / Food Control 90 (2018) 113e120
pathogens such as. E. coli O157:H7 and Salmonella. However, these chemical
methods leave a chlorine residue that causes health concerns in the meat.
Therefore, researchers have evaluated non-thermal technologies to
decontaminate foods at room tempera-tures without altering the organoleptic
properties of food products. Use of non-pathogenic strains of E. coli in place
of target microor-ganisms for in-plant inactivation studies was recommended
by the National Advisory Committee on the Microbiological Criteria for
Foods, 2010 (Gurtler, Rivera, Zhang, & Geveke, 2010). Escherichia coli K12
is one such surrogate strain that has been used in various inactivation studies,
including studies of pulsed electric field on apple juice (Gupta, Masterson, &
Magree, 2003), UV-light on model apple juice (Ercan, Wang, Demirci,
LaBorde, & Elias, 2016; Murakami, Jackson, Madsen, & Schickedanz, 2006),
pulsed UV-light on whole chicken carcasses (Keklik, Demirci, & Bock,
2011), ozone on spinach (Wani, Jagpreet, Joseph, Jeremy, & Ian, 2015), and
ozonated water and electrolyzed oxidizing water on goat meat (Degala, Scott,
Nakkiran, Mahapatra, & Kannan, 2016).
Ultraviolet-light (UV-light) is one such non-thermal technology that is
approved for surface treatment of food (Guan, Fan, & Yan, 2012; US-FDA,
2002). The germicidal effect of UV-light (UV-C) is between 245 and 285 nm
(Yaun, Sumner, Eifert, & Marcy, 2003), thus it may be an alternative surface
decontaminant to be used for inactivating bacteria and viruses. However, the
inactivation of mi-croorganisms by UV-light depends on the UV dose (EPA,
1999). Ultraviolet light dosage is calculated by Eq. (1):
2 2
D (UV Dose; mJ cm ) ¼ I (Intensity, mW cm ) t (Exposure time,
s) (1)
Various foods and beverages have been processed with UV-light
at different intensities and treatment times to inactivate foodborne
pathogens, such as L. monocytogenes, E. coli O157: H7, and Salmo-
nella spp., as well as degradative enzymes, such as polyphenol
oxidase, peroxidase, and polygalacturonase.
Essential oils are the secondary metabolites produced by plants
to help them in their defensive mechanism against microorganisms
(Hyldgaard, Mygind, & Meyer, 2012; Tajkarimi, Ibrahim, & Cliver,
2010). Essential oils are classified as “generally recognized as
safe” (Burt, 2004) and their mode of action and antibacterial ac-
tivity of individual EOs depends on the chemical structure of EOs
components, pH, temperature, and oxygen level, and the level of
microbial contamination of the food product (Boskovic et al., 2013;
Burt, 2004). Several EOs have been used in the meat industry as
antimicrobial and antioxidants against foodborne pathogens such
as Salmonella, L. monocytogenes, and Staphylococcus.
However, achieving higher log reductions using these non-
thermal technologies, individually, may require higher treatment
intensities, and increased treatment time both of which cause
adverse effects on quality characteristics of food (Wood & Bruhn,
2000), including changes in color, texture, and lipid oxidation
rate. Consequently, hurdle technologies seem to be a better alter-
native for a synergistic antimicrobial effect with reduced energy
inputs and treatment intensities (Leistner, 2000). These technolo-
gies can counter stress adaptation of microbial cells associated with
sub-lethal treatments by disturbing several functions of the cell
(Yousef, 2001). Therefore, researchers currently are focusing on
finding potential antimicrobial blends that can enhance food
preservation and at the same time satisfy green consumerism
(Hyldgaard et al., 2012).
Recently used combinations include organic or natural antimi-
crobial agents (Ross, Griffiths, Mittal, & Deeth, 2003), inorganic or
metal ions, and two or more non-thermal technologies. To cite a
few, the combination of acidic electrolyzed water, UV-light and
ultrasound on raw salmon fillets increased log reductions of
1
L. monocytogenes from 0.17 to 0.75 log CFU g (Krajnik, Feng, Bang,
& Yuk, 2017). Also, a UV-assisted TiO2 photocatalysis and high
hydrostatic pressure combination compared to individual treat-ments reduced
internalized murine norovirus by 5.5 log10 (below detection level) (Kim et al.,
2017). On the other hand, hurdle treatment of lemongrass oil with cold
nitrogen plasma promoted the anti-listerial activity of lemongrass oil on pork
loin, and po-tential impacts on sensory attributes of pork were minimized
(Cui, Wu, Li, & Lin, 2017). Lemongrass oil has also exhibited anti-biofilm
activity against L. monocytogenes (de Oliveira, Brugnera, Cardasu, Alves, &
Piccoli, 2010) on stainless steel surfaces and in strains of Staphylococcus
aureus in combination with grapefruit (Adukwu, Allen, & Phillips, 2012).
Therefore, this study was conducted to explore the potential of synergistic
efficiency of UV-light and essential oils to inactivate E. coli K12 on the
surface of goat meat and their impact on meat quality attributes.
2. Materials and methods
2.1. Microorganism
For this study, E. coli K12 was obtained from Carolina Biological Supply
Company, Burlington, NC. A stock culture of E. coli K12 was prepared by
streaking on Sorbitol MacConkey Agar (OXOID LTD., Basingstoke,
Hampshire, England) plates, incubated at 37 C for 24 h and then stored at 4 C,
sub-cultured by transferring a single colony onto a fresh agar plate every
week. For inoculum prepara-
tion, a single colony was transferred into 10 mL of tryptic soy broth
(TSB, (Sigma Aldrich. St. Louis, MO) and incubated for 24 h at 37 C
and 100 rpm. The pure culture was transferred into 100 mL of TSB,
incubated at 37 C and 100 rpm for 12 h, transferred to two 50 mL
sterile conical tubes, and then centrifuged (Sorvall ST 8R Centrifuge,
Thermo Electron LED GmbH, Langenselbold, Germany) at 2580 g
for 10 min at 4 C. The supernatant was decanted, and the pellet
was washed and suspended in 500 mL of sterile 0.1% peptone water
(Fisher Scientific, Fair Lawn, NJ). The initial inoculant population
1
was 6.3e6.6 log10 CFU mL of E. coli K12.
2.2. Preparation and inoculation of goat meat samples
Fresh boneless goat meat was obtained from the Georgia Small
Ruminant Research and Extension Center at Fort Valley State Uni-
versity, in Fort Valley, GA, and then vacuum packed and stored
at 20 C until used. Frozen meat was thawed at 4 C for 24 h and
then cut into small pieces, each weighing 20 ± 1 g. Goat meat
samples were rinsed with tap water to remove blood, sprayed with
70% ethanol and air dried in a laminar flow hood (Labconco Purifier
Class II Biosafety Cabinet, Labconco Corp. Kansas, MO) for 15 min
before inoculation. Goat meat samples were inoculated with 100 mL
of prepared E. coli K12 inoculum on the surface and left at room
temperature (22 ± 1 C) for 1 h for bacterial attachment (Al-Holy &
Rasco, 2015; Ozer & Demirci, 2006). Uninoculated goat meat
samples were used as a negative control and were tested for natural
microflora.
2.3. UV-light production and treatment
Ultraviolet light was provided by using a Spectrolinker, XL-1500
Series (Spectronics Corporation, Westbury, NY). The unit was fac-
tory calibrated at 254 nm. Energy dosage used for each treatment
was calculated based on intensities and treatment time used. In-
2
tensities of 100 and 200 mW cm , and treatment time 2, 4, 6, 8, 10,
and 12 min were selected for this study which yielded the energy
2
dosages as 0.2e2.4 mJ cm . The Spectrolinker XL-1500 was turned
on for 5 min for warm-up and inoculated goat meat samples were
 H.L. Degala et al. / Food Control 90 (2018) 113e120
exposed to UV-C by placing them in petri dishes at 10 cm from the UV-C
strobe (mercury vapor bulb). The set energy dosage was applied by setting
intensity and time.
2.4. Lemongrass oil treatment
Organic lemongrass oil (Cymbopogon flexuosus) was obtained from Plant
Therapy Inc. (Twin Falls, ID) for this study. Lemongrass oil (LG) of 0.25%
(0.05 mL), 0.5% (0.1 mL) and 1% (0.2 mL) concen-trations (w/v) per sample
was spread on the surface of goat meat samples for 2, 4, 6, 8, 10, and 12 min.
2.5. Hurdle technology using UV-light and lemongrass oil
Inoculated goat meat samples were treated with UV-C and LG. In this
treatment, samples were first treated on the surface with 0.25%, 0.5% and 1%
2
LG, followed by exposing them to 100 and 200 mW cm intensities of UV-C
(1 min LG treatment followed by 1 min UV-C treatment; 2 min LG treatment
followed by 2 min UV-C treatment; 3 min LG treatment followed by 3 min
UV-C treatment and so on), respectively.
2.6. Microbial analysis
To determine the population of E. coli K12 on treated and un-treated goat
meat samples, each sample was placed in 180 mL of sterile 0.1% peptone
water in a sterile stomacher bag. The sample was then pummeled at 230 rpm
for 30 s in a stomacher (Model 400 Circulator, Brinkmann Instrument Inc.,
Westbury, NY). The ho-mogenized solution was serially diluted in sterile
0.1% peptone water and spirally plated in duplicate on Sorbitol MacConkey
Agar using an EddyJet2 spiral plater (Neutec Group, Farmingdale, NY). After
incubating at 37 C for 24 h, colonies were counted by using a Bantex colony
counter (Model 920A, American Bantex Corp., Chandler, AZ).
2.7. Enrichment process
Enrichment was performed to ensure that there were no injured cells.
Enrichment procedures for the hurdle treatment 1% LG and UV-C 200 were
carried out for 2 and 12 min treatment time as detailed in the laboratory
methods in the bacterial analytical manual for diarrheagenic E. coli (US-FDA,
2011). For E. coli K12 enrichment, 25 g of sample (control and treated) was
aseptically placed into 225 mL of TSB Broth with Novobiocin (Sigma-
Aldrich) (dilution factor of 1:10) and incubated for 24 h at 37 C. Then, one
mL was serially diluted with 0.1% peptone water, plated in dupli-cates for
control and samples, and incubated for 24 h at 37 C.
2.8. Quality characteristics of meat
2.8.1. Color
Surface color of goat meat samples was measured using a HunterLab
MiniScan XE plus (Hunter Associates Laboratory, Reston, VA). The
instrument was calibrated before use. For each individual and hurdle
treatment, three samples for treatment time of 0, 6, and 12 min were used.
Measurements were taken at three different places on the top surface of
samples for L*, a*, and b* values. The measurements were taken immediately
after treatment and after 24 h. The samples were stored in individual Ziploc
bags at 4 C for 24 h after treatments.
2.8.2. Texture
Warner-Bratzler (WB) hardness values of goat meat samples were
determined using a TA-XT2i Texture Analyzer (Stable Micro
115
Systems, Scarsdale, NY) equipped with a WB cell. The instrument was
calibrated for weight with 2000 mg and for height with returning speed of 10
1
mm s , returning distance of 40 mm, and contact force of 10 g before
measuring the samples. A size # 7 cutter was used to make the sample cores
(120 mm) in triplicates for each individual and hurdle treatments for 0, 6, and
12 min. Three cores were made from each sample for measurement. Hardness
values of treated and untreated goat meat samples were measured by placing
each sample in a triangular slit of the shear blade, with muscle fibers almost
parallel to the force direction. As the blade was pulled through the opening,
the sample was sheared into two parts (Mahapatra, Harris, Nguyen, &
Kannan, 2011; Ruiz de Huidobro, Miguel, Blazquez, & Onega, 2005). From
the plot, the highest peak of the curve that is resistance of the meat sample to
shearing was recorded as maximum shear force. This value indicates the
tenderness of meat, and the hardness values were recorded as force (N).
2.8.3. Lipid oxidation
The effect of hurdle technologies on the oxidative stability of goat meat
was carried out using a thiobarbituric acid reactive substances (TBARS) assay
with a Food TBARS Assay Kit (Oxford Biomedical Research, Rochester
Hills, MI). This method measures the malondialdehyde (MDA) concentration,
an aldehyde formed as a secondary product of propagation phase in free
radical chain re-
action (Tomovic, Jokanovic, Sojic, Skaljac, & Ivic, 2017). These al-
dehydes are largely associated with deterioration of meat that occurs due to
cleavage of hydroperoxides and results in off flavor (Chen, 2016; Ho & Chen,
1993). Reagents, standards and samples were prepared as recommended by
the manufacturer's instructions for protein-containing samples. Samples were
allowed to react for 60 min at room temperature and centrifuged (Sorvall) at
15,000 g and 22e25 C for 5 min. Both standards and the lower aqueous layer
of samples were read at 532 nm by using SmartSpec™ Plus
Spectrophotometer (Bio-Rad Laboratories, Hercules, CA). A stan-dard curve
was plotted using the absorbance values of each stan-dard versus the
malondialdehyde (MDA) concentration for each standard. Net absorbance
values for meat samples were calculated using the equation from the
calibration curve, and the MDA value obtained was multiplied by a dilution
1
factor to give a final value of mg MDA kg of goat meat.
2.9. Statistical analysis
Trials were replicated four times, on different days, with two meat
samples for each treatment time and control (positive and negative) all of
which were analyzed in duplicate at each treatment time (n ¼ 16). A one-way
analysis of variance was carried out for each experiment. Data were subjected
to Tukey's studentized range test in SAS Version 9.4 (SAS Institute, Cary,
NC) to determine if there were significant differences (P 0.05) between mean
log re-ductions for each treatment time. Data presented are the average log
reduction with standard error of the mean.
3. Results and discussion
The efficacy of UV-light and LG in inactivating E. coli K12 to in-crease
the shelf-life of goat meat with minimized quality attributes has been
evaluated.
3.1. Log reduction of E. coli K12 on goat meat by individual UV-C
treatments
Log reductions of E. coli K12 on goat meat by individual UV-C
treatments were presented in Fig. 1. The reductions were
116 H.L. Degala et al. / Food Control 90 (2018) 113e120
Fig. 1. Reduction of E. coli K12 on goat meat surface after treatment with UV-light. Bars with
different letters are significantly different (P 0.05).
significantly (P 0.05) increased when UV-C intensity increased from 100 to
2
200 mW cm . More specifically, UV-C treatment applied individually
1 resistivity of E. coli to UV-C treatments with increased treatment time
demonstrated a reduction of 1.18 log10 CFU mL at an intensity of 200 mW
2 (Mofidi, Rochelle, Chou, & Mehta, 2002). This phenomenon might be one of
cm for 12 min. Re-ductions of approx. 1 log of L. monocytogenes on raw
salmon fillets using pulsed UV-light were reported by Ozer and Demirci
(2006), which is comparable to this study. It is hypothesized that limited
penetration depth, and presence of superficial lipid and proteins in meat with
strong UV-absorbing properties, form an additional barrier for UV photons’
availability to inactivate natural microbiota scattered throughout the rough
food matrix. This restricts useful-ness of UV-light as a surface decontaminant
(Bintsis, Litopoulou-Tzanetaki, & Robinson, 2000). In our study, increasing
2 UV-absorbing proper-ties also might have affected the log reductions in this
UV-C in-tensity from 100 to 200 mW cm significantly increased the bac-
1 study. Thus, the 1% LG þ UV-C with 200 mW cm for 2 min treatment time
terial reduction from 0.61 to 0.77 and 1.06 to 1.18 log10 CFU mL ,
respectively. However, increasing treatment time from 2 to 12 min had an
insignificant effect (P > 0.05) on bacterial reduction.
3.2. Log reduction of E. coli K12 on goat meat by individual LG
treatments
Log reductions of E. coli K12 on goat meat by individual LG treatments
were presented in Fig. 2. The reductions were signifi-cantly (P 0.05) increased
when LG concentration increased from 0.25% to 1%. Individual LG treatment
demonstrated a reduction of
1 2
2.16 log10 CFU mL with 1% LG for 8 min. However, studies by Salem,
Amin, and Afifi (2010) and Rounds, Havens, Feinstein, Friedman, and
Ravishankar (2012) on minced beef and cooked beef patties, respectively,
have shown reductions below detection levels with 1.5% LG. These studies
indicate that increasing LG con-centration can enhance the bacterial reduction
on meat surface. Among the individual treatments applied in our study, 1%
LG
Fig. 2. Reduction of E. coli K12 on goat meat surface after treatment with lemongrass oil. Bars
with different letters are significantly different (P 0.05).
1
treatment reduced the bacterial population by 2.16 log10 CFU mL from the
goat meat surface. However, the effect of increased treatment time from 2 to
1
12 min on bacterial reduction (2.05e2.1 log10 CFU mL ) was insignificant (P
> 0.05). Therefore, this study recommends 1% LG for 2 min treatment as a
potential individual non-thermal process to increase the shelf-life of goat
meat.
3.3. Log reduction of E. coli K12 on goat meat with non-thermal hurdle
technology for UV-light
Six different hurdle treatments of LG and UV-C were used to reduce
bacterial concentration of E. coli K12 on goat meat. Complete reduction (6.66
1
log10 CFU mL , below detection levels) was ach-ieved using a 1% LG þ
2
UV-C with 200 mW cm hurdle treatment (Fig. 3). Increasing concentration
and intensity significantly (P 0.05) increased bacterial reductions. In general,
increasing treatment time from 2 to 12 min had an insignificant (P > 0.05)
effect on bacterial reductions. The ability of pathogenic organisms to develop
resistance when exposed to sub-lethal stresses possibly increased the
the reasons for insignificant increase in reductions. Also, as observed in an
earlier study (Hyldgaard et al., 2012), E. coli, a Gram-negative bacterium, is
more resistant to essential oils (EOs) due to the presence of hydrophilic lip-
osaccharides in its cell membrane that could have probably resul-ted in
insignificant synergistic microbial reductions compared to individual
treatments in this study. According to Bintsis et al. (2000), limited penetration
depth and presence of superficial lipid and proteins in meat that have strong
2
1
that resulted in a synergistic microbial reduction of 6.66 log10 CFU mL
(below detection levels) compared to other hurdle treatments seems to be the
best option that can be used in place of current non-thermal hurdle
technologies to reduce E. coli K12 on meat surfaces.
3.4. Impact of enrichment on bacterial concentration
As presented in Fig. 3, E. coli K12 concentrations were reduced to below
1
detection levels (6.66 log10 CFU mL ) with 1% LG with UV-C 200 mW cm
hurdle treatment. Further enrichment of these sam-ples was positive
indicating only a sub-lethal injury, and cells could repair themselves. Similar
results were reported by Krishnamurthy (2006) with pulsed UV-light on
Staphylococcus aureus in milk foam, L. monocytogenes in beef jerky
processing (Harrison, Singh, Harrison, & Singh, 2006), and E. coli O157:H7
in needle tender-ized beef steaks managed under simulated industry
conditions (Brooks, Brashears, Miller, Echeverry, & Chancey, 2010).
3.5. Effect of non-thermal hurdle technology for UV-light on quality
characteristics of goat meat
3.5.1. Color
Tables 1 and 2 illustrate the L* (lightness-darkness), a* (redness-
greenness) and b* (yellowness-blueness) values of different indi-vidual and
hurdle treated goat meat samples for 0, 6, and 12 min treatment time for 0 and
24 h. Although there were some changes in L*, a* and b* values between
control and treated samples, in general, the differences were not significant (P
> 0.05) between 0 and 24 h with individual treatments. However, hurdle
2
treatments with LG þ UV-C with 100 mW cm combinations significantly (P
0.05) lowered L*, a* and b* values of treated samples compared with
untreated control samples immediately after treatment
 H.L. Degala et al. / Food Control 90 (2018) 113e120 117

Redcuction of E. coli K12, log10 CFU mL-1

7 a a a a a a

3
b b b
bbb b c c b
2 c c c c
c c c d dd d
d d d
1 d d e e e e

0
2 4 6 8 10 12
Treatment time, min
LG 0.25+UV-C 100 LG 0.25+UV-C 200 LG 0.5+UV-C 100
LG 0.5+UV-C 200 LG 1.0+UV-C100 LG 1.0+UV-C 200
Fig. 3. Reduction of E. coli K12 on goat meat surface after treatment with hurdle technologies for UV-light. Bars with different letters are significantly different (P 0.05).

Table 1
L*, a*, and b* values of individual UV-C and LG treated goat meat samples.

Treatment, mW cm 2/% Time, min L* a* b*

0h 24 h 0h 24 h 0h 24 h

UV-C 100 0 35.5b 32.8c 13.4a 14.2c 9.4a 8.3c

6 39.2a 37.1a 11.0c 23.2a 10.2a 16.6a
12 36.4b 36.5b 12.7b 17.8b 10.7a 15.0b
UV-C 200 0 35.5a 32.8c 13.4a 14.2b 9.4b 8.3b
6 33.2b 34.7b 13.4a 16.2b 13.4a 12.2a
12 35.9a 36.1a 12.8b 17.4a 8.7c 12.4a
LG 0.25 0 35.5a 32.8c 13.4a 14.2b 9.4b 8.3b
6 35.7a 37.1a 9.6b 11.3c 6.5c 6.9c
12 34.6a 35.3b 13.6a 17.8a 11.1a 17.0a
LG 0.5 0 35.5b 32.8c 13.4a 14.2b 9.4c 8.3c
6 32.0c 38.3b 12.8a 14.7a 10.0b 15.8b
12 38.7a 40.8a 13.2a 14.3b 15.1a 22.1a
LG 1.0 0 35.5b 32.8c 13.4a 14.2a 9.4b 8.3b
6 32.2c 38.5b 13.3a 12.6b 10.6b 6.5a
12 38.6a 40.4a 11.5b 13.1b 11.5a 20.5a
Values in the same column, within the same treatment with different letter are significantly different (P 0.05).

(40.1e38.2, 13.1 to 11.0, and 14.7 to 11.3), respectively. However the color
values did recover after 24 h (Table 2). Also, the values were significantly (P
0.05) increased with increased treatment time from 0 to 6 min and then
decreased with 12 min treatment time (Table 2). The findings are similar as
observed in pulsed-light-treated ready-to-eat cured meat products (Ganan,
Hierro, Hospital, Barroso, & Fernandez, 2013) and raw salmon fillets treated
by using UV-light with ultrasound (Krajnik et al., 2017). But the findings are
unlike a high-pressure treatment that changed the color and was undetectable
as meat got cooked (Jung, Ghoul, & de Lamballerie-Anton, 2003). The
changes in L*, a* and b* values of meat samples was due to the interaction of
protein myoglobin in the tissues of meat with oxygen forming oxymyoglobin,
or heme group displacement inducing color to the meat (Carlez, Veciana-
Nogues, & Cheftel, 1995; USDA, 2011). From the previous studies it can also
be hypothesized that changes in color of meat tissue are possibly due to local
temperature increase due to exposure to UV-light (Ozer & Demirci, 2006) or
oxidation of lipids leading to modified organoleptic properties of meat in
certain hurdle treat-ments (Guyon, Meynier, & de Lamballerie, 2016).
3.5.2. Texture
The WB hardness values of goat meat for individual UV-C and LG
treatments increased or decreased with increasing treatment time. The 12 min
0.5% LG treated sample had the lowest WB hardness value (11.83 N) and the
1% LG treated sample had the highest hardness value (30.96 N) (Table 3).
The differences in WB hardness values of control and treated meat samples
were insignificant (P > 0.05) for 0.25% and 0.5% individual LG treatments.
Similar ob-servations were reported for beef using low-voltage direct electric
current (Mahapatra et al., 2011). In case of hurdle treatments, the 12 min
2
0.25% LG þ UV-C with 100 mW cm treated sample had the lowest WB
hardness value (10.47 N), whereas, the 0.25% LG þ UV-C with 200 mW cm
2
treated sample had the highest hardness value (40.98 N) (Table 3). The
difference between hardness values of control and treated meat samples were
insignificant (P > 0.05) except with 0.25% LG þ UV-C with the 200 mW cm
2
hurdle treatment. In contrast to high-pressure processing that altered
hardness, juiciness and water-holding capacity of raw meat (Guyon et al.,
2016), hurdle treatments (UV-C þ LG) in this study did not affect the textural
quality of meat. The findings are similar as
118 H.L. Degala et al. / Food Control 90 (2018) 113e120

Table 2
L*, a* and b* values of hurdle treated goat meat samples.

Treatment, mW cm 2/% Time, min L* a* b*

0h 24 h 0h 24 h 0h 24 h

LG 0.25þUV-C 100 0 40.1a 36.4c 13.1b 14.6a 14.7a 13.8b

6 33.1c 38.5a 14.3a 13.5a 11.9b 17.9a
12 38.2b 37.1b 11.0c 14.1a 11.3b 17.6a
LG 0.5þUV-C 100 0 40.1a 36.4b 13.1b 14.6b 14.7a 13.8c
6 32.8c 38.3a 14.9a 11.3c 14.0a 16.1b
12 36.5b 36.0b 13.6b 16.0a 11.8b 18.3a
LG 1.0þUV-C 100 0 40.1a 36.4b 13.1a 14.6a 14.7a 13.8b
6 38.1b 37.7a 12.5a 14.2a 9.3c 10.5c
12 33.2c 37.6a 10.8b 12.7b 11.9b 21.2a
LG 0.25þUV-C 200 0 40.1a 36.4b 13.1b 14.6c 14.7a 13.8b
6 37.7b 33.1c 9.1c 20.7b 8.7c 12.7c
12 35.8c 40.6a 17.3a 21.5a 12.7b 23.0a
LG 0.5þUV-C 200 0 40.1a 36.4c 13.1b 14.6b 14.7a 13.8b
6 33.1c 42.2a 15.2a 13.1c 12.2c 8.5c
12 34.9b 39.9b 13.6b 15.1a 12.8b 16.5a
LG 1.0þUV-C 200 0 40.1a 36.4c 13.1b 14.6c 14.7a 13.8c
6 36.8c 41.2a 16.6a 17.2a 13.6b 19.9b
12 38.4b 37.0b 13.1b 15.3b 14.2a 20.5a

Values in the same column, within the same treatment with different letter are significantly different (P 0.05).

Table 3
Warner-Bratzler hardness values of non-thermal individual and hurdle treated goat meat samples.

Treatment Warner-Bratzler Hardness Values, N Treatment Warner-Bratzler Hardness Values, N

2 2
Individual, mW cm /% Control Treated Combination, mW cm /% Control Treated
0 min 6 min 12 min 0 min 6 min 12 min

UV-C 100 9.09b 16.27a 13.63a LG 0.25þUV-C 100 14.56a 12.78a 10.47a
UV-C 200 9.09b 12.25b 15.86a LG 0.5þUV-C 100 14.56a 18.27a 14.62a
LG 0.25 21.5a 15.14a 11.83a LG1.0þUV-C 100 14.56a 19.16a 15.79a
LG 0.5 21.51a 19.08a 24.94a LG0.25þUV-C 200 25.02b 19.46b 40.98a
LG 1.0 21.51b 14.81b 30.96a LG0.5þUV-C 200 25.02a 31.20a 30.54a
LG 1.0þUV-C 200 25.02a 21.50a 23.97a
Values in the same row, within the same treatment with different letter are significantly different (P 0.05).

Table 4
TBARS values of non-thermal individual and hurdle treated goat meat samples.

Treatment TBARS, mg MDA kg 1 meat Treatment TBARS, mg MDA kg 1 meat

Individual, mW cm 2/% Combination, mW cm 2/%
Control 0.42 ± 0.01b Control 0.42 ± 0.01e
UV-C 100 0.49 ± 0.07b LG 0.25þUV-C 100 1.72 ± 0.04d
UV-C 200 0.33 ± 0.01c LG 0.5þUV-C 100 0.31 ± 0.00f
LG 0.25 0.29 ± 0.00d LG 1.0þUV-C 100 3.66 ± 0.12a
LG 0.5 0.17 ± 0.00e LG 0.25þUV-C 200 0.22 ± 0.00g
LG 1.0 2.27 ± 0.01a LG 0.5þUV-C 200 2.73 ± 0.05b
LG 1.0þUV-C 200 2.41 ± 0.04c
Values in the same column with different letter are significantly different (P 0.05).

observed for raw salmon fillets using UV-light with ultrasound (Krajnik et al.,
2017). Therefore, UV-C and LG hurdle treatments seem to be a promising
alternative to conventional processing techniques in the meat industry.
3.5.3. Lipid oxidation
The TBARS values for individual UV-C and LG treatments ranged from
1 (0.21e1.21 and 0.31e4.57 mg MDA kg meat, respectively). Similar results
0.17 to 0.49 mg MDA kg meat. These treatments had shown a significant (P
0.05) decrease in lipid oxidation compared to the control except for an
increase with 1% LG treatment (Table 4). On the other hand, TBARS values
1
for hurdle treatments ranged from 0.22 to 3.66 mg MDA kg of meat, and the
values increased for certain treatments and decreased for others. The 12 min
2 al., 2010). The present study also showed a significant (P 0.05) reduction in
1% LG þ UV-C with 100 mW cm hurdle treatment had the highest TBARS
1
value (3.66 mg MDA kg meat) compared to the control.
2
However, the 2 min 0.5% LG þ UV-C with 100 mW cm and 8 min 0.25%
2
LG þ UV-C 200 mW cm hurdle treatments decreased these values to 0.31
1
and 0.22 mg MDA kg of goat meat, respectively (Table 4). The TBARS
values were within the range reported by Rababah et al. (2011) in another
study on ground fresh goat meat treated with natural green tea or commercial
grape seed in com-bination with synthetic tert-methyl-butylhydroquinone
1
were reported by other studies, including cooked pork patties treated with
0.05% clove, rosemary, or cassia bark extracts (Kong, Zhang, & Xiong,
2010), porcine and bovine ground meat treated with oregano and sage (3%
w/w) (Fasseas, Mountzouris, Tarantilis, Polissiou, & Zerva, 2008) and in fresh
chicken breast meat treated with thyme and balm essential oils (Fratianni et
 H.L. Degala et al. / Food Control 90 (2018) 113e120
oxidation of lipids with certain combination treatments and a sig-nificant (P
0.05) increase with the other combination treatments compared to the control
(Table 4). However, the hurdle treatment (1% LG þ UV-C with 200 mW cm
2
) that reduced bacterial con-centrations below detection levels increased the
1
oxidation (2.41 mg MDA kg ), but by a lesser amount than oxidation levels
observed by Rababah et al. (2011) in fresh ground goat meat. The chemical
and thermal reactions initiated due to the exposure of meat to UV-light and
LG might have induced oxidative and thermal deteriora-tion resulting in lipid
oxidation, as reported by Rahman, Park, Sang, Al-Harbi, and Oh (2012) in
fresh chicken breast meat with slightly acidic low concentration electrolyzed
water.
4. Conclusions
This study shows that the UV-C and LG processes applied indi-vidually
had significant effects on microbial reduction on goat meat. The hurdle
technology of these selected non-thermal pro-cesses showed much improved
inactivation of E. coli K12 to below detection levels. In both individual and
hurdle treatments, increasing treatment time from 2 to 12 min had an
insignificant (P > 0.05) effect on bacterial reductions, whereas increasing the
intensity of UV-C and concentration of LG significantly (P 0.05) increased
bacterial reduction on goat meat. In conclusion, this study demonstrated that
the hurdle approach with UV-C and LG can be successfully applied to
improve the microbial quality of goat meat. However, enrichment of the
medium, indicating chances of recovery of bacterial cells over a period, as
well as changes in quality attributes, such as color and oxidation of lipids,
make it necessary to optimize the treatment conditions to enhance the
antibacterial effect of this hurdle technology on foodborne patho-gens in raw
meat. Sensory testing for taste and odor should be performed to determine
changes in sensory attributes of goat meat due to LG that might affect
consumer acceptance. An alternative approach such as incorporation of LG in
an edible film coat or nanoencapsulation to mask its strong smell may be
considered. Also, future research should be performed for large scale systems,
and mathematical models should be developed to predict the effective
application of hurdle technologies in the food industry.
Acknowledgements
This work was supported by the USDA National Institute of Food and
Agriculture, Evans-Allen project under accession number 1001168 and the
1890 ARD Food Safety Consortium (Food Safety research, teaching and
outreach program for 1890 land-grant universities).
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