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Accepted Manuscript
Effects of packaging parameters on the inactivation of Salmonella contaminating
mixed vegetables in plastic packages using atmospheric dielectric barrier discharge
cold plasma treatment
Su Yeon Kim, In Hee Bang, Sea. C. Min
PII:
S0260-8774(18)30357-1
DOI:
10.1016/j.jfoodeng.2018.08.020
Reference:
JFOE 9370
To appear in:
Journal of Food Engineering
Received Date: 25 May 2018
Revised Date:
18 August 2018
Accepted Date: 18 August 2018
Please cite this article as: Su Yeon Kim, In Hee Bang, Sea. C. Min, Effects of packaging parameters on
the inactivation of Salmonella contaminating mixed vegetables in plastic packages using atmospheric
dielectric barrier discharge cold plasma treatment, Journal of Food Engineering (2018), doi: 10.1016/
j.jfoodeng.2018.08.020
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to
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ACCEPTED MANUSCRIPT
Highlights
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Atmospheric cold plasma (ACP) decontaminates mixed vegetables in plastic
containers
Effective container parameters include the kinds of plastics and package shape
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Effective treatment parameters are container shaking and sample–electrode distance
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Other key parameters are secondary packaging and headspace-sample volume ratio
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Effects of packaging parameters on the inactivation of Salmonella contaminating
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mixed vegetables in plastic packages using atmospheric dielectric barrier discharge
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cold plasma treatment
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Su Yeon Kim, In Hee Bang, Sea. C Min*
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Department of Food Science and Technology, Seoul Women’s University,
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621 Hwarangno, Nowon-gu, Seoul 01797, Republic of Korea
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Short version of title: Packaging requirements for in-package plasma treatment
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*Corresponding author. Tel.: +82-2-970-5635; fax: +82-2-970-5977.
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E-mail address: smin@swu.ac.kr
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Abstract
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Effects of packaging parameters on the inactivation of Salmonella contaminating mixed vegetables
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in plastic packages using atmospheric dielectric barrier discharge cold plasma treatment (ADCPT)
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were investigated. The inactivation rate of indigenous aerobes of grape tomatoes in low density
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polyethylene packaging (1.2 log CFU/tomato) was higher than that in polyethylene terephthalate
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packaging (0.8 log CFU/tomato). Increasing oxygen concentration in the package headspace by 85%
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did not affect the Salmonella reduction rate. However, an increase in the volume ratio of headspace
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to sample from 30:1 to 43:1, a change from indirect treatment to direct treatment, and the use of
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secondary packaging led to an increase in the Salmonella reduction rates by 1.2, 2.3, and 0.7 log
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CFU/tomato, respectively. The water vapor permeability of the tested packages increased after
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ADCPT by 16.7–41.7%, while tensile properties, transparency, glass transition temperature, and
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surface morphology did not change. Differences in inactivation effects according to package shape
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were eliminated by shaking during treatment. The results demonstrated the packaging parameter-
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dependent efficacy of in-package ADCPT and effective ADCPT for mixed vegetable
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decontamination with minimal package property modification.
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Keywords: cold plasma, packaging, Salmonella, vegetable, tomato
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1. Introduction
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Many studies have addressed the emerging nonthermal technologies used in food processing to
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minimize undesirable effects of conventional thermal technologies, including supercritical fluids,
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ultrasonics, high hydrostatic pressure, pulsed electric fields, and cold plasma for improved food
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storability and microbiological safety (Amaral, et al., 2017; Misra et al., 2017). Cold plasma (CP)
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treatment has been investigated to promote microbial decontamination and modify the food material
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to have the desired characteristics, while maintaining its texture and nutritional and functional
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properties (Coutinho et al., 2018). CP treatment inactivates microorganisms in foods through the
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action of highly energetic species (e.g., ions, free radicals, electrons, and ultraviolet photons) that
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break covalent bonds and initiate various chemical reactions (Kim et al., 2014; Pignata et al., 2017).
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However, the efficacy of CP treatment on microbial decontamination requires further elucidation for
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appropriate applications of quality assurance systems by the food producers (Da Cruz et al., 2006).
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Furthermore, considering oxidative action of CP, the sensorial impact of the treatment has to be
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assessed using adequate evaluation methods (Pacheco et al., 2018; Tappi et al., 2014).
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Atmospheric dielectric barrier discharge cold plasma treatment (ADCPT) has received increasing
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attention from the food industry because the generation of CP inside a sealed container prevents
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post-process contamination of the treated food (Li and Farid, 2016). This is particularly beneficial for
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pre-packaged fresh-cut ready-to-eat foods and allows this in-package treatment to be potentially
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combined with modified atmosphere packaging for enhanced microbial safety and preservation
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(Bourke et al., 2017).
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Recently, the sales and distribution of mixed vegetable salads, a type of fresh-cut ready-to-eat
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foods, have steadily increased. However, foodborne pathogen outbreaks through the consumption of
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mixed vegetable salad continue to be reported (Center for Disease Control and Prevention (CDC),
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2016), indicating that the microbial-inactivation process currently applied for mixed vegetable salad
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does not ensure the microbial safety of the product. Hence, a novel technique for the microbial
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inactivation of mixed vegetable salads is required.
The microbial inactivation efficacy of ADCPT is influenced by the composition and quantity of
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CP reactive species as well as the possibility of contact between the reactive species and food
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(Laroussi and Leipold, 2004), both of which can be influenced in turn by the packaging parameters,
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including the packaging material, package headspace composition, and others. Thus, the packaging
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parameters are of interest for industrial application of ADCPT. However, the effects of ADCPT on
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microbial inactivation according to packaging conditions have not yet been reported. In addition, it is
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crucial to check for any changes in package properties following ADCPT to distribute the packaged
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food products appropriately as commercial products. Furthermore, effects of in-package cold plasma
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treatment on the inactivation of microorganisms on a vegetable, such as grape (cherry) tomato or
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lettuce, have been previously reported (Min et al., 2017; Min et al., 2018; Misra et al., 2014c).
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However, mixed vegetables have not been tested and this is necessary to evaluate this technology as
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a microbial decontamination method for mixed vegetable salads, one of the most common fresh-cut
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ready-to-eat foods. Thus, the objectives of the present research were (i) to determine the main
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packaging conditions that affect ADCPT’s microbial inactivation efficacy by considering the kind of
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packaging material, package shape (rigid package vs. flexible pouch), package headspace gas
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composition, ratio of headspace volume to sample volume, distance between the sample and
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electrode, and use of secondary packaging; and (ii) to verify whether ADCPT is a technology that
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can inactivate the microorganisms on food products while maintaining the properties of the
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packaging material, such as water vapor permeability, tensile strength, percentage elongation at
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break, opacity, thermodynamic properties, and surface morphology.
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2. Materials and methods
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2.1. Preparation of mixed-vegetable sample
Mixed vegetable samples were prepared for the Salmonella inactivation study, each containing 4
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pieces of romaine lettuce (25 × 70 mm, 1 g each), 4 pieces of red cabbage (10 × 60 mm, 1 g each),
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14 pieces of carrot (3 × 3 × 50 mm, 0.7 g each) and 1 grape tomato (~8 g). Mixed vegetable samples
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were immersed in a 300 ppm sodium hypochlorite solution and gently rubbed for 3 min, followed by
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being sprayed with ethyl alcohol and rubbed for 10 s; they were then washed by being immersed in
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distilled water five times. Washed samples were dried for ~2 h and inoculated with Salmonella. The
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experiments studying the inactivation of indigenous mesophilic aerobic bacteria and indigenous
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yeast and molds used the mixed vegetable samples that had been washed by a single immersion in
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distilled water for 30 s. The sample preparation, packaging, and microbial analysis were all
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performed in a laminar-flow biohazard hood (SterilGARD, Baker Company, Inc. Sanford, ME,
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2.2. Packaging parameters
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The kind of packaging material was one of the parameters considered when studying the
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inactivation effect of ADCPT for decontaminating vegetables in plastic packages. Commercially
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available low density polyethylene (LDPE) (linear low density polyethylene 50-μm thickness;
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Packline, Seoul, Korea), and a composite of nylon (3%)-LDPE (Hanmipojang, Busan, Korea) were
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used to create flexible pouch packages. LDPE, polypropylene (PP, 50-μm thickness; Packline) and
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polyethylene terephthalate (PET, 50-μm thickness; Packline) films were used to construct rigid
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containers (Fig. 1a-c). The rigid containers were built on a supporting frame (Fig. 1d) made by
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removing the lid and cutting the side and bottom areas of a commercially available PET rigid
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container (700 mL volume, 85 cm2 base area) using a razor. The frame was tightly wrapped with the
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LDPE, PP, or PET film, and the open ends of the films were heat-sealed, forming a rigid container
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(Fig. 1d). The gas in the package headspace was atmospheric air and the volume ratio of headspace
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and sample (HSR) was 30:1 in this experiment. The distance between the sample and electrode was
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set at 0 cm (direct treatment, Fig. 4), which is described more in detail later. Secondary packaging
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was not used in this experiment.
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The package shape was used as another packaging parameter. Three shapes of packages were
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made for the experiment: a PET clamshell package (700 mL volume, 85 cm2 base area) (Fig. 2a), a
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rigid container made of the supporting frame and the LDPE film (Fig. 2b), and a flexible pouch (700
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mL volume, 50 μm thickness; Fig. 2c). Both the clamshell package and the rigid container are “rigid
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packages”, with a wide headspace between the food and the packaging, compared with the pouch
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package made without the frame (Fig. 3). Open ends of the pouch packages were heat-sealed after
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food samples were inserted. The experiments using the package shape as a packaging parameter
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were conducted with and without the shaking of packages during ADCPT to test the effect of
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shaking on the microbial inactivation by ADCPT. The other conditions were identical to those used
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in the experiment studying the kind of packaging material.
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The package headspace gas composition, the third parameter investigated, was varied to examine
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if modified atmosphere packaging (MAP), which is applied to extend the shelf-life of RTE
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vegetables (Farber et al., 2003), influences the inactivation effect of ADCPT. For the package
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headspace gas composition, CO2 was the control gas, set at 10%, while the nitrogen concentration
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was varied between 0 and 90%, with the remainder being oxygen (oxygen concentration varied
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between 85 and 5%). The selected gas compositions fell within the range of gas compositions
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recommended for the MAP conditions for tomato, lettuce, and cabbage. A pouch package made of a
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composite film of nylon and LDPE was used in this experiment. The additional conditions included
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30:1 HSR, direct treatment, and no secondary packaging.
The fourth parameter to be investigated was HSR. These experiments used the rigid containers
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made of the supporting PET frame and LDPE film, with a volume of either 700 or 1,000 mL, to set
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the HSR as 30:1 or 43:1, respectively (Fig. A.1). The base areas of the 700 and 1,000 mL containers
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were 85 and 125 cm2, respectively. The other conditions included atmospheric air-plasma treatment,
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direct treatment, and no secondary packaging.
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The effect of the distance between the sample and electrode, more specifically, between the
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geometric centers of food and treatment reactor on the inactivation efficacy of ADCPT was also
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investigated. The distance for direct treatment was set to 0 cm, while the distance for indirect
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treatment was set to 15 cm (Fig. 4). The package used in the experiment was the rigid LDPE
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container with the PET frame (Fig. 2b), with a base area of 195 cm2, giving an HSR of 52:1. The
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treatment used in this experiment was an atmospheric air-plasma treatment without secondary
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packaging. The results from these experiments would be useful in investigating the efficacy of
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ADCPT under circumstances where the packaged food is not accurately positioned between the
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electrodes, for example, when a commercially available conveyor belt is used for continuous
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application of ADCPT.
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Finally, the effect of secondary packaging on the efficacy of ADCPT was investigated. The
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clamshell package (Fig. 2a) was used as the primary packaging, while the secondary packaging
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involved wrapping the clamshell-packaged sample with LDPE film (Fig. 5). The LDPE film was
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attached to the top and bottom of the clamshell package using a laminate glue to eliminate any empty
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space, and the three sides of the open film were tightly heat-sealed. In this experiment, a direct
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atmospheric air-plasma treatment was used with an HSR of 30:1.
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2.3. ADCPT
The ADCPT system used in this study (SWU-4, Seoul Women’s University, Seoul, Korea; Fig. 6),
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which generates a plasma field between the base dielectric barrier and the upper aluminum
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rectangular electrodes (20 × 16 cm) (AL6061; Kwang-lim Co. Ltd., Hwasung, Korea), was
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manufactured by Renosem (Bucheon, Korea). Packaged samples were placed in the gap between the
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upper electrode and borosilicate glass (dielectric barrier, 29 × 25 cm, thickness 0.4 cm). The gap
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distance was maintained at 6 cm. An AC power supply (220 V, 60 Hz) delivering a high voltage (up
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to 50 kV, peak-to-peak voltage) was coupled to the aluminum electrodes. The voltage measurement
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was conducted using a high-voltage electric probe (EP-50, Pulse Electronic Engineering Co., Ltd.,
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Noda, Japan). The output of the probe was displayed on a digital oscilloscope (TDS-3012b
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Oscilloscope, Tektronix, Beaverton, OR, USA).
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Treatment time was 3 min for all treatments. The shaking, which lasted for 15 s every 45 s at 2
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turns/s, was conducted manually in a horizontal direction in all experiments except the experiment
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studying the effect of package shape on the microbial inactivation, which treated samples with and
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without shaking. To measure the voltage between the two electrodes after the treatment, the probe
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was coupled with a 2000:1 voltage divider, an oscilloscope was used, and information on the current
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was obtained from a capacitor (C0 = 1 nF). The charge of capacitor was plotted versus the applied
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voltage (Lissajous figures) and the areas of the figures were reported as the total power delivered to
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the plasma (Misra et al., 2014a). The CP formation voltage was 28.2 kV and the power sent to the
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two electrodes without the sample was determined to be 17.6 W.
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2.4. Inoculation and analysis of microbial organisms
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Salmonella, indigenous mesophilic aerobic bacteria, and indigenous yeast and molds were
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investigated as the target microorganisms in the experiment studying the effect of the packaging
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material type on the microbial inactivation by ADCPT. Salmonella was chosen as the target
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microorganism in the experiments investigating the effects of the other packaging parameters on the
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microbial inactivation. The selected strains were Salmonella enterica subspecies enterica serovar
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Montevideo (CCARM 8052), S. Enteritidis (CCARM 8040), and S. Typhimurium (DT104)
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purchased from the Culture Collection of Antibiotic-Resistant Microbes (Seoul, Korea). These
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strains were investigated in previous research as the causal agents for cross-contamination on
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tomatoes (Shi et al., 2009) and lettuce (Horby et al., 2003). To form the inoculum, the strains were
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mixed together in the same volume ratio.
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For inoculation, samples were submerged in the inoculum bath (500 mL) of the Salmonella mixed
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strain culture for 5 min. The Salmonella concentrations for the inoculation of grape tomato and the
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other vegetables were ~9 log CFU/mL and ~7 log CFU/mL, respectively. The inoculated samples
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were dried in the hood for approximately 2 h prior to ADCPT. After drying, the concentration of
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Salmonella in the samples of grape tomatoes, romaine lettuce, red cabbage, and carrot slices were all
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~5 log CFU/sample. To determine the microbial concentration from the sample surface before and
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after CP treatment, each grape tomato (~8 g) in the mixed samples was transferred aseptically to a
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sterile stomacher bag (130 mL, Nasco Whirl-PakⓇ, Fort Atkinson, WI, USA) to which 10 mL of
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sterile peptone water (0.1%, w/w) was added, and each mixture of romaine lettuce, red cabbage, and
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carrot slices (~18 g) was put into a sterile bag (310 mL, Nasco Whirl-PakⓇ) with 162 mL of sterile
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peptone water. In each bag, a microbial suspension was made by rubbing the samples for 2 min
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through the surface of the bag. The suspension was diluted and plated on a xylose lysine
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deoxycholate agar, a plate count agar, and a potato dextrose agar, and cultured at 35 °C for 24 h,
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35 °C for 48 h, and 25 °C for 7 days, respectively, for the microbial counting of Salmonella,
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indigenous mesophilic aerobic bacteria, and indigenous yeast and molds of the sample.
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2.5. Water vapor permeability of the package
Water vapor permeability was determined using the Gravimetric Modified Cup method (McHugh,
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1993) based on the American Society of Testing and Materials (ASTM) E96 (ASTM, 2016). A
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cylindrical permeability cup made of polymethylmethacrylate (Plexiglas™) was used, and calcium
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sulfate (Drierite, W.A. Hammond Drierite Co. Ltd., Xenia, OH, USA) was placed inside a humidity
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chamber to maintain the relative humidity (RH) in the range of 3–8%. The temperature of the
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chamber was maintained at 23 ± 2 °C, and the air velocity of the fan installed inside the box was 152
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cm/min. The RH was measured using a hygrometer (Model THDx, Dickson, Addison, IL, USA).
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2.6. Tensile properties of the package
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Tensile properties, including tensile strength, percentage elongation at break, and elastic modulus,
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of the film were determined following the ASTM D882-01 standard method (ASTM, 2002), using a
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tensile property tester (Withlab. Co., Ltd, Anyang, Korea). The values for cross head speed and static
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load cell of the tester were 50 mm/min and 4.9 kN, respectively.
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2.7. Thermodynamic properties of the package
A dynamic mechanical analyzer (DMA-8000, PerkinElmer, Waltham, MA, USA) was used to
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measure the changes in elastic modulus and tan δ of the PP, LDPE, and PET films. The DMA
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measurement conditions for the film samples (25 × 8 mm) were set at 1 Hz frequency, while the
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temperature was raised from –50 °C to 180 °C at a speed of 3 °C/min. The point at which a peak of
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tan δ was detected during the phase where the elastic modulus decreased was defined as the glass
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transition temperature (Tg) (Chiou et al., 2006).
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2.8. Opacity of the package
Opacity was determined as the absorbance in the 400–800 nm range using a spectrophotometer
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(UV-2450, Shimadzu Co., Kyoto, Japan) based on the method developed by Gontard et al (1992).
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The film samples were cut to a size of 2 × 3 cm and the opacity of the film was calculated by
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integrating the area under the absorbance curve.
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2.9. Surface characteristics of the package
Field-emission scanning electron microscopy (FE-SEM, S-4700; Hitachi, Tokyo, Japan) was used
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to observe the film surface. The film samples were cut to a size of 5 × 5 mm and coated with
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platinum under vacuum conditions using a thin film coater (sputter coater; E-1010 Ion Sputter,
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Hitachi, Tokyo, Japan). The surface was observed at 7.0 kV voltage (Chung et al., 2012) under 100 ×
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magnification.
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2.10. Statistical analysis
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The experiments investigating microbial inactivation according to packaging parameters and
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those for the film property determination were each repeated three times. A total of six samples for
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each sample type were prepared for the three repeated experiments (n = 6). Three measurements
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were obtained for each sample for determination of film properties other than tensile properties,
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while five measurements were used for tensile property determination. Analysis of variance
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(ANOVA) was used to evaluate the differences among the means. If significant differences were
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detected, Tukey’s multiple range test was used to evaluate the means to estimate the significance of
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differences ( = 0.05) using PASW Statistics software (version 22.0.0, IBM SPSS Inc.; New York,
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NY, USA).
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3. Results and Discussion
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3.1. Effects of the kind of packaging material on the microbial inactivation
A significantly higher level of Salmonella inactivation was observed from the grape tomatoes in
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the flexible pouch made of the nylon-LDPE composite than those in the LDPE pouch, with the levels
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being 2.3 ± 0.1 and 1.8 ± 0.3 log CFU/tomato, respectively. Reactive species in cold plasma,
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including reactive oxygen species (ROS), reactive nitrogen species (RNS), and other atoms,
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metastables, radicals, and excited molecules, which are diffused through cell membranes, can
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inactivate microorganisms by reacting with membrane lipids, proteins, enzymes, and nucleic acids
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(Misra and Jo, 2017). Microbial inactivation can be also induced by bombardment of electrons, ions,
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and free radicals to the cell membranes, resulting in surface erosion and improper cell replication via
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DNA modifications caused by ultraviolet generated in cold plasma (Kim et al., 2014). The difference
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in the inactivation efficacy might be in part explained by the differences in dielectric permittivity
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between different packaging materials, which can induce different levels of microdischarge (Li et al.,
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2007) and thus different amounts of reactive species in cold plasma (Shuiliang et al., 2016). The
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higher dielectric permittivity of nylon (4.0-6.0) (Lampman, 2003) in the composite than in LDPE
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(2.3) (Basri et al., 2017) might lead to higher microdischage and more reactive species in CP,
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resulting in higher inactivation. However, the rigid container with LDPE material, which has lower
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dielectric permittivity (2.3) (Basri et al., 2017) than PET (3.3) (Pourasl et al., 2014), led to higher
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inactivation of indigenous mesophilic aerobic bacteria on the grape tomato sample, by ~0.4 log
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CFU/tomato, compared with packaging with the PET material (P < 0.05, Table 1). The proximity of
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the package to the electrodes is thought to influence reactive species production, resulting in an
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inactivation difference. In this study, the LDPE package in the LDPE rigid container adhered more
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strongly and evenly to the borosilicate dielectric barrier than the PET, as demonstrated in Fig. 7,
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resulting in the uniform production of microdischarge over a larger area and the consequent
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production of a larger amount of reactive species. This appeared to have enabled effective microbial
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inactivation, despite the relatively low permittivity.
The inactivation of Salmonella and indigenous yeast and molds on the grape tomato sample,
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however, did not differ according to packaging material (P > 0.05; Table 1). This may be because the
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microorganism constituting the indigenous mesophilic aerobic bacteria on the surface of grape
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tomatoes are more sensitive than Salmonella and indigenous yeast and molds to the changes in
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reactive species production caused by differences in the proximity between the packaging and the
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electrodes. The effect of packaging material on the microbial inactivation by ADCPT depended on
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the kind of microorganisms and this needs to be further investigated after identification of the
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indigenous microorganisms of grape tomatoes.
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Furthermore, inactivation rates of the indigenous mesophilic aerobic bacteria on the romaine
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lettuce, red cabbage, and carrot slices were not significantly different (P > 0.05) regardless of
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packaging material. The inactivation of Salmonella and indigenous yeast and molds on these slices
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was maintained at a level of ~1 log CFU/sample with no significant difference according to the kind
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of packaging material (Table 1). For the romaine lettuce, red cabbage, and carrot slices, no
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significant difference in the level of inactivation according to packaging material was observed for
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any of the studied microorganisms (Table 1). This may have been due to the complicated surface
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structure of the samples restricting the contact between the reactive species and the microorganisms
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(Ziuzina et al., 2014), so that the level of microbial inactivation was not substantial enough to
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demonstrate the influence of the packaging material on the efficacy of ADCPT on the microbial
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inactivation. Min et al. (2016) also reported that ADCPT under 34.8 kV for 5 min resulted in
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microbial inactivation on romaine lettuce samples within a level of 1 log CFU/sample, lending
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support to the observation that vegetables with complicated surface structure pose challenges for
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microbial inactivation.
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The LDPE material was chosen for the rigid container with PET frame in all later experiments, as
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it increased the efficacy of microbial inactivation through ADCPT on indigenous mesophilic aerobic
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bacteria.
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3.2. Effects of package shape and shaking on Salmonella inactivation
During the treatment without shaking, the grape tomatoes in the rigid containers (both clamshell
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rigid container and rigid container with the PET frame) exhibited more effective Salmonella
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inactivation by ~0.4 log CFU/tomato than those in the flexible pouches (Fig. 8a). This may have
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been due to the narrower space between the food and the packaging in the pouch packages than in
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the rigid containers (Fig. 3), which prevents uniform distribution of reactive species in the package
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and causes inefficient contact between the reactive species and the food (Min et al., 2016). By
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contrast, when shaking was applied during ADCPT, there was no significant difference in the level
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of Salmonella inactivation according to package shape (P > 0.05). This was presumed to have been
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caused by the increased contact between reactive species and the sample, with the shaking helping
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with the uniform distribution of reactive species in the pouch package during the treatment despite
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the narrower space between the sample and the pouch package. Previous research also found that
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shaking helped uniform ADCPT for packaged romaine lettuce samples when they were stacked in
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clamshell rigid containers (Min et al., 2016). The positive effect of shaking was also demonstrated
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with respect to microbial inactivation for the romaine lettuce, red cabbage, and carrot slices,
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packaged in both the LDPE rigid container with PET frame and the LDPE pouch (Fig. 8b), implying
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that shaking improves the contact between the reactive species and the microorganisms present on
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the complicated surface structure of the samples.
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3.3. Effects of package headspace gas composition and HSR on the Salmonella inactivation
There was no significant difference in Salmonella inactivation when air was used as the gas inside
329
the package during ADCPT and when the oxygen and nitrogen concentrations were varied (P > 0.05;
330
Table 2). ADCPT using oxygen, nitrogen, or air as the primary plasma-forming gas was previously
331
reported as being effective for microbial inactivation because these gases produce ROS, RNS, and
332
various other reactive species whose activities are crucial in microbial inactivation (Laroussi and
333
Leipold, 2004). The results of this study indicated no significant difference in microbial inactivation
334
through ADCPT as applied to MAP-packaged mixed vegetables with variation in oxygen or nitrogen
335
concentrations. This may have been due to the various reactive species produced by oxygen, nitrogen,
336
and air, which are known to be effective for microbial inactivation, all exhibiting a similar ability to
337
inactivate Salmonella on the surface of grape tomatoes. A similar result was presented by Misra et al.
338
(2014b). They reported that the inactivation rates of total aerobic mesophilic microorganisms and
339
yeast and molds on strawberries were not significantly different between those packaged in
340
containers flushed with 65% O2 + 16% N2 + 19% CO2 (high concentration of O2) and those in
341
containers flushed with 90% N2 + 10% O2 (high concentration of N2) gas mixtures, following
342
ADCPT at 60 kV.
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The effects of HSR on Salmonella inactivation are presented in Table 2. The grape tomatoes in
344
the package with 43:1 HSR, i.e., wider headspace, showed significantly higher level of Salmonella
345
inactivation through ADCPT than in the package with 30:1 HSR. This may be explained by the
346
increase in package volume leading to an increase in the total volume of gas inside the package,
347
thereby producing a larger quantity of reactive species (P < 0.05). The results suggest that it is the
348
increase in total gas volume, rather than the change in gas composition, which enhances the efficacy
349
of microbial inactivation through ADCPT on packaged foods.
350
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The romaine lettuce, red cabbage, and carrot slices did not display any influence of the parameters
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351
of gas composition or HSR on microbial inactivation. Again, this was possibly due to the
352
complicated surface structure of the slices restricting the contact between the reactive species and the
353
microorganisms on the surface of the slices.
354
3.4. Effects of distance between the sample and electrode on the inactivation of Salmonella
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In the case of grape tomatoes from mixed-vegetables, more effective Salmonella inactivation was
357
shown by direct treatment, where the food was positioned between two electrodes, than by indirect
358
treatment, where the sample was positioned far away from the electrodes (P < 0.05; Table 2). Even
359
though it was not conducted with a food system, a similar study by Ziuzina et al. (2013), where
360
Escherichia coli ATCC 25922 in a packaged 96 well plate was investigated, demonstrated more
361
effective microbial inactivation by direct treatment than indirect treatment during ADCPT under 40
362
kV. This may be attributed to short-lived reactive species, which would be more available for the
363
sample with direct treatment than with indirect treatment. Short-lived reactive species would be lost
364
or reacted on their way to the food positioned 15 cm away in this experiment.
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In the cases of romaine lettuce, red cabbage, and carrot slices, there were no significant
366
differences in inactivation levels between direct and indirect treatment, which was also attributed to
367
the complicated surface structure of the slices as previously discussed.
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3.5. Effects of the use of secondary packaging on the Salmonella inactivation
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The Salmonella inactivation through ADCPT on grape tomatoes increased from 1.3 ± 0.4 log
371
CFU/tomato to 2.0 ± 0.2 log CFU/tomato (P < 0.05), when secondary packaging was applied. This
372
suggests that the application of secondary packaging can improve the inactivation efficacy. By the
373
use of secondary packaging, a new material is added as a dielectric barrier and the thickness of the
374
whole package is altered. This may have elicited similar effects to changing the packaging material,
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as discussed with dielectric permittivity in section 3.1. In addition, the use of secondary packaging
376
could broaden the contact area between the package and the electrodes, resulting in a broader area
377
where CP-forming energy was transferred and greater production of reactive species. Nonetheless,
378
the material used as secondary packaging was glued onto the primary packaging in this study, which
379
may have led to a different result from that obtained with a sample that had a free space between the
380
primary packaging and secondary packaging. Future research will explore the relevant
381
including the presence of free space and its volume. The use of secondary packaging did not affect
382
the efficacy of microbial inactivation on the romaine lettuce, red cabbage, and carrot slices as the
383
other packaging parameters.
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variables,
3.6. Effects of ADCPT on the package properties
The effects of ADCPT on the tensile properties, transparency, and water vapor permeability of the
387
LDPE, PP, and PET packages are exhibited in Table 3. The water vapor permeability of the packages
388
increased after ADCPT (P < 0.05), while the tensile properties and transparency were not
389
significantly changed (P > 0.05). The increased water vapor permeability was probably due to
390
ADCPT undergoing physical etching and chemical bonding to hydrophilic functional groups, which
391
changed the package surface (Carrino et al., 2002). Nonetheless, the possible differences in the
392
surface morphologies of the three packages with and without ADCPT were not exhibited in the
393
micrographs at 100 × magnification (Fig. A.2). The potential abrasions induced by physical etching
394
might be smaller than those formed during the production and use of the packages prior to ADCPT.
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The tan δ and elastic modulus profiles of LDPE suggest that ADCPT did not alter its thermal
396
properties (Fig. A.3). The Tg of LDPE was not observed in the temperature range between −50 °C
397
and 180 °C used in this study, either before or after ADCPT. The T g of PP material was between
398
−10 °C and 20 °C in a study by Thirtha et al. (2005), in line with the present study reporting the Tg to
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lie between 5 °C and 15 °C. After ADCPT, the Tg was between 9 °C and 15 °C, indicating that the
400
ADCPT employed herein had no influence on the Tg of the PP material. The Tg of the PET material
401
also fell between 108 °C and 116 °C before ADCPT, and between 102 °C and 117 °C after ADCPT,
402
also indicating that the ADCPT had not affected the Tg of the PET material. Pankaj et al. (2014a, b)
403
reported that no significant change in Tg was observed when a Zein film was subjected to ADCPT at
404
80 kV for 4 min or when a polylactic acid film was treated at 80 kV for 3.5 min.
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405
4. Conclusions
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The indigenous mesophilic aerobic bacteria inactivation through ADCPT on grape tomatoes was
409
higher when the tomatoes were packaged in the LDPE rigid container than in the PET container,
410
possibly owing to more even adherence of LDPE than PET to the borosilicate dielectric barrier. For
411
grape tomatoes, more effective Salmonella inactivation through ADCPT was observed when the
412
packaging was a rigid container than when it was a flexible pouch, and the use of shaking during
413
treatment eliminated the difference in Salmonella inactivation according to package shape. There
414
was no difference in Salmonella inactivation on grape tomato surfaces through ADCPT when the
415
package headspace gas nitrogen and oxygen contents were varied. On the other hand, increasing the
416
HSR increased the Salmonella inactivation on grape tomato surfaces through ADCPT, indicating that
417
more effective Salmonella inactivation results, not from changing the headspace gas composition,
418
but from increasing the total gas volume. In addition, the Salmonella inactivation on grape tomato
419
surfaces was more effective when the packaged food was close to the electrodes, hence receiving
420
direct treatment, rather than treatment at a distance. Also, more effective microbial inactivation was
421
observed for the grape tomatoes with secondary packaging than those with primary packaging alone.
422
Regarding the package properties before and after ADCPT, no significant changes were observed
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except in water vapor permeability, suggesting that the ADCPT employed in this study is a
424
technology that can inactivate microorganisms on packaged food products while minimally affecting
425
the package properties for protecting and containing the food. The results of the present study
426
suggest that the optimum package conditions that exhibited the most efficient microbial inactivation
427
include the use of LDPE for packaging material, rigid containers for package shape, a larger HSR, a
428
minimum distance between the sample and electrode, and secondary packaging. In addition, the use
429
of shaking is an effective way of enhancing the microbial inactivation. The packaging parameters
430
identified in this study must be considered when the efficacy of in-package ADCPT in
431
decontaminating mixed vegetables is evaluated.
433
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Acknowledgements
434
This work was supported by the National Research Foundation of Korea (NRF) grant funded by
436
the Korea government (MSIP) (NO. 2016R1A2B4010368) and by Korea Institute of Planning and
437
Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET) through High Value-
438
added Food Technology Development Program, funded by Ministry of Agriculture, Food and Rural
439
Affairs (MAFRA) (318026-03).
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Table 1. Effects of the kind of packaging material for rigid containers on the inactivation of
549
Salmonella, indigenous mesophilic aerobic bacteria, and indigenous yeast and molds on mixed
550
vegetables by dielectric barrier discharge cold plasma treatment at 28.2 kV for 3 min.
Microbial reduction (log CFU/sample)
Microorganisms
Low density
Polyethylene
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Sample
Polypropylene
polyethylene
Indigenous mesophilic
Grape tomato
1.2 ± 0.1 a
0.8 ± 0.2 b
1.4 ± 0.0 a
1.1 ± 0.1 ab
1.5 ± 0.3 a
1.2 ± 0.2 a
1.5 ± 0.3 a
0.5 ± 0.2 a
0.6 ± 0.1 a
0.5 ± 0.1 a
1.0 ± 0.2 a
1.1 ± 0.3 a
1.0 ± 0.3 a
Indigenous yeast
Slices of
Indigenous mesophilic
red cabbage, and
aerobic bacteria
carrot
Indigenous yeast
551
a)
552
b)
Values are meaning mean and standard deviation.
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Values with different letters are meaning significant difference of data in the same row at P < 0.05.
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and molds
D
romaine lettuce,
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1.3 ± 0.4 a
Salmonella
1.5 ± 0.3 ab
0.9 ± 0.2 ab
aerobic bacteria
and molds
1.2 ± 0.2 b
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1.5 ± 0.3a) abb)
Salmonella
terephthalate
25
Table 2. Effects of the gas composition in the headspace of a nylon-low density polyethylene-laminate pouch package containing mixed
555
vegetables, and those of the head space volume to sample volume ratio (HSR), and the distance from electrode to sample in a low density
556
polyethylene rigid container with a PET frame on the inactivation of Salmonella on vegetables by dielectric barrier discharge cold plasma
557
treatment at 28.2 kV for 3 min.
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Microbial reduction (log CFU/sample)
Gas composition
Sample
Oxygen 21%,
Oxygen 5%,
HSR
Sample location in package
Oxygen 90%,
Nitrogen 78%
Nitrogen 85%
Nitrogen 0%
30:1
Carbon dioxide 0%
Carbon dioxide 10%
2.3 ± 0.11 )b2)
1.0 ± 0.3 a
1.1 ± 0.3 a
red cabbage, and carrot
558
a)
559
b)
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2.3 ± 0.1 b
Slices of romaine lettuce,
treatment
treatment
2.3 ± 0.2 b
1.5 ± 0.3 c
2.7 ± 0.2 b
3.8 ± 0.4 a
1.5 ± 0.3 c
1.0 ± 0.2 a
1.1 ± 0.1 a
0.9 ± 0.2 a
0.7 ± 0.1 a
0.7 ± 0.2 a
EP
Values are meaning mean and standard deviation.
Indirect
Carbon dioxide 10%
(Air)
Grape tomato
Direct
43:1
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Values with different letters are meaning significant difference of data in the same raw at P < 0.05.
26
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Table 3. Effects of dielectric barrier discharge cold plasma treatment on the water vapor permeability, tensile strength, elastic modulus, percent elongation
561
at break, and opacity of sample packages of low density polyethylene (LDPE), polypropylene (PP), and polyethylene terephthalate (PET)
Percentage elongation
Water vapor permeability
(g·mm·k-1·Pa-1·h-1·m-2)
Tensile strength (MPa)
0.012 ± 0.001a) bb)
23.77 ± 1.67 a
519.22 ± 22.28 a
106.69 ± 4.87 a
3055.57 ± 87.84 a
Treated
0.017 ± 0.003 a
24.10 ± 1.10 a
513.74 ± 37.99 a
107.40 ± 5.82 a
3146.81 ± 73.35 a
Untreated
0.012 ± 0.001 b
37.07 ± 1.63 a
657.05 ± 44.17 a
401.66 ± 13.66 a
3118.84 ± 186.96 a
Treated
0.014 ± 0.002 a
35.32 ± 4.15 a
656.11 ± 29.55 a
416.94 ± 28.28 a
3131.58 ± 133.91 a
Untreated
0.013 ± 0.001 b
176.04 ± 12.73 a
57.26 ± 10.39 a
2199.06 ± 23.42 a
17051.65 ± 441.47 a
Treated
0.016 ± 0.002 a
177.17 ± 15.48 a
67.19 ± 16.27 a
2202.04 ± 42.35 a
17154.94 ± 519.65 a
PP
b)
Values are meaning mean and standard deviation.
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PET
a)
Opacity
Untreated
LDPE
562
Elastic modulus (MPa)
at break (%)
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Variables
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Values with different letters are meaning significant difference between not treated and treated data of each material P < 0.05.
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Figure Captions
565
Fig. 1. Images of mixed vegetable-containing rigid containers of low density polyethylene
567
(LDPE) (a), polypropylene (PP) (b), and polyethylene terephthalate (PET) (c), structured with
568
the PET frame (d).
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569
Fig. 2. Photographs of the mixed vegetable-containing clamshell package (a), low density
571
polyethylene (LDPE) rigid container with the frame (b), and LDPE pouch package (c).
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Fig. 3. Images of the mixed vegetable-containing low density polyethylene (LDPE) rigid
574
container with frame (left) and the mixed vegetable-containing LDPE pouch (right) placed in
575
the dielectric barrier discharge cold plasma treatment zone. ‘A’ and ‘B’ are the distances
576
from the mixed vegetables to the packaging.
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Fig. 4. Images of the treatment sets for direct (a) and indirect (b) atmospheric dielectric
579
barrier discharge cold plasma treatment.
580
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578
Fig. 5. Configuration of the secondary packaging. Images of the entire mixed vegetable-
582
containing secondary packaging (a) and cross-sectional view of secondary packaging (b).
583
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Fig. 6. Configuration of the atmospheric dielectric barrier discharge cold plasma treatment
585
system used in the study.
586
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Fig. 7. Contact between the borosilicate glass and the package of low density polyethylene
588
(top), polypropylene (middle), or polyethylene terephthalate (bottom).
589
Fig. 8. Effects of shaking of treatment samples during atmospheric dielectric barrier
591
discharge cold plasma treatment, which were packaged in clam shell rigid container, low
592
density polyethylene (LDPE) rigid container with the frame, and LDPE pouch, on the
593
inactivation of Salmonella on grape tomatoes (a) and slices of romaine lettuce, red cabbage,
594
and carrot (b). The applied voltage and treatment time for ADCPT were 28.2 kV and 3 min,
595
respectively. Different letters indicate significant differences in effect within each packaging
596
type at P < 0.05.
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Appendix Figure Captions
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Fig. A.1. Treatment samples packaged in low density polyethylene rigid container with the
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frame, with head space volume to sample volume ratios of 30:1 (left) and 43:1 (right). Upper
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and bottom images are a top view and a side view, respectively.
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Fig. A.2. Micrographs at 100 × magnification of the surfaces of the packages of low density
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polyethylene (a), polypropylene (b), polyethylene terephthalate (c), with (right) and without
606
(left) atmospheric dielectric barrier discharge cold plasma treatment at 28.2 kV for 3 min.
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Fig. A.3. Thermodynamic mechanical behaviors of the packages of low density polyethylene
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(a), polypropylene (b), and polyethylene terephthalate (c) with (right) and without (left)
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atmospheric dielectric barrier discharge cold plasma treatment at 28.2 kV for 3 min.
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