Accepted Manuscript: 10.1016/j.ifset.2017.07.006
Accepted Manuscript: 10.1016/j.ifset.2017.07.006
Accepted Manuscript: 10.1016/j.ifset.2017.07.006
PII: S1466-8564(16)30239-9
DOI: doi: 10.1016/j.ifset.2017.07.006
Reference: INNFOO 1789
To appear in: Innovative Food Science and Emerging Technologies
Received date: 31 August 2016
Revised date: 5 April 2017
Accepted date: 3 July 2017
Please cite this article as: I. Albertos, A.B. Martin-Diana, P.J. Cullen, B.K. Tiwari, S.K.
Ojha, P. Bourke, C. Álvarez, D. Rico , Effects of dielectric barrier discharge (DBD)
generated plasma on microbial reduction and quality parameters of fresh mackerel
(Scomber scombrus) fillets, Innovative Food Science and Emerging Technologies (2017),
doi: 10.1016/j.ifset.2017.07.006
This is a PDF file of an unedited manuscript that has been accepted for publication. As
a service to our customers we are providing this early version of the manuscript. The
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journal pertain.
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1
Agrarian Technological Institute of Castilla and Leon (ITACyL). Ctra. Burgos Km
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2
School of Food Science & Environmental Health, Dublin Institute of Technology,
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Dublin, Ireland.
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Teagasc Food Research Centre, Ashtown, Dublin 15, Ireland.
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*Corresponding authors: [email protected] / [email protected]
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Abstract
The effect of atmospheric cold plasma generated by a novel in-package dielectric barrier
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investigated. DBD voltage (70kV and 80kV) and treatment time (1, 3 and 5 minutes)
However, significant effects on lipid oxidation parameters (PV, dienes) were observed
for the treated samples. Both studied treatment factors, treatment voltage and time,
changes in pH or colour (except for L*) were observed. These results suggest
fish processing, retaining product quality over its shelf life. However, further
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investigations are needed in order to implement this technology and to control and
Key words: Dielectric barrier discharge; cold atmospheric plasma; Atlantic mackerel;
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1.Introduction:
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Several research works have identified the potential of atmospheric cold plasma for
equilibrium (Schlüter et al., 2013; Surowsky, Schlüter, & Knorr, 2014). Although they
contain high temperature electrons, the neutrals, ions, and radicals remain close to room
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temperature and as such they are considered cold plasmas with limited macro heating of
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material to which they interface with (Misra et al., 2015; Mishra, Bhatia, Pal, Visen, &
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Trivedi, 2016; Min et al., 2017). Cold plasma may be generated by a diversity of
dielectric barrier discharge (DBD), atmospheric pressure plasma jet (APPJ), microwave
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Industrially cold atmospheric plasma equipment has not implemented in food industry
for direct food contact but is employed for packaging and label modification. The main
limitation is the necessity of working under vacuum and thus incompatible with food
processing (Misra, Keener, Bourke, Mosnier, & Cullen, 2014). Experimentally plasma
jet and dielectric barrier discharges (DBD) have been studied. Plasma jet typically
operate with noble gases (Misra, Tiwari, Raghavarao, & Cullen, 2011), which increase
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the cost of treatment. Ideally, ambient air would be use in the cold plasma technology in
order for food industry to implement this technology. In this sense, previous studies
atmospheric cold plasma inside sealed packages filled with air through the application
of sufficiently high voltages (Misra et al., 2014; Misra, Ziuzina, Cullen, & Keener,
2013; Pankaj, Misra, & Cullen, 2013). Dielectric barrier discharges are generated when
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high voltage is applied across the electrodes. These discharges generate energetic
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electrons that dissociate oxygen molecules by direct impact. This single O atom
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combines with oxygen molecules (O2) to form ozone gas (Misra et al., 2014). Another
advantage, in comparison with other cold plasma´s generators, is the treatment takes
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place inside sealed packages, which eliminates the risk of post-process contamination
and facilitates rapid treatment times as the resultant reactive species are contained
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within the package and continue to act post treatment (Misra et al., 2014).
Dielectric barrier discharges have successfully applied on food retaining food quality in
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dry products such as wheat flour (Misra et al., 2015), legumes such as peas (Bußler et
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al., 2015), dried laver (Kim, Puligundla, & Mok, 2015) or vegetables such as tomatoes
(Pankaj et al., 2013; Misra et al., 2014), spinach (Klockow & Keener, 2009) and fruits
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such as strawberries (Misra et al., 2014), grapes (Moon, Noh, Moon, & You, 2013),
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fresh-cut melon (Tappi et al., 2015) and orange juice (Almeida et al., 2015).
The activity of microorganism is the main factor limiting the shelf life in fresh fish
(Ólafsdóttir et al., 1997). However, there are no available studies concerning the effects
of cold plasma on the spoilage microbiology and quality of fish. Plasma sources for
decontamination of foodstuff such as meat, have been reported (Noriega, Shama, Laca,
Díaz, & Kong, 2011; Kim et al., 2011; Rød, Hansen, Leipold, & Knøchel, 2012; Kim,
Yong, Park, Choe, & Jo, 2013). However, the suitability of ACP for high lipid
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oxidation due to the formation of hydroxyl acids, keto acids, short-chain acids and
aldehydes (Misra, Tiwari, Raghavarao, & Cullen, 2011). The effect of ACP on food
quality parameters in meat products has not been studied extensively. Further studies
should be conducted to clarify these results. Kim et al. (2011) did not find any
significant changes due to plasma jet treatment (pH, TBARS, microscopic observation)
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except for colour, mainly L* values of the meat surface was increased. Rød et al. (2012)
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demonstrated that TBARS values of plasma treated samples increased with power and
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storage time but that the plasma did not induce measurable colour differences. Kim et
al. (2013) found lower TBARS values in plasma treated bacon than the control upon
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treatment, but increased subsequently as a function of storage. Also, significant
reductions in the sensory quality parameters were observed in plasma treated samples.
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There are few reports of DBD treatment on meat products. Jayasena et al. (2015)
observed minor deterioration of fresh pork and beef quality. Only high exposure time
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(10 minutes) caused lipid oxidation. Furthermore colorimetric measures showed that
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L* was not affected by DBD, whereas a* values were lowered significantly after 5 and
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7.5 min of DBD exposure. Wang, Zhuang and Zhang (2016) demonstrated that DBD
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The objectives of this study were to investigate the effects of different conditions
(voltages and times) for DBD on the treatment of fish spoilage bacteria, and how this
fillets.
2.1. Chemicals
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All the chemicals were analytical grade obtained from Sigma-Aldrich (Wicklow,
Ireland). All the solvents were HPLC grade and also purchased from Sigma-Aldrich
Six kilos of Atlantic mackerel (Scomber scombrus) caught in early February 2015 were
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purchased in Stevie Connolly Seafood (Dublin, Ireland). The average weight for each
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2.3. In-package plasma treatment
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Two fillets were packaged in commercial 270 µm-thick polyethylene terephthalate trays
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(150 mm x 70 mm x 35 mm) and sealed with a high barrier-50 µm film. A plasma
discharge was generated inside the trays using dielectric set-up, as shown in Figure 1.
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The package was placed between two circular aluminium plate electrodes (outer
polypropylene sheet was used to stabilize the discharge. The electrode separation was
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adjusted to the tray height of 35 mm. The applied voltage to the electrode was
frequency of 50 Hz, the input to which is regulated using a variable transformer. The
samples were treated in triplicate at two discrete voltages of 70 and 80 kV for different
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treatment times (1, 3 and 5 minutes). The experiment was performed in duplicate. The
atmospheric air conditions at the time of treatment were 15ºC and 50% relative
(Testo 176T2, Testo Ltd., UK). Control and treated packages were stored at 4ºC. In
order to maximize antimicrobial efficacy of the treatment, samples were stored for 24-h,
allowing interaction of the metastable reactive species with the product and subsequent
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reaction or reversion of the reactive species to the original gas composition (Ziuzina,
Fish samples (10 g) were aseptically transferred into bags (Seward 80 bags, United
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with a Stomacher blender for 5 min (Seward, London, UK). For each sample,
appropriate serial decimal dilutions were prepared in MRD for the following
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microorganism counts:
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(i) Total aerobic mesophilic bacteria were determined using Tryptic Glucose Yeast Agar
15ºC for 72 h.
(iii) Lactic acid bacteria (LAB) on double-layer Man Rogosa Sharpe medium incubated
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at 30ºC for 72 h.
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25 °C for 48 h.
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pH
The pH of fillets was measured at room temperature using a portable pH meter (Orion
Proximate composition
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lipids were extracted from 10-g samples with methanol/chloroform (1:1, v:v) according
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The fatty acid profile of the samples was determined in triplicate from the Bligh & Dyer
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dryness under nitrogen. The remaining residue was dissolved in 1 mL of hexane and a
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methylation procedure carried out by adding 100 μL of 0.5M methanolic KOH and
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leaving the reaction for 10 min at room temperature (RT). The upper layer was
transferred to a 2-mL vial. Analysis of fatty acid methyl esters (FAME) were carried out
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equipped with a DB-23 column 60 m x 0.32 mm, (0.25 µm film thickness) (Agilent
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Technologies, Palo Alto, CA, USA) and a flame ionisation detector. Helium was used as
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the carrier gas. The oven temperature was programmed to 50 ºC for the first 7 min and
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increased to 200 ºC at a rate of 25 ºC/min; then, the temperature was increased to 230 ºC
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at a rate of 3 ºC/ min and held for 26 min. Injector and detector temperatures were 250
ºC and 280 ºC, respectively. One µL of the hexane extract was injected in split mode
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(ratio 25:1), and FAMEs were identified by comparison of retention times with those of
37 FAME’s standard mix (Supelco, Sigma Aldrich, CO). Polyene ratio was calculated
on the basis of fatty acid composition, being ([20:5] + [22:6]) 100/ [16:0]. The ratio
PV was measured directly on the Bligh & Dyer extract according to the method
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Conjugated hydroperoxides were measured on the Bligh and Dyer extract dissolved in
hexane, as described by Undeland, Stading and Lingnert (1998). The absorbance was
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measured at 268 nm and results were calculated as mmoles of hydroperoxides per
kilogram of oil.
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Thiobarbituric acid reactives substances (TBARS)
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Samples were analysed using the methodology described by Vyncke (1975) on a 5%
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trichloracetic acid extract of the restructured fish muscle. Results were expressed as mg
The colour parameters lightness (L*), redness (a*) and yellowness (b*) were measured
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using a colorimeter (Colour Quest XE Hunter Lab, Northants, UK). The illuminant was
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D65 (colour temperature of 6504 K) and the standard observer was 10º. The
colorimeter was standardised using a light trap and a white calibration plate.
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Measurements were taken on the samples packaged in transparent plastic bags at three
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different points.
Ten grams of mackerel were placed in sealed NMR tubes and held at 25ºC in a water
bath for 1 h. NMR data were generated using a Mara Ultra Instrument (Oxford
The data were subjected to One-way ANOVA. Fisher LSD (Least Significant
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Difference) test was applied for determining group differences at 95% confidence level.
Statgraphics Centurion XVI was used for carrying out the statistical analysis.
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3. Results & Discussion
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3.1. Effect of cold plasma on microbiological growth
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Figure 2 shows the changes in the microbial flora of Atlantic mackerel subjected to
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ACP. The initial total aerobic mesophilic bacteria (control) were 4.1±0.07 log CFU g-1,
which is comparable to values reported in the literature of between 3.0 and 5.0 log CFU
g-1 on filleted fisht (Dalgaard, Gram & Huss, 1993; Chytiri, Chouliara, Savvaidis, &
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Kontominas, 2004). There was no significant (P>0.05) reduction in the total aerobic
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Total aerobic psychrotropic bacteria incubated at 15ºC were higher in Atlantic mackerel
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microorganism counts depending upon the incubation temperature related to the nature
psychrotrophic bacteria was more dependent on plasma exposure time than on voltage
applied. In any case, the most effective reduction was achieved using the highest
LAB counts were lower than Pseudomonas counts. LAB were also found to be more
dominant storage. This finding can be explained due to the inhibition of other bacteria
by the formation of lactic acid and bacteriocins (Gram & Dalgaard, 2002). Besides,
LAB can grow under both anaerobic and aerobic conditions. Other authors found
Pseudomonas to be the dominant microflora for filleted chilled fish (Chytiri et al.,
2004). Both microorganisms (LAB and Pseudomonas) were found to display greater
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sensitivity to applied voltage than treatment time. Kim et al. (2011) studied the effect of
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atmospheric pressure plasma on inactivation of pathogens (L. monocytogenes, E. coli
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and S. typhimurium). Concerning LAB and Pseudomonas, the previous work along with
the present study, demonstrated that plasma treatment at high voltage was effective for
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reducing fish spoilage microorganism over short time periods. Wang et al. (2016)
media.
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Ozone is one key metastable generated in large quantities by DBDs and which can be
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measured relatively easily inside of the package Wang et al. (2016) claimed that ozone
is a relatively long half-life compared to other reactive species formed during discharge.
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Other reactive oxygen species (ROS) such as atomic oxygen (O) and hydroxyl radicals
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(OH) are also generated and they can react with almost all bacteria cell resulting in
damage to DNA proteins, lipids and membranes (Kim et al., 2011; Kim et al., 2013).
The prototype in-package system used in this study has previously been characterised
using electrical and optical diagnostics (Moiseev et al., 2104). The post-discharge gas
composition within the sealed packages were quantified using UV–Vis absorption
spectroscopy. The concentration of ozone and nitrogen oxides (O3, NO2, NO3, N2O4)
was found to increases with treatment time however a strong decrease in O3 levels was
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nitrogen oxides is ascribed to high specific power densities in the closed container and
to increasing RH levels. Humid air large gap DBD plasmas in closed containers
generate along with O3, high levels of nitrogen oxides and HNOx (x = 1, 4) acids which
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3.2. Effect of cold plasma on physicochemical parameters
pH
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The pH values were similar to values reported in the literature for Atlantic mackerel
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(Senturk & Alpas, 2013). Atlantic mackerel did not show any clear trend in pH
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behaviour after plasma exposure (Figure 3).
There were no differences on the pH levels of Atlantic mackerel after DBD treatments
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with the exception of 80 kV at 5 min. These results were consistent with Kim et al.
(2011) and Ulbin-Figlewicz, Brychcy and Jarmoluk (2013), where cold plasma did not
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induce pH changes.
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The pH values of the samples submitted to 80 kV at 5 min were clearly the highest.
Furthermore, there was not an apparent relationship between pH and bacterial growth.
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pH has been reported to be a poor indicator of microbial growth and fish freshness
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(Alfaro, Hernández, Baliño-Zuazo, & Barranco, 2013). Nevertheless, Senturk and Alpas
(2013) specified that fresh Atlantic mackerel with a pH higher than 7.00 was considered
to be spoiled. All treatments tested maintained values under this critical limit.
Proximate composition
Moisture and fat content of Atlantic mackerel were found to be in the range of 69.91-
68.11 and 14.14-14.9 g 100 g-1, respectively. Both results agreed with previous studies
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on Atlantic mackerel (Torres, Vázquez, Saraiva, Gallardo, & Aubourg, 2013; Aubourg,
Rodríguez, & Gallardo, 2005). Fat and moisture content did not change for the
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Fatty acid composition (FA)
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Analysis of fatty acid profiles detected that docosahexaenoic acid (DHA, C22:6 n-3)
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was the most abundant polyunsaturated fatty acid, and palmitic acid (C16:0) and oleic
acid (C18:1, n-9) the main saturated and monounsaturated fatty acids, respectively. This
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is in agreement with previously reported data (Maestre, Pazo, & Medina, 2011).
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Fatty acids composition of the treated samples was modified by ACP, as shown in Table
1. The levels of oleic acid (C18:1, n-9) and eicosapentaenoic acid (EPA, C20:5 n-3)
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were lower for the control samples compared to plasma treated samples. These
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reductions can be attributed to the reactive oxygen and nitrogen species generated and
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Polyene ratio also reflected the loss of 3 PUFAs (C: 20:5 and C: 22:5) for the control
samples. Another study showed that there was no significant correlation between total
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amount of PUFAs and mackerel shelf life in term of oxidation (Maestre et al., 2011).
Primary oxidation was followed by PV and dienes assessment (Table 2). Control
samples had 6.89 milliequivalents of O2 per kilogram of oil. Ozogul and Balikci (2013)
reported similar initial PV. A significant (P<0.05) primary oxidation (PV and Dienes)
development was observed for DBD treatment. A comparison of different voltages (70
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kV and 80 kV) and treatment time (1, 3 and 5 min) showed both variables increased the
rate of oxidation. Similarly, Joshi et al. (2011) suggested that lipid oxidation is
Vandamme, Leys and De Winne (2014) also revealed that cold plasma caused the
formation of several volatiles related to lipid oxidation. ACP can generate reactive
species that have strong oxidation capacities. During DBD treatment, free radicals are
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generated that trigger lipid oxidation (Kim et al., 2013).
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TBARS values ranged from 0.74±0.01 to 0.75±0.00 mg of malondialdehyde (MDA) per
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kilogram of fish. There were no significant differences (P>0.05) between control and
samples submitted to ACP treatment. The effect of ACP on lipid oxidation measured
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through TBARS values is not clear. Whereas, Rød et al. (2012) and Kim et al. (2013)
reported higher TBARS values for plasma treated samples on bresaloa and pork loin,
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Kim et al. (2011) found lower TBARS values of plasma treated bacon, however this
trend reverted over storage. The TBARS values of DBD plasma treated pork and beef
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samples were unmodified up to a treatment time of 7.5 minutes (Jayasena et al., 2015).
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Colour has a direct influence on the acceptance of fish and influences consumers´
No clear trend was found between any plasma treated conditions, similar to those
evident for the plasma treated samples compared to control samples. Kim et al. (2011,
2013) also observed that the L* value decreased for bacon and pork loin treated with
ACP. There were not differences between ACP treated samples and controls for a* and
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b* values. These results indicated that the ACP did not influence on the colour
markedly.
NMR provides useful information about the interactions between water and myofibrillar
meat proteins (Table 4). Three peaks are thought to be directly related to three water
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components in muscle tissue. The first component is water closely associated (“bound”)
with macromolecules (T2b). T21 is immobilised water, which is located in the protein-
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dense myofibrillar network. The final component is extramyofibrillar water or free
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water (T22). Table 4 shows that water tightly bound to macromolecules (T2b) is not
influenced by DBD treatment. Similarly, Bertram et al. (2001) demonstrated the T2b did
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not reflected any mechanical stress and micro or macro-structural changes in the meat
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matrix. In all treatments, the majority of water is trapped by the dense myofibrillar
network (T21). A significant decrease in T21 was however observed for plasma treated
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samples. This is probably due to the fish structure alteration, which will weaken the
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matrix that is trapping the T21 water. Simultaneously, extramyofibrillar water (T22)
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4. Conclusions
DBD is shown to be a potential treatment for reducing the spoilage bacteria (total
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voltage and time were both found to have significant effects on microbial inactivation.
Results indicated that ACP caused changes in immobilised (T21) and extramyofibrillar
(T22) water, but no differences were found in water closely associated to molecules
(T2b). Processing conditions of DBD treatment (voltage and time) rendered the mackerel
more susceptible to lipid oxidation. However, ACP does not affect adversely
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Acknowledgements
Irene Albertos is recipient of a doctoral fellowship awarded by the National Institute for
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Figure 1
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d
6 c
b
d e ab bc bc
5 cd c a
log cfu g-1 sample
2 Pseudomonas
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Control 70kV 1min 70kV 3min 70kV 5min 80kV 1min 80kV 3min 80kV 5min
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Figure 2
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6.45
b
6.4
6.35
a a a a a
6.3
a
pH
6.25
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6.2
6.15
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6.1
Control 70 kV 70 kV 70 kV 80 kV 80 kV 80 kV
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1 min 3 min 5 min 1min 3min 5min
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Figure 3
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Figure 1: Schematic of the experimental set-up for DBD of Atlantic mackerel fillets.
DBD treatments.
Different letters have mean values that are significantly different (p<0.05) due to the treatment among the same microorganism.
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Figure 3: pH of Atlantic mackerel fillets submitted different DBD treatments.
Values (mean ± standard deviation. n=3) followed by different lowercase letter in same column are significantly different (p<0.05).
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Table 1: Main fatty acid composition of Atlantic mackerel submitted different DBD
treatments.
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70kV 1min 0.66±0.01abc 0.26±0.01b 0.28±0.03a 1.00±0.00c 1.95±0.06
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70kV 5min 0.83±0.01cd 0.40±0.00d 0.59±0.08c 1.00±0.00c 1.91±0.13
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80kV 1min 0.54±0.02a 0.34±0.01cd 0.46±0.03bc 1.00±0.00c 2.71±0.08
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PV (meq. active oxygen/kg lipids) Dienes (mmol of hydroperoxides/kg
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lipid)
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Table 3: Color (L*, a* and b*) of Atlantic mackerel submitted to different DBD
treatments.
L* a* b*
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Control 57.42±2.15d 3.67±0.63ab 14.12±2.75ab
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70kV 3min 51.70±0.50ab 3.96±0.06bc 13.21±0.55ab
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70kV 5min 53.87±1.26bc 4.19±0.29bc 15.13±0.12b
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Table 4: NMR parameters (T2b, T21, T22) area of Atlantic mackerel submitted to different
DBD treatments.
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Control 8814±3879a 331221± 1466d 10327±1573a
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70kV 3min 22221±1959b 300835±3826c 14576±2572c
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70kV 5min 295586±1015b 22705±3159d
273197±3769a
12774±1033ª
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14029±1033a
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0±0
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Industrial Relevance
Cold atmospheric plasma (CAP) has gained attention as an emerging and non termal
technology for decontamination of food. This technology has been used on fruits and
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technology has not been investigated in fish, being a highly persibale product.
The use of dielectric barrier discharge (DBD) to produce cold plasma showed a
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potential industrial application at low cost and convenience. Cold plasma was found to
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be effective for reducing the main problem of oily fish quality such as the spoilage
bacteria. However, this technology seems to accelerate oxidative pathways; for this
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reason, further studies to investigate the use of antioxidants in combination with cold
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Highlights
studied.
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DBD caused changes in inmobilised and extramyofibrillar water.
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