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In-package cold plasma technologies

Article in Journal of Food Engineering · March 2019

DOI: 10.1016/j.jfoodeng.2018.09.019

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 In-package cold plasma technologies
NN Misra1*, Ximena Yepez2, Lei Xu2, Kevin Keener1,3
Center for Crops Utilization Research, Iowa State University, Ames, IA, USA
1

2
Department of Food Science, Purdue University, West Lafayette, IN 47907, USA
3
Department of Food Science and Human Nutrition, Iowa State University, Ames, IA, USA
*Corresponding author: N.N. Misra; Tel: +1-515-294-9461; E-mail: misrann@iastate.edu

Preprint submitted to Journal of Food Engineering

DOI: https://doi.org/10.1016/j.jfoodeng.2018.09.019

Abstract
Cold plasma is an ideal antimicrobial agent with a gamut of reactive chemical species, that could
be obtained from electrical discharges in atmospheric gases. The reactive species are effective
against a range of microorganisms, including bacteria, fungi, spores and viruses, as well as
pesticides and mycotoxins. Generation of cold plasma inside sealed packages allows to localise
and extend the action time of reactive species on microorganisms, while preventing any post-
process contamination. In this review, we present an examination of the design aspects of the
in-package plasma systems, the packaging requirements, and discuss their efficacy with respect
to microbiological and chemical safety of foods.

Keywords: electrical discharge; decontamination; food safety; E. coli; ozone

1
Introduction
Food processing technologies have come a long way with developments evolving from
application/deprivation of heat, utilization of microorganisms, natural and chemical
preservatives, and application of electromagnetic fields for preservation. Of the several food
preservation processes that humankind has developed over the centuries, canning holds a distinct
place. This technology has stood the test of times, supported humanity during times of peace as
well as wars, and remains widely used in the food industry. With the revolution brought by
introduction of polymers in the twentieth century, canning branched into retort pouch
technology and gained even more popularity (Misra, et al., 2017). There are numerous reasons
that were responsible for the success of canning and retort pouch technology. However, the
simplest and quite intuitive design principle turns out to be the processing in a closed
(hermetically sealed) environment that prevented post-processing contamination, thereby
ensuring a long shelf-life.

Despite the popularity of thermal processing, it has its own widely known demerits, mainly the
considerable loss in food quality (Holdsworth & Simpson, 2008). To address this issue,
researchers spent the last four decades in exploring and developing nonthermal technologies.
Among the nonthermal technologies developed, by far, only irradiation and high-pressure
processing (HPP) have gained the most popularity and success in industry and for HPP, also
among consumers (Misra, et al., 2017). It should be noted that HPP, (including high hydrostatic
pressure) also involves (pressure) treatment inside sealed pouches, thus avoiding the likelihood
of post-process contamination.

A notable recent development within the evolution of non-thermal food processing technologies
is the application of cold plasma for agri-food decontamination, and enhancement of food
properties (Misra, Schlüter, & Cullen, 2016). The cold plasma processes are not only limited to
food applications, but are also making an impact in the agriculture (Puač, Gherardi, & Shiratani,
2018), medical (von Woedtke, Reuter, Masur, & Weltmann, 2013), and environmental sectors
(Bobkova & Rybkin, 2015). To introduce the fundamentals of plasma technology to novices to
the field, we will provide a very brief discussion of the physics and chemistry of the technology
in this review. A salient feature of this technology is the ability to establish a plasma inside a
sealed package. This approach is referred to as the “in-package plasma” technology and has a
striking parallelism with that of canning and HPP in that the plasma treatment is carried out
inside a sealed package. However, that does not render it into a sterilization technology for foods,
as it is primarily a surface treatment process. What it does point at is the possibility of raising
the bar for surface decontamination technologies for shelf-life extension of minimally processed,
fresh, and/or raw foods. Of course, this originates from the in-package nature of the technology.

There exist dedicated reviews on the basics of cold plasma (Misra, et al., 2018), its applications
in decontamination of foods (Misra & Jo, 2017; Misra, Tiwari, Raghavarao, & Cullen, 2011;
Surowsky, Schlüter, & Knorr, 2014), enzyme inactivation (Misra, Pankaj, Segat, & Ishikawa,
2016), and agricultural applications (Puač, et al., 2018), and a recent edited book on the topic
(Misra, Schlüter, et al., 2016). However, there has been no dedicated reference on the topic of
in-package cold plasma technologies and their potential applications in the food industry. The
approach towards containment of the plasma inside a sealed package could be different; in fact,
a range of in-package configurations have evolved within the recent years. Therefore, in this

2
review we will provide a detailed account of the philosophy and design of the various in-package
configurations, with a focus on the studies conducted within the past five years. The choice of
applications that we will discuss is motivated by our personal experience and their relevance to
industry, specifically the fresh produce, meat, fish, poultry, and dairy sectors. We will also briefly
discuss the potential applications of in-package plasma technology in ensuring food safety and
the status of the efforts in scaling-up. This article is based on references obtained through a
search strategy built for google scholar (including patents) and web of science databases with
the keywords plasma, electrical discharge, in-package, sealed package, encapsulated plasma, and
food, followed by careful screening to retain the most relevant journal papers. It is expected that
this review will draw the attention of the food engineering research community in exploring new
in-package plasma designs and forwarding the idea of in-package food processing, in general.

Fundamentals of plasma technology

Plasma is an ensemble of several excited atomic, molecular, ionic, and radical species, co-existing
with numerous others, including electrons, positive and negative ions, free radicals, gas atoms,
molecules in the ground or excited state, quanta of electromagnetic radiation (UV photons and
visible light) (Misra, et al., 2018). The ionization of a given gas can be established via application
of thermal energy (heating) or electromagnetic fields (electric field or high energy light). For
technological applications of plasmas at room-temperature and under atmospheric pressure
conditions, application of electric field is the most popular method. We will confine this review
to a discussion of cold plasmas operating at atmospheric pressure. Detailed discussions
introducing the chemistry and physics of plasmas can be found from several recent references
(Lu, et al., 2016; Misra, et al., 2018; Misra, Schlüter, et al., 2016). Therefore, we will provide a
succinct review of the essential concepts of plasma for the sake of facilitating our discussions and
completeness.

In the context of cold plasma technology, the term “cold” is often debatable. Herein, cold does
not refer to sub-zero temperatures; nor is there any convention with regards to the temperature
range. However, it is informally known that plasma sources operating at near ambient to under
60 ˚C can be considered as cold plasmas. From the perspective of physicists, the term cold
implies a lower temperature of the heavy species (ions, radicals, neutrals) as compared to
electrons in the ionized gas. This thermodynamic non-equilibrium between electrons and heavy
species is a direct consequence of the asymmetric momentum transfer during collisions under the
influence of an electrical potential difference (c.f. Misra, et al. (2018) for details). Another
relevant term is “atmospheric pressure”, the origin of which resides in the fact that cold plasmas
were historically produced under low-pressure conditions. At sub-atmospheric pressures, the low
gas density would make the molecules amenable to ionization at low potential differences. With
advances in plasma science and technology, for most practical applications cold plasma can now
be generated at atmospheric pressures. What distinguishes the various plasma sources employed
for biological applications are-

(i) the way the energy is input to the gas, e.g. using a microwave, intense UV light, barrier
discharge, corona, or jet configurations;
(ii) the operating parameters of energy input source (frequency, voltage, power density etc.)

3
For this review, we will only consider the barrier discharge configuration of plasma sources,
which are typically operated using a DC (direct current) or an AC (alternating current) source
from line (50-60 Hz) to radio frequencies. Barrier discharges are comprised of two electrodes at
differential potentials, separated by a dielectric material. The dielectric barrier between the
electrodes limits the current flow, thereby preventing an electric arc (direct gush of electrons)
and facilitating the ionization of the gas within the inter-electrode space. According to the
configurations of the electrodes and barriers, one could make a dielectric barrier discharge (DBD)
or a surface dielectric barrier discharge (SDBD) (see Figure 1 for details). Note that the
geometries inherently render a DBD into a volumetric type of discharge, whereas an SDBD is
confined to a surface. Each of these configurations have their own design and operational merits,
as will become evident from facts presented in the subsequent sections of the review.

Fig. 1. Schematic of a DBD (dielectric barrier discharge) (top), and a surface DBD (bottom).

Having outlined the physical concepts central to cold plasma technology, we will shift our focus
to plasma chemistry. The chemical reactions in any plasma are quite complex, involving a
number of species with life-times ranging from nanosecond to hours (cf. Gaens and Bogaerts
(2013) for a kinetic model with 1880 reactions and 84 species). The complexity arises due to a
mixture of mono- to multi-atomic molecules in the feed gas to plasma. Yet another layer of
complexity is added by water molecules present in the gas or that introduced from food materials
placed in the discharge. Considering these facts, it becomes obvious that humid air plasma is by
far the most complex in terms of the chemistry. The air plasma is a potent source of a myriad
of reactive oxygen species (ROS) and reactive nitrogen species (RNS). ROS in humid air plasma
with antimicrobial activity include hydrogen peroxide (H2O2), ozone (O3), superoxide anion
(O2●−), hydroperoxyl (HO2●), alkoxyl (RO●), peroxyl (ROO●), singlet oxygen (1O2), hydroxyl
radical (●OH), and carbonate anion radical (CO3●−). Common examples of RNS in humid air
plasma include nitric oxide (NO●), nitrogen dioxide radical (●NO2), peroxynitrite (ONOO−),
peroxynitrous acid (OONOH), and alkylperoxynitrite (ROONO) (Arjunan, Sharma, &
Ptasinska, 2015). The reaction mechanisms responsible for the formation of active species in a
cold plasma include, electronic impact processes (vibration, excitation, dissociation, attachment
and ionization), ion-ion neutralization, ion-molecule reactions, Penning ionization, quenching,
three-body neutral recombination, and neutral chemistry, besides photoemission, photo-
absorption and photo-ionization (Misra, Pankaj, et al., 2016). The reactive species and their
concentration in the plasma would vary depending on many factors, including the gas in which

4
plasma is induced, the configuration of the plasma source, power input to the gas, duration of
treatment, and the humidity levels (Misra & Jo, 2017).

The concept and design of in-package plasma systems

The key idea of in-package plasma treatment is the localization of the gaseous disinfectants
inside a package wherein they contact with the food product to be disinfected. For in-package
plasma treatment, the product is first packaged in plastic (or occasionally, glass) packaging and
sealed. The gas inside the package could be ambient air or a modified gas mixture. When this
package or the gas within is exposed to a strong electric field for a short period of time, a
breakdown of the gas occurs. This ionised state of the gas, the plasma, acts as the sterilizing
agent and effects the microbial inactivation without affecting the packaging materials integrity.
Many of the plasma species have long life-time ranging from minutes to hours (Moiseev, et al.,
2014; Park, Choe, & Jo, 2018). Due to their high diffusivity coefficients these species rapidly
diffuse around the pack ensuring a uniformity of treatment. Being reactive, any unreacted plasma
species will spontaneously recombine to result in the original gas after timescales that depend
on the species energy, temperature, pressure, the package type and volume, the presence of food,
the humidity, light, and the initial concentration of each species in the package (which itself
depend on how the plasma was generated) (Attri, et al., 2015; Moiseev, et al., 2014; Park, et al.,
2018). Thus, one starts the process with a known gas mixture (or air) and ends with the same
gas mixture after few hours, while effectively eliminating a significant population of the spoilage
microorganisms.

Fig. 2. Schematic of the processes occurring during in-package cold plasma treatment. (1) The pack with
food products is sealed inside the rigid package with ambient air or a modified gas mixture; (2) The
package is subjected to a high voltage electric field resulting in gas breakdown and plasma generation; (3)
The breakdown products, viz. reactive oxygen species (ROS) and reactive nitrogen species (RNS) diffuse
in the pack and inactivate the spoilage microorganisms over a span of few hours; (4) The ROS and RNS
species recombine and/or extinguish to form the original gas.

A gamut of engineering designs for creating plasma discharges inside sealed packages have
evolved over the last few years. Among these, the three distinguished configurations include, (i)
the volumetric DBD plasma (Keener & Klockow, 2017), (ii) the SDBD plasma inside the package
(Yong, Kim, Park, Alahakoon, et al., 2015; Yong, et al., 2017), and (iii) the on-package SDBD
plasma (Diver & Potts, 2015). Schematics of these configurations are provided in Figures 3(a),
3(b), and 3(c), respectively. Note that the plasma set-up of Jayasena, et al. (2015) differs from
the SDBD plasma inside the package (i.e. (ii)) with respect to the flexible design of the electrodes,
that are integrated with the package.

5
Fig. 3 (a)The volumetric in-package DBD plasma, (b) SDBD plasma inside the package, and (c) SDBD
placed firmly on the package containing the products to be treated.

Essentially, the three configurations vary in terms of the operating voltage, frequency, and the
placement of electrodes. Among them, the volumetric DBD relies on application of very high
voltages (in the order of 101 kV - 102 kV) across the entire package, which allows to ionize the
gas even at line frequencies of 50 Hz to 60 Hz, thus eliminating the need for a frequency
generator; see Figure 3(a). Note however, that the volume DBD for in-pack decontamination
can also be operated at higher frequencies (Min, et al., 2016). The SDBD configurations employ
relatively low voltages (1 kV - 10 kV) and high frequency (in the order of 10 kHz) supplies,
which limits the degree of ionization and thus, the amount of reactive species. When the SDBD
configuration is placed inside the package (Figure 3(b)), the ionization occurs predominantly
at the surfaces available between the two electrodes. This limits the number density of reactive
species that could be produced, and ultimately demands extended treatment times for desired
microbial inactivation. In addition, the chances of corrosion of electrodes and the resulting
contamination could be a concern with such a configuration.

When the SDBD is placed on the package (Figure 3(c)), the narrow penetration depth of the
strong electric field results in ionization of the air in the headspace, resulting in formation of the
reactive species. This system also employs high frequency power supply. It may be noted that
high frequencies could contribute towards gas heating in discharges (Jidenko, Bourgeois, &
Borra, 2010). To maintain the nonthermal conditions, the gas heating phenomenon could
potentially limit the treatment times to below that required for effective log reduction of
pathogenic microbes. The placement of SDBD on or inside the package allows to treat packages
of any size, whereas in a volume DBD the package dimension is limited by the maximum gas
gap allowable for ionization. That said, the volume DBD system is known to work well in air for

6
package heights up to 8 cm -10 cm (Keener & Klockow, 2017). A notable advantage of using the
SDBD inside the package is the likeliness of a milder effect on the packaging material as
compared to the volume DBD or the on-package SDBD. While the operation principles of the
barrier discharges are quite similar, their microbial inactivation efficiencies vary markedly. In
general, the volume DBD appears to result in higher microbial inactivation among the three (cf.
Table 1). Nevertheless, there is no single parameter that could describe their efficacy and the
role of the discharge regimes remain unexplained. For example, it is unclear if the direct exposure
of the produce to strong electric fields in a volume DBD renders any specific advantage for
microbial decontamination.

Irrespective of the configuration employed, the in-package plasma results in formation of

antimicrobial species inside the sealed primary packaging, thereby eliminating the safety
concerns associated with handling difficulties, that would otherwise restrict its use (Diver &
Potts, 2015; Misra, Keener, Bourke, & Cullen, 2015; Yong, Kim, Park, Alahakoon, et al., 2015;
Yong, et al., 2017). Further, the destruction of microorganisms in foods under packaged
conditions could lead to several advantages. Specifically, the in-package plasma treatment
approach allows to: (i) reduce the risk of post-process contamination with external food spoilage
and pathogenic agents (microorganisms, toxins) (Shi, Ileleji, Stroshine, Keener, & Jensen, 2017),
(ii) decrease the microbial load on the packaging material (Pankaj, Bueno-Ferrer, Misra,
Milosavljević, et al., 2014), (iii) directly freeze, refrigerate or store under room temperature
conditions (Misra, Pankaj, Frias, Keener, & Cullen, 2015; Xu, Garner, Tao, & Keener, 2017),
(iv) employ a variety of packaging materials (Pankaj, Bueno-Ferrer, Misra, Bourke, & Cullen,
2014; Pankaj, Bueno-Ferrer, Misra, O'Neill, Tiwari, et al., 2014), and modified gas atmospheres
(Misra, Moiseev, et al., 2014; Shi, Ileleji, et al., 2017), (v) trigger sustainable release of
antimicrobial or freshness enhancing compounds from the packaging material (Pankaj, et al.,
2017; Pankaj, Bueno-Ferrer, Misra, et al., 2014b).

In-package decontamination
Literature reveals that in-package plasma systems have been employed for inactivation of a wide
class of pathogens and spoilage microorganisms in model systems, fruits, vegetables, dairy
products, eggs, and meat or meat products (Misra, Schlüter, et al., 2016). Table 1 provides a
summary of the process parameters employed in these studies along with their salient results,
and forms the basis for our discussions in the following sections. Considering that the major
food-borne outbreaks have been attributed to the contamination with Salmonella,
Campylobacter, Escherichia coli, and Listeria monocytogenes, majority of the studies have
focused on their inactivation. Note that these reports are not directly comparable with each
other considering that the plasma sources and process parameters are different. However, we will
attempt to draw some general conclusions regarding their efficacy as a process intervention for
decontamination in the industry. We wish to point that a discussion of the decontamination
efficacy of the SDBD on-package type of plasma source (Diver & Potts, 2015) was not possible
due to the absence of peer-reviewed studies in literature.

7
Table 1. A summary of the research studies reporting the decontamination of foods and food simulants using different in-package cold plasma configurations.

Plasma Reference
Operating parameters Package description Product characteristics
Source
Frequency Voltag Gas Material Dimension Gap Organism Product Initial Max log Time
e/Powe (mm) (mm) load reduction (min)
r
12 kV/ LDPE Klockow and Keener
60 Hz 40 W Air pouch 3.78 L 3 E. coli Spinach 8.2 4.6 5 (2009)
12 kV/ LDPE
60 Hz 40 W O2 pouch 3.78 L 4 E. coli Spinach 8.4 6.4 5

50 Hz 15 kV He/Air PE pouch 4.8 L 30 E. coli Media 7 2 5 Connolly, et al. (2013)

Rigid PP/
cryovac Misra, Ziuzina, Cullen,
50 Hz 40 kV Air pouch 230x310 22 E. coli Media 7 ND* 5 and Keener (2013)
Rigid PP/ Ziuzina, Patil, Cullen,
cryovac Keener, and Bourke
50 Hz 40 kV Air pouch 22 E. coli Media 7 ND* 0.3 (2013)
Rigid PP/
cryovac Misra, Patil, et al.
50 Hz 60 kV Air pouch 230x310 40 Total mesophiles Strawberry 4.99 2.4 5 (2014)
DBD Yeast/mould Strawberry 4.96 3.4 5
Rigid PP/ Ziuzina, Patil, Cullen,
cryovac Keener, and Bourke
50 Hz 70 kV Air pouch 230x310 40 E. coli Tomato 3.1 ND* 1 (2014)

S. Typhimurium Tomato 6.3 ND* 10 s

L. monocytogenes Tomato 6.7 ND* 2

E. coli Strawberry 4.4 3.5 5

S. Typhimurium Strawberry 6.6 3.8 5

L. monocytogenes Strawberry 7.3 4.2 2

Rigid PP/
cryovac Misra, Moiseev, et al.
50 Hz 60 kV N2/O2 pouch 230x310 40 Total mesophiles Strawberry 4.99 3.7 5 (2014)

Yeast/mould Strawberry 4.96 3.3 5

8
 Rigid PP/
cryovac
50 Hz 80 kV Air pouch 230x310 30 L. monocytogenes Media-biofilms 4.5 ND* 1 Han, Patil, et al. (2016)
Rigid PP/
cryovac
pouch 230x310 30 S. aureus Media-biofilms 6 2.96 1
Rigid PP/
cryovac
pouch 230x310 30 E. coli Media-biofilms 5 ND* 1

50 Hz 100 kV Air PET 250x250 E. coli Cherry tomato 5 ND* 2.5 Ziuzina, et al. (2016)

L. innocua Cherry tomato 6 3.5 2.5

Mesophiles Cherry tomato 5.7 3.5 2.5

Yeast/mould Cherry tomato 5.7 3.5 2.5

Albertos, Martín-Diana,
50 Hz 80 kV Air PET/film 150x70 35 Total psychrotrophs Mackerel 5.9** 1.3 5 et al. (2017)

Lactic acid bacteria Mackerel 4.2** 1 5

Pseudomonas sp. Mackerel 4.6** 0.8 5

Albertos, Martin-Diana,
50 Hz 80 kV Air PET/film 150x70 35 Enterobacteria sp. Herring 3.2 ND* 5 et al. (2017)
Rigid PP/
O2/CO cryovac
60 Hz 90 kV 2/N2 pouch 44 Salmonella enterica Orange juice 5 ND* 2 Xu, et al. (2017)
Rigid PP/ McClurkin-Moore,
O2/CO cryovac Ileleji, and Keener
60 Hz 70 kV 2/N2 pouch 305x280 46 Total mesophilic Grains 2.23 6 (2017)
Rigid PP/ Los, Ziuzina, Boehm,
cryovac Cullen, and Bourke
50 Hz 80 kV Air pouch E. coli Wheat, flour 4.1** 3.67 5 (2017)

E. coli Barley, flour 4.1** 4.01 5

Rigid PP/
cryovac
50 Hz 80 kV Air pouch 310x230 22 Yeast/mould Wheat, grain 3.8 2.5 20 Los, et al. (2018)

Total mesophiles Barley, grain 4.6 2.4 20

9
 27 kV/ PET/PEP/ Rød, Hansen, Leipold,
2.78 kHz 31 W Ar/O2 LLDPE 175x275 10 Listeria innocua Beef, dry cured 6.2 1.6 0.3 and Knøchel (2012)
Romaine
0-2.4 kHz 34.8 kV Air Nylon/PE 152x203 30 E. coli O157:H7 Lettuce 6 0.9 5 Min, et al. (2016)
Romaine
Salmonella sp. Lettuce 6 0.3 5
Romaine
L. monocytogenes Lettuce 6 0.9 5
Romaine
Tulane virus Lettuce 6 1.3 5
Romaine
N2/O2 E. coli O157:H7 Lettuce 6 0.4 5
Romaine
Salmonella sp. Lettuce 6 0.3 5
Romaine
L. monocytogenes Lettuce 6 0.8 5
Romaine
TV-virus Lettuce 6 0.2 5
Hertrich, Boyd, Sites,
0-2.4 kHz 35 kV Air PET 30 Salmonella sp. Cherry Tomato 3.88 0.75 3 and Niemira (2017)
Romaine
Lettuce 6.14 0.34 3

Mixed salad 5.23 0.29 3

Romaine Min, Roh, Boyd, et al.
0-2.4 kHz 42.6 kV Air PET 148x128 30 E. coli O157:H7 Lettuce 5.4 1.1 10 (2017)

1.4 kHz 35 kV Air PET 140x124 51 Salmonella sp. Grape Tomato 3.3 3 Min, et al. (2018)
Rigid PP/
O2/CO cryovac Wan, Chen, Pankaj,
60 Hz 85 kV 2/N2 pouch 370x355 52 Salmonella sp. Egg shell 7 6.37 15 and Keener (2017)
Chiper, Chen,
Ar/ PA/EV/PA Mejlholm, Dalgaard,
16 kHz 11 kV CO2 /PE 75x75 5 P. phosphoreum Salmon 5.4 3 1 and Stamate (2011)

SDBD
13.56 MHz 150 W He Pouch/PE 110x15 0.6 L. monocytogenes Ham 8.85 1.73 2 Song, et al. (2009)
inside 50 kHz 2 kV N2/O2 L. monocytogenes Agar 7.59 ND* 2 Lee, et al. (2011)
package
L. monocytogenes Chicken breast 3.17 ND*

10
 Plastic
1.5 kHz 250 W Air container 137x104 53 E. coli Milk, whole 6.28 2.43 10 Kim, et al. (2015)

S. Typhimurium Milk, whole 6.43 2.40 10

L. monocytogenes Milk, whole 6.21 2.46 10

Plastic Yong, Kim, Park,
1.5 kHz 250 W Air container 137x130 53 E. coli Cheese 5.8 2.88 15 Alahakoon, et al. (2015)

S. Typhimurium Cheese 5.8 3.11 15

L. monocytogenes Cheese 5.8 2.26 15

15 kHz 100 W N2/O2 Zipper bag 129x199 E. coli Beef loin 5.91 1.90 10 Jayasena, et al. (2015)

S. Typhimurium Beef loin 5.87 2.57 10

L. monocytogenes Beef loin 5.51 2.58 10

10-50 kHz 8 kV Air PE Campylobacter Media 7 4.4 0.5 Diver and Potts (2015)
CO2/O 8200
2 PE Enterobacteriaceae Chicken cfu/g 0.0

E. coli Chicken 930 cfu/g 0

Campylobacter Chicken 310 cfu/g 0.0

Total aerobic Chicken 6 4.3

*ND=not detectable; **Bacterial counts are approximate from figure

11
Model studies
Numerous model studies have been carried out to decontaminate bacteria, yeast, spores, and
toxins grown on model microbiological media using in-package cold plasma sources. In many
cases, the in-package systems allow to reduce E. coli, L. monocytogenes, and Staphylococcus
aureus to non-detectable counts on growth support media, starting from a 6-8 log 10 of initial
bacterial load (Connolly, et al., 2013; Han, Boehm, et al., 2016; Han, Patil, et al., 2016; Lee, et
al., 2011; Ziuzina, et al., 2013). Plasma treatments have been found to reduce the concentration
of L. monocytogenes by >6 log10 CFU in agar media after 1 min of treatment using a volume
DBD system (Han, Boehm, et al., 2016; Han, Ziuzina, et al., 2016), and after 2 min of treatment
using an SDBD inside the package (Lee, et al., 2011). In these studies, apart from the discharge
configurations, the gas, voltage, and frequency were also different, with the former operating at
70 kVRMS (50 Hz), while the latter operating at 800 V, (50 kHz). However, both the configurations
resulted in a remarkable bacterial reduction within a short treatment time. In a recent study,
the inactivation of Brochothrix thermosphacta biofilms using a volumetric in-package DBD
plasma at 80 kV has been reported (Patange, Boehm, Bueno-Ferrer, Cullen, & Bourke, 2017).
The results revealed that achieving inactivation in buffer media was much easier (>6 log10 in 30
s) as compared to that in complex simulated meat-like growth media (only 2 log 10 in 300 s). The
successful inactivation of bacteria associated with poultry, viz. Pseudomonas fluorescens,
Salmonella enterica Typhimurium, and Campylobacter jejuni in liquid cultures using a volume
DBD in-package plasma at 80 kV has also been reported (Rothrock, et al., 2017). Apart from
bacteria, the reduction in Bacillus atrophaeus spores arrested on paper strips have been found
to be rapidly inactivated (> 6 log10 in 60 s at 70 kVRMS) by volumetric in-package DBD plasma
treatment (Patil, et al., 2014). In conclusion, the successful inactivation of bacteria, bacterial
spores, and biofilms using in-package volumetric and surface DBD plasma has been demonstrated
in literature. However, these results do not appear to translate easily when applying the same
process conditions in real food matrices, as will be further evidenced in the following sections. In
one of the studies, it was found that the treatment time dictated the extent of post-treatment
storage required for maximum microbial inactivation (Leipold, Schultz-Jensen, Kusano,
Bindslev, & Jacobsen, 2011). Therefore, it is suggested that the treatment time should be
optimized based on the time to maximum production of the desired reactive species, beyond
which they could decompose through interaction with the package or other species.

Fruits and vegetables

Fresh produce remains the leading cause of foodborne illness outbreaks implicating pathogens
such as Shiga Toxin producing Escherichia coli, Salmonella, L. monocytogenes, among others.
An effective means of controlling contamination in fresh produce is to apply post-harvest
decontamination interventions that can replace or supplement the washing operation (Murray,
Wu, Shi, Jun Xue, & Warriner, 2017). The in-package decontamination process is particularly
important for fruits, vegetables, and ready-to-eat foods (Misra, Pankaj, et al., 2015; Xu, et al.,
2017) ; these food categories demand use of ambient temperature processes for ensuring safety,
with minimal impact on product quality. The earliest study of volume DBD based in-package
plasma treatment involved the treatment of spinach inoculated with E. coli O157:H7 inside a
flexible package (Klockow & Keener, 2009). The results were quite promising with 1.5 log10 -2
log10 reduction after 0.5 hour of treatment and up to 3-5 log10 reduction within 24 h of treatment

12
at 12 kV for 5 min. Later, cold plasma treatment of fresh produce was shown to reduce the total
aerobic microbes by up to 5 log10 in products such as tomatoes and strawberries, when using a
volumetric DBD powered at 60 kV and 50 Hz frequency (Misra, Keener, Bourke, Mosnier, &
Cullen, 2014; Misra, Patil, et al., 2014). The studies also confirmed insignificant changes in the
respiration rate and absence of detectable physiological stresses. The possibility of in-package
plasma treatment of strawberries in modified atmospheres with better retention of quality and
higher inactivation rates was also reported (Misra, Moiseev, et al., 2014). Recently, Hertrich, et
al. (2017) employed a volumetric DBD at 35 kV to treat tomato-and-lettuce mixed salads with
plasma sealed inside commercial polyethylene terephthalate plastic packages. The microbial load
of inoculated Salmonella, and that native to cherry tomatoes or lettuce reduced by 0.75 log10 and
0.34 log10 CFU/g, respectively, indicating the poor effects of this set-up in Salmonella
decontamination in mixed salads. In another study by Min et al., treating romaine lettuce by a
volumetric DBD system at 42.6 kV for 10 min resulted in 1.1 log10 CFU/g reduction of
E. coli O157:H7 (Min, Roh, Niemira, et al., 2017).

Overall, increasing treatment time (plasma generation time) and voltage has been reported to
have a positive impact on reducing the bacterial population. Physical properties such as color or
texture of products treated using high voltage volume DBD plasma have also been investigated.
In cherry tomatoes, no significant loss in firmness were found when treated for 2.5 min at 100
kV, and stored for 10 days (Ziuzina, et al., 2016). Thus, it can be concluded that the microbial
decontamination efficiency is highly affected by the configuration of the plasma discharge, nature
of the contamination, plasma transfer direction, as well as by the sample characters, such as the
topography and composition.

While most published studies have focused on treating unit samples with interesting results, it
is unclear if these effects of cold plasma can be translated on an industrial scale. Explorations
with plasma treatment of cherry tomatoes in a bag (80-100 g), with a pilot scale continuous
plasma system, at 100 kV for 150 s have been reported (Ziuzina, et al., 2016). This continuous
set-up reported a reduction of E. coli and L. innocua by 5 log10 and 3.5 log10, respectively. The
production of ozone was 900 ppm in 150 s. In contrast, previous works by the same group
reported similar ozone production within 10 s-30 s of treatment, and reaching 5500 ppm within
5 min at 70 kV (Ziuzina, et al., 2014). The microbial inactivation in cherry tomatoes were under
detected limits for E. coli and L. monocytogenes, within 1 and 2 min treatment time,
respectively. In conclusion, the laboratory results do not appear to scale linearly with the
industrial scale prototype. Therefore, further work in this direction, including computer
simulations of the field conditions and plasma chemistry is desirable to deduce recommendations
for scale-up (Misra, et al., 2018).

Meat and meat products

Pathogens such as L. monocytogenes, E. coli O157:H7, Campylobacter jejuni and Salmonella sp.
can easily thrive on meat causing severe foodborne illness in consumers. To meet the growing
demands for high quality and safe meat products, it is necessary to develop and implement
advanced technologies in the meat industry. In one of well-known studies, Jayasena, et al. (2015)
reported the inactivation of L. monocytogenes, E. coli O157:H7 and S. Typhimurium inoculated
on pork-butt by 2.04 log10, 2.54 log10, and 2.68 log10 CFU/g, respectively using the SDBD inside-
package plasma configuration in air. In beef loin the counts of L. monocytogenes, E. coli and S.

13
Typhimurium were observed to decrease by 1.90 log10, 2.57 log10, and 2.58 log10 CFU/g,
respectively. Jayasena, et al. (2015) found minimal changes in the colour, and texture. However,
they observed the malonaldehyde levels to rise for treatment times exceeding 10 min. It may be
recalled that the malonaldehyde concentration is an indicator of the lipid oxidation. Lee, et al.
(2016) also observed significant reductions in total aerobic bacteria, L. monocytogenes, E. coli,
and S. Typhimurium by 3.36 log10, 2.14 log10, 2.73 log10, and 2.71 log10 CFU/g on chicken breast,
respectively after 10 min of in-pack plasma treatment using the flexible SDBD type
configuration. They also reported a decrease in a* value and increase in L* (lightness) value of
the plasma treated chicken breast. Using the same flexible plasma source, Yong, et al. (2017)
have observed the L. monocytogenes, E. coli O157:H7, S. Typhimurium and A. flavus
populations to decrease by 2.4 log10, 2.7 log10, 3.0 log10 and 3.2 log10, respectively in beef jerky
after 10 min of air plasma exposure. Interestingly, insignificant changes in metmyoglobin content,
shear force, and myofibrillar fragmentation index were recorded in SDBD in-pack plasma-treated
beef jerky. Unlike Lee, et al. (2016), here the L⁎ value was found to decrease, and the a⁎ and
total colour difference to increase after plasma exposure. In another study, Wang, Zhuang,
Hinton, and Zhang (2016) reported that the shelf-life of chicken can be extended by up to 14
days using a modified atmosphere for plasma generation in volumetric DBD system. Cold plasma
in produced in modified gas compositions (65% O2 + 30% CO2 + 5% N2) results in limiting the
microbiological proliferation (> 4 log10) than in air. Furthermore, the changes in colour of the
plasma treated chicken were found to have changed insignificantly. Thus, the studies so far have
revealed no consensus with regards to the suitability of decontamination of chicken without
affecting the quality parameters. This is undeniably due to the different nature of the plasma
sources, and the process conditions employed for these studies. Nevertheless, it is clearly evident
that modified gas atmospheres combined with plasma treatment results in better retention of
quality without compromising on acceptable levels of decontamination.

Fish and fish products

In one of the earliest studies evaluating decontamination of fish, Chiper, et al. (2011) employed
a volumetric DBD operating at atmospheric pressure in Ar and 93% Ar+ 7% CO2 gas mixture
at 13 kV applied voltage (16 kHz frequency) to decontaminate cold smoked salmon. They
observed ~3 log10 reduction in Photobacterium phosphoreum population following 60 s -120 s
treatment without any post-treatment storage. On contrary, the authors reported negligible
impact on the population of L. monocytogenes or Lactobacillus sakei. The in-package volume
DBD plasma has been shown to reduce the population of the spoilage bacteria (total aerobic
psychrotrophs, Pseudomonas sp. and lactic acid bacteria) by ca. 1 log10 at 80 kV in fresh mackerel
(Scomber scombrus) fillets (Albertos, Martín-Diana, et al., 2017). However, no effect on aerobic
mesophilic counts, and an increased oxidation of the lipids poses question over the suitability of
cold plasma treatments under these conditions.

In another study, the recovery of spoilage microorganisms in volumetric DBD plasma treated
Herring (Clupea harengus) has been studied over a period of 11 days storage at 4 ˚C (Albertos,
Martin-Diana, et al., 2017). It was observed that in-package plasma has limited role in controlling
the total aerobic mesophilic, total aerobic psychrotrophics, Pseudomonas, lactic acid bacteria
and Enterobacteriaceae, with the added problem of erratic pH dynamics. Unlike many of the
previous reports (Gavahian, Chu, Mousavi Khaneghah, Barba, & Misra, 2018), the lipid

14
oxidation was found to be at par with the control throughout the storage period. In a recent
study, moderate effect of in-package volume DBD plasma at 70 kV and 80 kV for 5 min on
aerobic bacteria reduction in Sushi (salmon and cooked rice product) was reported (Kulawik, et
al., 2018). Unfortunately, an increase in lipid oxidation in sushi was inevitable for all treatment
conditions. In conclusion, the trade-off between microbial decontamination versus the oxidation
induction does not favor the treatment of fish and fish products using air plasma. However, such
issues could potentially be addressed using modified gas mixtures to maximize the microbial
inactivation and minimize the quality deterioration (Gavahian, et al., 2018).

Dairy products
Milk is rich in nutrients and therefore particularly susceptible to microbial spoilage. Raw milk
is conventionally treated with thermal processes to control pathogenic microorganisms. Thermal
processing to reduce the microbial load, though effective, changes the organoleptic and
nutritional properties in dairy foods (Myer, et al., 2016). With the hope that a non-thermal
approach to reduce the microbial load, may allow to protect the distinctive nutrients and flavor
of milk, in-package cold plasma has been explored as a decontamination intervention. Whole
milk inoculated with E. coli, L. monocytogenes, and S. Typhimurium, have been treated with
the in-package SDBD cold plasma at 15 kHz for 10 min (Kim, et al., 2015). The process was
shown to achieve a 2 log10 -3 log10 CFU/g reduction without any significant changes in the color
and lipid oxidation. A specific challenge of treating milk with cold plasma is the resulting pH
fluctuations; a 10 min treatment was found to reduce the pH from 6.9 to 6.6 (Kim, et al., 2015).
It is known that reactive plasma species from air can reduce the pH drastically in liquids, as
recently demonstrated in water using a volumetric DBD (Suwal, et al., 2018). In-package
treatment has also been explored for sliced cheese, wherein the counts of E. coli, S.
Typhimurium, and L. monocytogenes were found to reduce by 2.88 log10, 3.11 log10, and 2.26
log10 CFU/ml, respectively after 15 min of treatment (Yong, Kim, Park, Alahakoon, et al., 2015).
In another study investigating the decontamination of sliced cheddar cheese using in-package
SDBD plasma, it was observed that the decontamination efficacy against E. coli O157:H7, L.
monocytogenes, and S. Typhimurium was lower for cheese samples as compared to agar plates
(Yong, Kim, Park, Kim, et al., 2015). Earlier to this, Song, et al. (2009) reported that L.
monocytogenes inactivation levels were different for pathogen inoculated on ham versus cheese.
Such differences have been attributed to the surface characteristics of the samples, particularly
the roughness, which could serve as internalization sites for the organisms. In toto, studies
exploring the decontamination of dairy products have received less attention compared to other
products, most likely to avoid the challenge of potential lipid oxidation.

Chemical safety of foods

The use of pesticides in crops is subject to environmental, health, and safety laws and regulations.
A high demand of food may lead farmers to increase the use of pesticides, especially in some
products that are highly susceptible to plant diseases. Reactive plasma species from cold plasma
can degrade pesticide residues (herbicides, insecticides, fungicides) into less toxic compounds
(Misra, 2015). In the past, strawberries immersed in a cocktail of azoxystrobin, cyprodinil,
fludioxonil and pyriproxyfen, were treated with a volumetric in-package DBD plasma at 80 kV
for 5 min (Misra, Pankaj, et al., 2014). A considerable degradation of the pesticide residues by
69%, 45%, 71%, and 65% for azoxystrobin, cyprodinil, fludioxonil and, and pyriproxyfen,

15
respectively was reported for the first time. Subsequently, in another study, blueberries were
immersed in a solution of boscalid and imidacloprid, packaged, and treated with the same
volumetric DBD plasma (Sarangapani, O'Toole, Cullen, & Bourke, 2017). The degradation
efficacy of the treatment was found to vary between 75-80%, while retaining key quality
attributes (polyphenols, flavonoids, ascorbic acid, anthocyanin content), and physical parameters
such as color and texture.

Besides, pesticides, mycotoxins are another class of chemical safety hazards which have their
origin from fungal growth in grains. Recently, Shi, Ileleji, et al. (2017) demonstrated that the
aflatoxin content in corn is reduced by 82%, after a 10 min treatment with a high voltage volume
DBD cold plasma. In a follow-up work, the authors proved that a degradation pathway that
involved the disappearance of a double bond in the furofuran ring, thereby reducing the
bioactivity of aflatoxin B1 (Shi, Cooper, Stroshine, Ileleji, & Keener, 2017). Based on these
studies, it can be concluded that cold plasma could not only serve as a microbial inactivation
intervention in the food industry, but also ensure chemical safety of grains and horticultural
products.

Packaging aspects
The in-package plasma technology for foods relies on the use of polymeric package itself as a
dielectric layer and has been studied using several packaging materials such as LDPE (low
density polyethylene), HDPE (high density polyethylene), polystyrene (PS), Tygon etc. (Keener,
et al., 2012). Herein, the packaging material is an integral part of the treatment step, being
exposed to the plasma discharge. The exposure of the surface of packaging material to the
reactive plasma species ensures that the internal package surface is decontaminated. In fact, cold
plasma has been used as a tool to reduce the microbial load of package material, such as PET
foils, polystyrene, LDPE, and other polymeric materials (Mastanaiah, Banerjee, Johnson, & Roy,
2013). On the flip side, for safety and quality reasons it becomes important to assess all possible
changes induced by the cold plasma in the packaging material, including, migration limits of
additives, monomers, oligomers and low molecular weight substances into the food, as well as
water vapor and oxygen permeability (Pankaj, Bueno-Ferrer, Misra, Milosavljević, et al., 2014).
Chemical migrations in excess of permitted levels has not been observed when using biopolymer
based food packaging, such as polylactic acid (PLA) films (Pankaj, Bueno-Ferrer, Misra, et al.,
2014a). In some of the recent studies, natural antimicrobial additives such as bacteriocins and
essential oils have been incorporated into biopolymer based packaging to leverage the etching
and release of the active ingredient resulting from plasma treatment; c.f. Pankaj, Bueno-Ferrer,
Misra, et al. (2014b) and Pankaj, et al. (2017). To conclude, if processors employ in-package
plasma, they do not need to separately decontaminate the food and package. Thus, in-package
plasma system can efficiently simplify the food process.

Scale-up of the technology

The promising reports of microbiological inactivation with quality retention in foods using in-
package cold plasma technology clearly points at the commercialization potential of the
technology. The volumetric in-package plasma processes can easily be scaled-up for continuous
large-scale treatment of food materials inside closed containers placed between the electrodes
DBD, on a moving conveyer belt. In fact, industrial or pilot scale prototypes have also been

16
designed and built for industries to evaluate (Anacail, 2018; Ziuzina, et al., 2016). Currently,
the industrial adoption of in-package plasma technologies is greatly limited by the lack of suitable
equipment that could match the rate of industrial production lines. This in turn arises from the
extended treatment times, generally running into order of minutes. This challenge could be
overcome through a detailed study of the plasma chemistry as a function of various
environmental, product and package conditions. Research in this direction has already been
initiated (Brayfield, et al., 2018). Upon identifying the most potent antimicrobial species, the
process conditions can be tuned to maximize their production. Several other issues pertinent to
research needs and design aspects for scale-up and commercialization of the in-package plasma
technology were recently reviewed (Cullen, et al., 2018; Keener & Misra, 2016; Misra & Jo,
2017).

Conclusions
Microbial cross-contamination of foods can occur in the processes of harvesting, handling,
transportation and processing. In-package treatment with cold plasma is a novel alternative for
decontamination of foods and preventing against cross-contamination. The most distinctive
designs for in-package plasma systems include the use of a volumetric DBD, placement of a
SDBD inside the package, and the less reported, SDBD placed on the package. The in-package
cold plasma systems have been widely reported to inactivate microorganisms in foods and model
systems, including bacteria, spores, biofilms, fungi, yeast, mold and viruses. To this end, much
success has been achieved for decontamination of fruits and vegetables, as compared to fat rich
dairy and meat products. The limiting factor with application of cold plasma to meat products
has been the oxidation of lipids due to the ROS, and therefore, extensive studies using low
oxygen, modified atmospheres is encouraged. For in-package plasma processes, it is essential to
ensure that besides general food grade requirements for packaging materials, the ability to
withstand the plasma discharges without causing chemical migration or pinholes are met. We
envisage several far-reaching impacts of in-package plasma technologies in the food and bio-
processing sectors in future.

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