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Plasma activated water (PAW): Chemistry, physico-chemical properties,

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DOI: 10.1016/j.tifs.2018.05.007

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 Trends in Food Science & Technology 77 (2018) 21–31

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Trends in Food Science & Technology

journal homepage: www.elsevier.com/locate/tifs

Review

Plasma activated water (PAW): Chemistry, physico-chemical properties, T

applications in food and agriculture
Rohit Thirumdasa, Anjinelyulu Kothakotab, Uday Annapurec,∗, Kaliramesh Siliverud,
Renald Blundelle,f, Ruben Gattf, Vasilis P. Valdramidisg,h
a
Department of Food Process Technology, College of Food Science & Technology, PJTSAU, Telangana, India
b
Department of Food and Agricultural Process Engineering, Kelappaji College of Agricultural Engineering and Technology, Thavanur 679573, India
c
Department of Food Engineering & Technology, Institute of Chemical Technology, Mumbai 400019, India
d
Department of Grain Science & Industry, Kansas State University, Manhattan, KS, USA
e
Department of Physiology and Biochemistry, Faculty of Medicine and Surgery, University of Malta, Msida MSD 2080, Malta
f
Metamaterails Unit, Faculty of Sciences, University of Malta, Msida MSD 2080, Malta
g
Department of Food Studies and Environmental Health, Faculty of Health Sciences, University of Malta, Msida MSD 2080, Malta
h
Centre of Molecular Medicine and Biobanking, University of Malta, Msida MSD 2080, Malta

A R T I C LE I N FO A B S T R A C T

Keywords: Background: Cold plasma is an emerging non-thermal disinfection and surface modification technology which is
Plasma activated water chemical free, and eco-friendly. Plasma treatment of water, termed as plasma activated water (PAW), creates an
Reactive oxygen species acidic environment which results in changes of the redox potential, conductivity and in the formation of reactive
Reactive nitrogen species oxygen (ROS) and nitrogen species (RNS). As a result, PAW has different chemical composition than water and
Microbial disinfection
can serve as an alternative method for microbial disinfection.
Seed germination
Scope and approach: This paper reviews the different plasma sources employed for PAW generation, its physico-
Novel technologies
chemical properties and potential areas of PAW applications. More specifically, the physical and chemical
properties of PAW are outlined in relation to the acidity, conductivity, redox potential, and concentration of
ROS, RNS in the treated water. All these effects are in microbial nature, so the applications of PAW for microbial
disinfection are also summarized in this review. Finally, the role of PAW in improving the agricultural practices,
for example, promoting seed germination and plant growth, is also presented.
Key findings and conclusions: PAW appears to have a synergistic effect on the disinfection of food while it can also
promote seedling growth of seeds. The increase in the nitrate and nitrite ions in the PAW could be the main
reason for the increase in plant growth. Soaking seeds in PAW not only serves as an anti-bacterial but also
enhances the seed germination and plant growth. PAW could potentially be used to increase crop yield and to
fight against the drought stress environmental conditions.

1. Introduction
By 2050, the population on earth is estimated to reach 10 billion,
which points to the need for innovative approaches for food production
and processing to meet the global demand for nutritional intake. The
greatest challenge is to produce safe food with high quality considering
the new risks encountered during the food production because of
emerging pathogens. The outbreaks of Shiga-toxin producing
Escherichia coli bacteria (STEC) serotype O104:H4 is an example which
resulted in 782 Haemolytic Uremic Syndrome (HUS) STEC cases and
3128 non-HUS STEC cases with diarrhea of which 46 were fatal (ECDC,
Rasko et al., 2011). There is an increase in demand from the consumers
for the minimally processed foods with low preservatives and improved
food quality. Non-thermal food processing technologies could be the
alternative methods for food preservation, minimizing the negative
effect on the nutritional profile. Some of the non-thermal processing
technologies which are already employed in the food processing in-
dustries to extend the shelf-life are irradiation, high pressure proces-
sing, UV light processing and ozonation (Koutchma, 2008). The authors
have applied UV treatment for the juices and apple cider. Other non-
thermal processing technologies like, pulsed electric fields and ultra-
sounds are mainly used for the enhancement of extraction of bioactive
compounds from fruits and vegetables. Recently, cold atmospheric
plasma technology has received more attention in food applications.

∗
Corresponding author.
E-mail addresses: us.annapure@ictmumbai.edu.in, udayannapure@gmail.com (U. Annapure).

https://doi.org/10.1016/j.tifs.2018.05.007
Received 5 September 2017; Received in revised form 12 March 2018; Accepted 2 May 2018
Available online 04 May 2018
0924-2244/ © 2018 Elsevier Ltd. All rights reserved.
R. Thirumdas et al.
Plasma is referred as the fourth state of matter comprised of positive
and negative ions, electrons, excited and neutral atoms, free radicals,
molecules in the ground and excited states and the UV photons
(Fridman, 2008). Plasma is subdivided into thermal (hot) plasma and
non-thermal (cold) plasma based on thermodynamic temperature
equilibrium of the constituents (Bogaerts, Neyts, Gijbels, & Van der
Mullen, 2002). The temperature of cold plasma never exceeds a tem-
perature of 60 °C except for few plasma jets. Some of the widely used
plasma sources for food applications are dielectric barrier discharges
(DBD), plasma jets and corona discharges. In recent years, many sci-
entists and researchers have employed cold plasma in several food
applications: microbial disinfection, enzymatic inactivation, improving
the cooking quality of rice varieties, starch modification, and for en-
hancing the seed germination (Thirumdas, Sarangapani, & Annapure,
2015).
Most of the studies on the antimicrobial activity of plasma have
been conducted; on applying the gas plasma directly over the food
stuffs to get the maximum microbial inactivation efficiency. But few
researchers have reported that there are some negative effects like loss
of colour, change in surface topography due to etching and degradation
of bioactive compounds after the surface treatment (Misra et al., 2014).
To overcome these problems, plasma activated water (PAW) also called
plasma acid, plasma activated liquids, nutrients broths (Adamovich
et al., 2017; Puač, Gherardi, & Shiratani, 2017; Schnabel et al., 2016;
Scholtz, Pazlarova, Souskova, Khun, & Julak, 2015), containing mainly
reactive species, could be an alternative method for disinfection of
foods. Some of the studies have focused on the utilization of PAW for
bacterial inactivation and efficiently controlling bacteria growth. The
advantage of PAW is that it is easy to apply replacing the traditional
sanitizing solutions applied for disinfections. Nevertheless, further
studies will be required focusing on Life Cycle Assessment in order to
consider the technology at scale-up industrial environments.
This work presents a short introduction to PAW, plasma sources for
PAW generation, chemistry and properties of PAW and its potential
applications in food and agriculture. This review also provides useful
information for researchers looking for alternative methods of food
decontamination and disinfection while discussing the possibilities of
improving agricultural practices.
2. PAW generation and its chemistry
The type and the concentration of the reactive species that are
present in PAW depend on the gases and liquids used to generate
plasma (Lukes et al., 2012, 2014). Depending on the chemical en-
vironment, excited voltage and generation mode, reactive oxygen spe-
cies (ROS) and reactive nitrogen species (collectively described as
RONS) may be formed. The species are formed in the liquid or at the
liquid–gas interface. The existing literature set-ups are summarized in
Table 1. It is evident that apart from the plasma sources used, the
treatment time and gases used, the distance between the liquids and
plasma plume, nature of electrodes are important issues that should not
be underestimated. For example, the use of oxygen, nitrogen and water
as parent molecules for the production of PAW, will result in the for-
mation of a number of primary species (including atomic oxygen, singlet
oxygen, superoxide, ozone, hydroxyl radicals and excited and atomic
nitrogen) which will then continue to react to form secondary species
(including hydrogen peroxide, peroxynitrite, nitric oxide, nitrates and
nitrite ions) (Brisset & Pawlat, 2016; Lukes et al., 2014). Table 2 shows
the possible chemical reactions occurring during the PAW generation.
These are the main chemical reactions which result in the formation of
ROS and RNS in the PAW possessing the antimicrobial activity. As
presented in Table 1, there are two major approaches of generating
PAW. One involves contact of the plasma streaming with the water
while the other induces the plasma directly into the water. Chemistry
and reaction products of PAW generated above the water surface are
different from the PAW generated directly in the liquids.
22
Trends in Food Science & Technology 77 (2018) 21–31
3. Physical and chemical properties of PAW
3.1. pH
pH is the measure of the hydrogen ion concentration of a solution.
The reactions taking place between the chemical species formed in the
plasma and water results in the acidification. The pH of PAW is dras-
tically decreased with increase in treatment time due to the formation
of strong acids. In the patent on plasma activated water developed by
Pemen, Hoeben, van Ooij, and Leenders (2016) it was stated that the
proper combination of both non-thermal and thermal plasma for PAW
generation results in a controlled pH (from 0 to 7). Oehmigen et al.
(2010) have reported that the acidification of aqueous liquids through
the plasma reaction results in the generation of hydrogen peroxides,
nitric acid, and peroxynitrous acid. The formations of newly formed
chemical species in PAW are attributed to decrease in the pH. This
could be one of the main reasons for the anti-microbial activity of PAW.
Riordan, Minogue, Healy, O'Driscol, and Sodeau (2005) have reported
that the dissolution of these ions is the result of their solubility, the
nature of air gas/solid/liquid interface and the relationship between the
gas phases and dissolved counterparts in the aqueous phase. Ma et al.
(2015) observed a quick drop in pH during the initial phase of plasma
treatment while thereafter it reached a steady range. The pH was de-
creased from 7 to 3.2 after 10 min of activation using atmospheric
plasma jet (Ar/O2 - working gas) and did not show any change after
10 min (Ma et al., 2015). Xu, Tian, Ma, Liu, and Zhang (2016) also
observed a similar decrement in pH up to 3.7 after 5 min of treatment.
The decrease in the pH and the formation of acidifying compounds in
the PAW may vary from reactor to reactor (Bruggeman & Leys, 2009)
and feed gas used for plasma generation (Tian et al., 2015). Shainsky
et al. (2012) examined the dependence of pH values of PAW on dif-
ferent feed gases (Ar, O2, Air) used for plasma generation. They did not
find a significant change in pH of water when PAW was generated from
argon gas, while drop in pH was observed when generated from oxygen
and air with pH values of 2.01 and 2.07, respectively. Furthermore, the
storage studies of PAW revealed that the pH values slightly decreased
upon the storage time in PAW generated from air plasma but the pH of
PAW generated from oxygen showed a linear increment. Shainsky et al.
(2012) observed a decrease in PAW pH from 2.07 to 1.5 after 70 h of
storage. Shen et al. (2016) investigated the pH of PAW at different
storage temperatures (25 °C, 4 °C, −20 °C, −80 °C) up to 30 days of
storage. The authors have observed a decrease in pH to 2.3 from 6.8
after 20 min of plasma activation. They did not find any significant
change in pH values of PAW stored at different temperatures up to 30
days. This shows that the PAW inactivation efficiency could last for a
month. Plasma activation of distilled water for 20 min decreased the pH
to 2.8 (Traylor et al., 2011). These researchers also found that the pKa
of PAW after the activation is similar to the pKa value of nitrous acid.
3.2. Redox potential
The oxidation-reduction potential (ORP) measures the ability of a
solution to oxidize or reduce another substance and depends upon the
concentration of oxidizers and their strengths. The advantage of mea-
suring the ORP of water is that it provides a rapid and single-value
assessment of the disinfection potential (Suslow, 2004). ORP is con-
sidered as the important factor affecting the microbial inactivation,
which damages the cell membrane of microbes and defense mechanism
(Mcferson, 1993). Of those ROS species formed in PAW, hydrogen
peroxide mainly involves in the redox reactions where it can behave as
an oxidant (E0 = 1.77 V) or as a reductant (E0 = −0.7 V) (Lukes et al.,
2012). Zhang et al. (2016) reported that addition of oxidizing chemicals
results in an increase of ORP and observed a 63.3% increase in ORP
values of distilled water after the plasma activation for 20 min using
Ar/O2 gas plasma. A study on the generation of PAW using atmospheric
pressure plasma jet for 5, 10, and 15 min using premix of argon and
R. Thirumdas et al. Trends in Food Science & Technology 77 (2018) 21–31

Table 1
Overview of plasma systems that can be used for production plasma activated water. The main classification is based on previous report by Locke et al. (2012).
Mode of operation Critical parameters Chemistry References

1. Plasma in contact with liquids

Discharge over water and
hydrated Surfaces
Discharge with water
spray
Gas discharge in bubbles
2. Plasma directly in water
Gliding arc plasma discharge - Air flow
formed above liquid solution - Gap distance of
Increase surface area caused electrodes
by liquid spray - Distance between
Generation of the discharge electrode tips and liquid
within the bubbles - Treatment time
- Type of gases
- Voltage source
Electric discharges directly in - End plasma distance and
water water surface
- Gases
- Electrode types (e.g.
graphite, copper)
- Operating voltage
- Discharge current
- Frequency
- Electrode size
- H2O2 Kamgang-Youbi et al. (2009); Naitali et al. (2010); Ma
- Nitrite et al. (2015); Haghighat et al. (2017); Puač et al. (2017)
- Nitrates
- Superoxide anion
radicals
- Singlet oxygen
- Hydroxil radicals
- Ozone
- •OH, 1O2, •O2−
- Hydrogen peroxide Ma et al. (2016); Naumova et al. (2011); Park et al.
- Peroxide (2013); Shainsky et al. (2012); Shen et al. (2016); Zhang
- Nitrate et al. (2016); Ma et al. (2016)
- Nitrite
- Hydrogen peroxide
- Superoxide anion
(O2)
- Ozone
- Nitric oxide radicals
- Hydroxyl radical

Table 2 Comparative value of ORP (540 mV) was observed by Shen et al. (2016)
Chemical reactions taking place during PAW generation resulting in the for- in PAW generated using plasma jet with air as working gas with an
mation of ROS and RNS. Adapted from Pârvulescu, Magureanu, and Lukes activation time of 20 min. The work of Ma et al. (2015) reported similar
(2012) by courtesy of John Wiley & Sons. ORP value of 550 mV and resulted in the reduction of bacterial count by
H2O + e → OH• + H• + e− (1) 3.5 log reduction after 15 min of PAW application to the strawberries.
H2O + e → H+ + OH• + 2 e− (2) The higher the ORP values, the stronger the oxidizing capacity and
H2O + e → H• + O• + H• + e− (3) possesses a high antimicrobial potential (Ma et al., 2015).
O2 + e → O+ + O + 2e (4)
O2 + e → O− + O (5)
O + O2 → O3 (6)
O3 + NO → NO2 + O2 (7) 3.3. Conductivity
N + O2 → NO + O (8)
O + N2 → NO + N (9) Conductivity is a measure of the ability of water to facilitate electric
O + NO2 → NO + O2 (10) current flow through it. The presences of extraneous ions in water
2 NO + O2 → 2NO2 (11)
greatly affect the conductivity. The reactive species and ions produced
NO2 + OH → HNO3 (12)
H2O2 + hν → OH• + OH• (13) during plasma treatment readily dissolve in the water, which evidently
3 NO2 + H2O → 2 HNO3 + NO (14) alters the conductivity. The formation of ROS and RNS during plasma
H2O2 + H+ + NO2− → ONOOH + H2O (15) activation of water will contribute to an increase in the conductivity of
OH• + OH• → H2O2 (16)
PAW. The increase in conductivity of PAW by the formation of NOx
NO + NO → N2 + O2 (17)
NO + OH• → HNO2 (18)
species using gliding arc plasma were reported (Brisset, Benstaali,
HNO2 + OH• → NO2 + H2O (19) Moussa, Fanmoe, & Njoyim-Tamungang, 2011; Benstaali, Moussa,
NO2 + hν → NO + O• (20) Addou, & Brisset, 1998) and by spraying water directly into the gliding
NO3 + hν → NO + O2 (21) arc plasma zone (Burlica & Locke, 2008). The conductivity is generally
NO2 + NO3 → N2O5 (22)
measured in micromhos per centimeter or microsiemens per centimeter
N2O5 + H2O → 2HNO3 (23)
2 NO2 + H2O → NO2− + NO3− + 2H+ (24) and the conductivity of distilled water vary between 0.5 and 3 μS/cm.
3 NO2− + 3 H+ → 2 NO + NO3− + H3O+ (25) Ma et al. (2015) found the conductivity of distilled water to be 450 μS/
OH + NO2 → [O=N–OOH] → O=N–OO− + H+ (26) cm after the activation with Ar/O2 gas plasma jet for 20 min due to the
generation of active ions. The report of Tian et al. (2015) showed that
the 18.8 μS/cm conductivity after 20 min of plasma activation using
oxygen gases (Ar 98% and O2 2%) was conducted by Xu et al. (2016). plasma microjet. The obtained values of conductivity were observed to
They observed an increment in ORP value from 146 mV to 314 mV for be much less compared to that reported by Ma et al. (2015). Both the
5 min treatment and on further increase in activation times to 10 and authors worked on using similar working gas but the applied voltage
15 min lead to ORP values of 397 mV and 467 mV, respectively. The (0.40–0.42 kV) is very low in the case of PAW generated using plasma
authors also employed OES to examine the reactive species formed in microjet and this might be the reason for the low conductivity. Fur-
PAW and found good agreement between the OES results and ORP thermore, the conductivity of PAW generated inside the water directly
values. Tian et al. (2015) observed higher ORP values (up to 20%) for is more when compared to that of the PAW generated above the water
PAW generated inside the water when compared to the PAW generated surface. In another study conducted by Xu et al. (2016) for generation
above water surface. Locke, Lukes, and Brisset (2012) reported that the of PAW using atmospheric plasma jet observed a linear increase in
electric discharge plasma over the liquid surface has significant differ- conductivity (218 μS/cm) from 17 μS/cm (untreated water) after
ences in properties from those directly generated in the liquid because 15 min of plasma activation. Locke et al. (2012) observed a stronger
of the lower breakdown strength, density and conductivity of the at- intensity of radiations and higher electron density in the discharge due
mospheric gas. Like pH, the different storage temperatures of PAW did to increase in conductivity. Brisset et al. (2011) investigated the acidity
not cause any significant change in ORP values but different storage control of plasma oxidation reactions using air plasma over the aqueous
times resulted in the decrement of ORP values (Shen et al., 2016). This surface and observed an increase in conductivity and attributed it to the
shows that the ORP values are not temperature compensated. peroxynitrite chemistry. But when working with nitrogen free working

23
R. Thirumdas et al. Trends in Food Science & Technology 77 (2018) 21–31

Table 3
Salient results of studies conducted on physical and chemical properties of PAW.
Plasma devices Working gas Activation time (min) pH ORP (mV) Conductivity (μS/cm) Reference

Plasma jet Ar/O2 15 3.0 550 450 Ma et al. (2015)

Plasma microjet Air 20 2.3 540 Shen et al. (2016)
Plasma microjet Ar/O2 20 6.1 250 18.8 Tian et al. (2015)
DBD micro discharge Air 15 2.7 – – Traylor et al. (2011)
Plasma jet Ar/O2 15 3.7 467 218 Xu et al. (2016)
Gliding arc Air, O2, N2 15 2.8, 3.2, 3.0 – 1100, 300, 500 Burlica and Locke (2008)
Plasma microjet Ar/O2 20 – 490 – Zhang et al. (2016)
High voltage electrode Argon 15 3.0 – 200 Thagard, Takashima, and Mizuno (2009)
DBD Air,O2 20 2.1, 2.2 – – Shainsky et al. (2012)
Low frequency plasma jet He 5 4.2 – – Ikawa et al. (2010)
DBD with hallow electrodes Air 10 1.9 550 2000 Zhang et al. (2016)
Gliding arc Argon 2 3.6–3.7 – 50–70 Burlica et al. (2010)

gases, the conductivity is attributed to H3O+ ions formed in the water
since nitrogen oxides are not found (Lukes et al., 2012). Lukes, Clupek,
Babicky, and Sunka (2008) conducted a study on the influence of ap-
plied voltage and conductivity of water on the intensity of ultraviolet
radiation formed from the corona discharge. The increase in con-
ductivity of water greatly influenced the emission intensity of UV ra-
diation. A similar increase in radiated power in the UV range was ob-
served with increasing water conductivity (Bruggeman & Leys, 2009).
Laurita, Barbieri, Gherardi, Colombo, and Lukes (2015) investigated the
effect of nanosecond pulsed DBD air plasma on pH and conductivity of
PAW. The authors observed an increase in conductivity to 1435 μS/cm
from 1.5 μS/cm after 10 min of activation. Table 3 shows an overview
of investigations on physical and chemical parameters of PAW gener-
ated from different plasma devices (e.g., DBD, jets etc.) and carrier
gases.
3.4. Hydrogen peroxide production
H2O2 is a ROS formed in the PAW which plays a significant role in
the antimicrobial properties of PAW. Several researchers investigated
the chemical processes for the H2O2 formation and assessed its im-
portance for the antimicrobial activity of PAW. The analytical methods
for the measurement of H2O2 include assays like iodometric titration,
permanganate titration, titanium oxalate (spectrophotometer), perox-
idase enzyme assay kit. In the acidic medium, H2O2 concentration along
with the superoxide anion contributes to the most important part of the
oxidation properties of the PAW (Shainsky et al., 2010). Lukes et al.
(2008) stated that the mechanism of H2O2 formation, the recombina-
tion of OH radicals formed by the electronic impact of water molecule
dissociation. The calculations on fluid chemistry performed by van Gils,
Hofmann, Boekema, Brandenburg, and Bruggeman (2013) have inter-
preted that the all adsorbed OH radicals will get converted into H2O2
and then thus formed H2O2 in the gas phase will be transported to the
treated liquids. Stara and Krčma (2004) studied the H2O2 generation
from the discharge in water and investigated the factors influencing the
hydrogen peroxide production. The authors have reported that the
applied voltage and discharge duration linearly increased the formation
of hydrogen peroxide. For example, Ikawa, Kitano, and Hamaguchi
(2010) found 1.469 mM H2O2 concentration in the helium plasma jet
activated water after 180 s of activation. In other studies the con-
centration of H2O2 formed in PAW was estimated to be 22.4 μM after
20 min of air plasma activation (Shen et al., 2016). As stated by Lukes
et al. (2008), the concentration of H2O2 depends upon the conductivity
of water after the discharge. In acidic medium, the conjugate base
((HO2−) measured using mass spectrophotometry) of H2O2 can lead to
the additional production of H2O2 (van Gils et al., 2013). The authors
have observed the final concentration of H2O2 produced is approxi-
mately 0.6 mM and is sufficient enough to inhibit bacterial growth.
Shainsky et al. (2010) conducted experiments on generation of PAW
by directly exposing the deionized water to DBD plasma. They have
observed 58.7 mM H2O2 concentration immediately after the exposure
to plasma which dropped to 0.2 mM after the 15 min of activation. For
example, the half-life of H2O2 is 1 ms at air-liquid interface and is
comparatively high to the half-life of singlet oxygen and hydroxyl ions
found to have 1 μs and 1ns respectively (Møller, Jensen, & Hansson,
2007). However, the H2O2 is considered as the steady end product in
water and has a half-life in the range of 8 h–20 days (Sun et al., 2012).
Laurita et al. (2015) quantitatively analyzed the concentration of H2O2
and found it to be 200 μM in DBD air plasma activated PAW. The au-
thors have also conducted the post-discharge kinetics on the decom-
position of H2O2 in PAW at different times. After 25 min of post-dis-
charge kinetics, the H2O2 concentration was decreased to
approximately 110 μM. Similarly, Lukes et al. (2014) also conducted
the post-discharge kinetics of H2O2 and the concentration was de-
creased to 100 μM from an initial concentration of 200 μM after 5 h of
post discharge time. The formation of nitrate from the reaction between
the nitrite and hydrogen peroxide during post-discharge could be one of
the reasons for the decrease in hydrogen peroxide concentration
(Burlica, Grim, Shih, Balkwill, & Locke, 2010). An investigation has
been carried out to evaluate the concentration of H2O2 generated by
gliding arc discharge in water (Kim et al., 2013). The flow of air and
water into the gliding arc generator was optimized so as to get max-
imum yield of H2O2. Plasma activation of water resulted in a maximum
concentration of 0.8 mM of H2O2 after activation.
3.5. Nitrites (NO2−) and nitrates (NO3−) ions concentration
The detection of nitrites and nitrates ions in the PAW is the main
evidence for the formation of RNS and considerable interest was drawn
by many researchers in recent years for its anti-microbial activity. Shen
et al. (2016) reported that the long-lived nitrate ions in PAW are formed
as the secondary products and extend the anti-microbial activity on
storage. The authors have observed the concentration of NO3− and
NO2− in 20 min PAW around 42 mg/L and 1.2 mg/L, respectively. The
post-discharge reactions between NO2− and H2O2 occurring in PAW
resulted in the formation of peroxynitrite which has a significant anti-
bacterial property (Lukes et al., 2014). Like ROS, the NO3− and NO2−
concentration decreases with increase in storage time. Burlica et al.
(2010) generated PAW using continuous gliding arc plasma reactor at
different water flow rates (0.5–2 ml/min). The nitrogen oxides formed
through the dissociation of N2 and O2 in the air plasma react with water
and result in the formation of nitrite ions and these nitrite ions react
with H2O2 to form nitrate ions. Lukes et al. (2014) studied the forma-
tion of nitrate from the post-discharge reaction between nitrite and
H2O2. The authors have proposed a reaction for formation of nitrate as
follows:
NO2− + H2O2 + H+ → NO3− + H2O + H+
It was previously reported that the concentrations of nitrate and
nitrites ions were 113 mg/L and 1.5 mg/L after 30 min of PAW

24
R. Thirumdas et al. Trends in Food Science & Technology 77 (2018) 21–31

activation using oxygen gas DBD plasma treatment (Oehmigen et al.,

Kamgang-Youbi et al. (2009)

2010). The discharge of plasma over the water surface and directly

Oehmigen et al. (2010)

inside the water resulted in different concentrations of nitrates and

Shainsky et al. (2012)

Traylor et al. (2011)

Naitali et al. (2010)

Zhang et al. (2016)

Zhang et al. (2016)

nitrites formed in the PAW generated using premixed Ar/O2 gas plasma

Shen et al. (2016)

Tian et al. (2015)

Sun et al. (2012)

Ma et al. (2015)
Xu et al. (2016)
microjet (Tian et al., 2015). The concentration of nitrates and nitrites
formed in PAW generated by direct discharge in the water is slightly

Reference
higher to that generated over the surface of the water. Park et al. (2013)
conducted experiments on the effect of nitrate and nitrite ions formed
in PAW for plant growth. The activation of water up to 2 min using

Surface attached cells

Surface attached cells

Surface attached cells
gliding arc plasma resulted in 56 mg/L and 12 mg/L of nitrate and ni-
trite ion concentrations, respectively. In the presence of UV radiations,

Planktonic cells
Planktonic cells
Planktonic cells

Planktonic cells
Planktonic cells

Planktonic cells
Planktonic cells
Adherent cells

Adherent cells
the nitrates and nitrites act as indirect photosensitizers and produce

Form of cells
secondary oxidants such as superoxide and hydroxyl radicals (Tarr,
2003).

4. Applications of plasma activated water (PAW)

Inactivation (in Log10 CFU/mL or CFU/g)

It has been well established that the application of cold plasma di-
rectly on food products plays a significant role in the microbial in-
activation. Among the several experiments conducted on the microbial
inactivation, the use of different working gases and applied voltages are
the important factors for the anti-microbial activity. The indirect ex-

1.9,1, 0.25, 0.3, 0.7

posure of fresh produce to cold plasma is through the plasma activated

3.5, 3.6, 4.5, 5.0

1.84, 3.16, 5.36
0.52, 1.27, 3.07
3.52, 3.98, 4.69
water (Scholtz et al., 2015). Recently, the application of PAW is gaining

1.7, 2.0, 2.25

1.5, 1.6, 1.9

6.8, 5.7, 2.5

3.2, 3.6, 4.0
importance among the researchers as a source of anti-microbial solution

0.22, 1.5

4.1, 5,7
or disinfectant solution. After the postharvest handling, washing the

1, 2, 5

6, 2
raw produce and fresh fruit cuts with water or other disinfection so-

5.6

7
lutions for enhancing shelf-life is an important component of food
Treatment time (min)

safety programs from farm to fork. One of such disinfection solutions

currently being used is the application of high oxidation reduction
potential (ORP) water. A particular benefit of using PAW is that it can

10, 20, 30
0.5, 1, 1.5

replace the high ORP water produced by addition of chemicals. The

5, 10, 15
5, 10, 15

5, 10, 20
other potential application of PAW is the enhancement of seed germi-

2, 4, 6
5, 10

nation and plant growth. Ji et al. (2015) reported that the reactive
15

15

20
20

10
20
species formed from the chemical donors play a prominent role in the
Storage period (day)

seed germination and plant development. Changing the properties of

water with the nonthermal plasmas and its utilization may affect the
1, 3, 7, 15, 30

plant growth process and increase the agricultural produce quality

(Park et al., 2013).
0, 1
0

0
4
–
–

–
–
–

–
–
4.1. Role of PAW on microbial inactivation
Activation time (min)

This section presents the role of PAW on microbial inactivation and

summarizes a number of studies that appeared in the literature the past
5, 10, 15, 20

years. Table 4 illustrates the log reduction of different microorganisms

after PAW treatment. From the reports it was observed that most of the
5, 10

PAW applications have been applied to planktonic, adhered or food

20
15

20
20
20
10
10

20
7

surfaced attached cells (Kamgang-Youbi et al., 2009; Sarangapani,

Key findings of inactivation of microorganism using PAW.

Patange, Bourke, Keener, & Cullen, 2018). The ROS and RNS species
plume touching the water surface
plume touching the water surface
discharge over the water surface
discharge over the water surface
discharge over the water surface

discharge over the water surface

Plasma discharge over the water surface

Plasma discharge over the water surface

generated in the PAW by plasma activation are responsible for micro-

bial inactivation (refer to Section 4.1.1, 4.1.2 for full description of
discharge inside the water

Plasma discharge inside the water

Plasma discharge inside the water

Plasma discharge inside the water

their mechanism in microbial inactivation). The formation of these

chemical species in PAW shows the synergistic effect of high ORP and
low pH proved to possess anti-microbial activity (Zhang et al., 2016).
Dolezalova and Lukes (2015) reported that the presence of humid air or
Mode of activation

the contact with liquid dramatically changes the reaction products and
the mechanism of microbial inactivation. The chemistry of PAW gen-
erated under water is much more complex and in addition to chemical
Plasma
Plasma
Plasma
Plasma
Plasma
Plasma
Plasma

species, the physical parameters like strong electric fields, UV radia-

tions, shock waves also contribute to microbial inactivation (Li et al.,
2008).
L. mesentroids
S. cerevisiae
Aerobic bacteria
Microorganism

Most recent work on the application of PAW on fresh produce like

strawberries for microbial inactivation was reported by Ma et al.
B. subtilis
S. aureus

H. alvei,

H. alvei

(2015). The authors observed a total of 3.5 log10 CFU/mL reductions of

Table 4

E. coli

bacterial count in 20 min plasma activated water (plasma discharge

over the water surface) for 15 min of treatment time. Fernandez,

25
R. Thirumdas et al.
Noriega, and Thompson (2013) directly applied the cold atmospheric
gas plasma for the microbial inactivation of strawberries. They ob-
served only 1.72 log10 CFU/mL reduction of the bacterial count after of
nitrogen plasma jet treatment for 15 min. The inactivation percentage
of PAW is higher compared to the direct application of cold gas plasma.
This could be related to the surface topography of strawberries which
consists of several eyes and grooves and had a significant role on the
inactivation efficiencies. This might have restricted the cold gas plasma
species to reach deep inside the eyes which shielded the bacteria
whereas soaking in PAW easily facilitated the reactive species and en-
hanced the inactivation of bacteria.
Xu et al. (2016) inactivated button mushrooms using PAW gener-
ated (plasma plume touching the water surface) using atmospheric
plasma jet at high voltage 18 kV for different treatment times (5, 10,
15 min). The water activated for 10 min had a significant effect on
bacterial growth even at the 7th day of storage and observed a max-
imum of 1.5 log10 CFU/mL reductions. The authors reported that re-
active species formed in PAW accumulated around the cell membranes
causing the decrease in the membrane potential and cell death occurred
due to breach in the cell membrane. A similar type of microbial in-
activation mechanism of PAW (generated by direct discharge of plasma
into the water) was proposed by Tian et al. (2015). The authors ob-
served 5 log10 CFU/mL microbial reductions after a treatment for
20 min with PAW being generated under the water. The inactivation
efficiency of PAW generated beneath the water is much higher than
when PAW generated above the water surface (only 1.2 log reductions
is reported). The main reason for higher inactivation efficiency could be
the synergistic effect of physical processes like electric fields and shock
waves when generated directly in the water (Lukes et al., 2008). Lukes
et al. (2012) have also reported that the microbial inactivation effi-
ciency is higher when the plasma is directly discharged in the water or
in some cases when the plasma plumes are touching the liquid surface.
Moreau, Feuilloley, Orange, and Brisset (2005) investigated the leth-
ality of PAW generated using gliding arc plasma on Erwinia spp. There
is a complete inactivation in the growth rate of Erwinia spp. after 10 min
of treatment. Similarly, Naitali, Kamgang-Youbi, Herry, Bellon-
Fontaine, and Brisset (2010) observed 99.9% inactivation of Hafnia
alvei in 20 min PAW using gliding arc plasma reactor. They stated that
the inactivation efficiency of Hafnia alvei using PAW is different when
PAW was generated with and without subjecting to the plasma plume.
The direct discharge of plasma into water uses the principles of both
chemical and electrical effect for inactivation mechanism. A similar
inactivation mechanism has been observed in pulsed electric fields
applied to water. Souskova et al. (2011) studied the inactivation of
fungal (Aspergillus oryzae - DBM 4002, Cladosporium sphaerospermum -
DBM 4282), and yeast cells (Penicillium crustosum - DBM4159) by
generating direct current corona electric discharge over the surface of
the water. It was reported that complete death of all yeast cells from 5
log10 CFU/mL after 6 min of PAW activation. The authors observed that
the time for inactivation of A. oryzae spores is longer compared to
spores of C. sphaerospermum. The authors have also reported that, even
after 30 min of exposure could not inactivate A. oryzae spores com-
pletely. Whereas the complete inactivation of C. sphaerospermum spores
was observed after 25 min treatment. From the few reports, it was ob-
served that the inactivation efficiencies of plasma applied directly or
through PAW on fungal cells is less compared to that on the bacteria
cells. Scholtz et al. (2015) have reported that the difference in in-
activation efficiencies is due to complex cell structure of eukaryotes
than the prokaryotes. The strong defensive system (i.e., antioxidants,
enzymes) of the fungal cells protected the cells from oxidative stress
created by the plasma treatment. The inactivation of viruses using PAW
is still unexplored but there are a few reports available on direct cold
gas application (Alshraiedeh, Alkawareek, Gorman, Graham, &
Gilmore, 2013; Terrier et al., 2009).
26
Trends in Food Science & Technology 77 (2018) 21–31
4.1.1. Mechanism of ROS in microbial inactivation
Among the several ROS produced in PAW, H2O2, hydroxyl ions
(OH●), ozone (O3) chemical species are considered as potent anti-mi-
crobial agents. The hydroxyl radical (OH●) is an important ROS which
primarily targets the outer membrane of the microbial cells. Dolezalova
and Lukes (2015) described the mechanism of ROS causing lipid oxi-
dation of the cell membrane. The OH● radicals initiate the lipid per-
oxidation reaction by subtracting H from the unsaturated carbon bonds
of fatty acids result in the formation of malondialdehyde (MDA) as an
end product, which is used as the marker for lipid oxidation. The per-
centage of MDA concentration in bacterial suspension was increased by
48% after 45 min of plasma activation. The presence of mal-
ondialdehyde in microbial cells causes damage to DNA and result in cell
death (Marnett, 1999; Thirumdas et al., 2015). The mechanism of dif-
fusion of radicals into the cells through the membrane mainly depends
on the mass transfer at controlled diffusion rates (Watts, Kong, Orr,
Miller, & Henry, 1995). Yusupov et al. (2013) studied the interaction
mechanism between the ROS and bacterial cell wall components. The
authors have reported that ROS particularly OH● and H2O2 have the
potential to break the intra-molecular bonds of peptidoglycan which
could lead to cell wall breakdown. OH● removes the H atom from the
alpha carbon of peptide bonds -CO-NH- from the peptidoglycan back-
bone of the cell wall linked with the amino acids (Lukes et al., 2012).
Deng, Shi, and Kong (2006) have reported that the action of ROS on
bacterial spore caused slight shrinkage, cytoplasmic leakage and finally
breakdown of spore membrane. It is also known that the transport of
ROS from the PAW into the microbial cells causes internal damage
through the breakdown of DNA, the destruction of proteins and other
internal components of the cell (Lukes et al., 2012). Tian et al. (2015)
investigated the effect of PAW on the intracellular nucleic acids of
bacterial cells by detecting the release of intracellular components.
They have estimated the leakage ratio of DNA/RNA from the cells as the
function of plasma activation time. It was observed that there is an
increase by 42% of the leakage ratio of DNA/RNA after 20 min of ac-
tivation. They have stated that the integrity of cell membrane was de-
stroyed by PAW resulting in an increase in leakage ratio. Similarly, in
Saccharomyces cerevisiae, the amount of intracellular proteins and ex-
tracellular DNA was increased after PAW treatment probably due to the
cell wall and cell membrane leakages (Chen, Bai, & Xiu, 2010). In PAW
treated yeast cells, the authors have observed that the cell cycles were
arrested at G1 phase and this was attributed to DNA damage. In addi-
tion, they have also found an increase in the superoxide dismutase
enzyme activity in PAW treated cells showing the increase in oxidative
stress of the cells by ROS particularly superoxide ion O2−. Thus, the
authors concluded that PAW treatment could possibly cause cell da-
mage, cell mutation, and cell apoptosis.
Tian et al. (2015) carried out an investigation on the formation of
intracellular ROS concentration in PAW treated S. aureus using di-
chloro-dihydro-fluorescein diacetate (DCFH-DA) dye. Under the fluor-
escence microscopic observation, almost all the cells are stained green
and the fluorescence intensity of colour is very high for 10 min acti-
vated PAW generated using Ar/O2 gas plasma microjet. The fluores-
cence intensity and colour is found to be reduced in 20 min activated
PAW. The authors have explained that the reason could be due to high
oxidative stress created on cells leading to the death of cells. Further,
the authors examined the membrane potential of cells and the intensity
of red/green dots after PAW treatment. They have observed a decrease
in the red/green ratio (approximately near 1) from 1.348 after the
treatment suggesting the depolarization of cell membrane. The im-
portant antimicrobial mechanism of H2O2 is through the generation of
intracellular OH● in the presence of transition metals. The interaction
between the H2O2 and superoxide ion results in the formation of OH●
through Fenton or Haber-Weiss reaction (He & Häder, 2002) which
causes oxidative damage by stimulating the breakdown of double helix
strands of DNA (Keyer, Gort, & Imlay, 1995).
R. Thirumdas et al.
4.1.2. Mechanism of RNS in microbial inactivation
The potent RNS species formed in the water are nitric oxide (NO●)
and its derived products like nitrates, nitrites, and peroxynitrites
(ONOOH). The primary action of RNS on the microbial susceptibility is
through lowering the pH of the PAW. The formation of HNO3, HNO2
and HNOOH in PAW results in acidification responsible for inactiva-
tion. The formation of peroxynitrite ions in PAW is a very strong oxi-
dizer participating in reactions responsible for microbial inactivation.
The efficiency of microbial inactivation of PAW is different from that of
acidified plasma processed liquids (PPL). The inactivation efficiency of
acidified water was reported by Schnabel et al. (2016). Naitali et al.
(2010) observed a very slight decrease in microbial count of acidified
water compared to PAW. The synergistic effect of RNS with ROS and
physical parameters can have a combined inactivation efficiency of
plasma which are absent with acidified water. The formation of per-
oxynitrite ions in PAW can be detected by measuring the changes in
conductivity. The peroxynitrite formed in PAW was reported by Lukes
et al. (2012) in which it was shown that the peroxynitrite half-life is
short but sufficient to diffuse into cells and consequently lead to mi-
crobial inactivation. Peroxynitrite can interact with membrane lipids
and initiate lipid peroxidation ultimately leading to cell death. Rubbo,
Trostchansky, and O'Donnell (2009) stated that the peroxynitrite can
oxidize many macro-biomolecules like protein tyrosine residues, thiols,
and unsaturated fatty acids. Peroxynitrite ions have the potential to
cause oxidative, mutagenic and cytotoxic damage to the microbial cells
(Bryk, Griffin, & Nathan, 2000). Peroxynitrile ions may also react with
dissolved carbon dioxide to produce ONO2CO2−, which can then pos-
sibly produce a •CO3− radical, which is a powerful oxidizing agent
(Lymar and Hurst, 1988). It has been postulated that the •CO3− radical
is capable to oxidize several critical amino acids in proteins (Adams
et al., 1972), even in the presence of antioxidants which are normally
present in biological fluids (Lymar and Hurst, 1988).
4.1.3. Microbial inactivation by physical parameters
The important physical parameters responsible for microbial in-
activation are pH, ORP, UV radiation, shock waves, photons and elec-
tric fields formed in PAW (Fig. 1). The formation of reactive chemical
species in PAW decreased the pH. The environmental pH significantly
affects most of the microbes because they do not have the mechanism to
adjust their internal pH (Frazier and Westhoff, 1998). Yeast and molds
are more resistant to acidic pH than the bacteria. Most of molds and
yeasts can favor and survive in the pH range of 2–8.5 and 4–4.5, re-
spectively but the bacteria cannot survive in the pH below 3.7. The pH
and ORP are the direct measurement of ROS and RNS formed in PAW
and mainly depend on the activation time, feed gas and activation
distance from the liquid surface. Suslow (2004) reported that the time
taken for water with ORP of more than 650 mV to inactivate bacterial
species like E. coli, Salmonella spp., and Listeria monocytogenes was <
10 s, < 20 s, and < 30 s, respectively. The UV-radiation of wavelength
ranging between 200 and 280 nm is known to have the bactericidal
effect. The important mechanism of bacterial inactivation of UV ra-
diations is dimerization of thymine bases in their DNA strands (Laroussi
& Leipold, 2004). Spetlikova, Janda, Lukes, and Clupek (2010) in-
vestigated the role of UV-radiation on the bacterial inactivation formed
in PAW. It was reported that 40–50% of total bacterial inactivation was
contributed by the UV radiations formed by direct discharge of plasma
underwater. The higher the conductivity of PAW, the stronger the in-
tensity of UV radiations formed in the underwater discharged plasma.
Lukes et al. (2008) stated that the UV light formed in PAW contributed
nearly 30% of E coli inactivation, when the E. coli was present in the
growth medium during the plasma treatment. Wu et al. (2012) applied
non-thermal plasma to water using the plasma microjet device and
observed a total bactericidal UV-radiation density of 9 μJ cm−2, after
20 s of treatment.
Shock waves are generated in PAW which creates cavitation bubbles
that play a role in inactivation. Generation of high-intensity electric
27
Trends in Food Science & Technology 77 (2018) 21–31
fields in PAW could be lethal to microbes (Lukes et al., 2012). The
development of electric charge across the cell membrane increases the
permeability due to formation of the pores by a process called elec-
troporation. The ROS radicals can easily pass through the cell mem-
brane and cause oxidative damage to cells.
4.2. Enhancement of seed germination
Amongst the several reasons for loss of crop yields, the loss of seed
survivability due to contamination, low percentage of germination rates
and longer germination times are important (Mitra et al., 2014). The
seedling growth during germination involves two key steps, which are
primary cell elongation of the axial part of the embryo, and simulta-
neous or delayed cell division in the radicle meristem (Šírová,
Sedlářová, Piterková, Luhová, & Petřivalský, 2011). Ling et al. (2014)
reported that the cold plasma treatment enhanced the seed germination
during the draught stress conditions. Currently, the use of PAW for
enhancement of seed germination is limited. An underwater electric
front type discharge was used to generate PAW and treated the rye
seeds for 5 min. The germinability was increased by 50% and the
number of seeds germinated was also reported to increase (Naumova,
Maksimov, & Khlyustova, 2011). El-Maarouf-Bouteau and Bailly (2008)
stated that along with hormones, the ROS and NO radicals participated
in several signaling pathways involved in the seed germination. The
studies related to germination suggested that the ROS including su-
peroxide, hydroxyl radical, hydrogen peroxide and atomic oxygen are
responsible for seed germination (Su, Lan, Pritchard, Xue, & Wang,
2016). These ROS species are produced and released by mitochondria
inside the cell considered as active sites for production (Møller et al.,
2007). The formation of additional ROS generated in the PAW could
further enhance the seed germination.
The presence of ROS or seeds supplied with water containing ROS
donating compounds enhanced the germination rate by breakdown of
seed dormancy. Puač et al. (2018) reported that the presence of H2O2 in
the PAW could activate the CAT genes for the synthesis of new proteins
which have enhanced the seed germination of Paulownia tomentosa
seeds. In the investigation carried out by Su et al. (2016) on the en-
hancement of seed germination in the presence ROS (via methylvio-
logen as ROS donor), a close relation between the seed germination
initiation and breakdown of seed dormancy was found, while ROS acted
as a signal in dormancy alleviation. In water containing 1 mM me-
thylviologen, the germination rate after 10 days was observed to be
more than 60% compared to control. Similarly, when the water con-
taining 100 mM H2O2 was supplied to seeds, the germination rate was
increased by 79%. Liu, Ye, Liu, Chen, and Zhang (2010) also reported
that application of H2O2 decreased the abscisic acid hormone which is
responsible for seed dormancy and inhibits the seed germination. The
exogenous H2O2 stimulated the seed germination of barely dormant
seeds and inactivated the Abscisic acid hormone (El-Maarouf-Bouteau &
Bailly, 2008). While it appears that NO can break the seed dormancy
and enhance the seed germination (Šírová et al., 2011). Batak et al.
(2002) reported that the NO is an active agent in seed germination and
finding an alternative NO donor compounds during seed germination
significantly affects the rate of germination. The authors also stated that
in nitrate-stimulated seed germination, the nitrogen compounds like
nitrates and NO, affects the phytochrome activity by changing the light
requirements for seed germination. The RNS participate in several sti-
mulation pathways along with the plant hormones and some ROS,
break the seed dormancy and stimulate seed germination. Thus, we can
conclude that the active species formed in PAW could serve as external
donors of NO, NO2, H2O2, CO2 to enhance the seed germination.
4.3. Improvement in plant growth
Ammonium and nitrate are the predominant sources of nitrogen
absorbed by the plants for their growth from the soil. These are formed
R. Thirumdas et al.
Fig. 1. Schematic diagram of the PAW induced cell destruction through the different mechanisms caused by the reactive species (ROS and RNS), physical parameters
(pH, ORP, UV radiations and shock waves), lipid peroxidation ( ) and electroporation (+).
in the soil through nitrogen fixation by some nitrogen fixing bacteria.
The generation of nitrates in PAW can be achieved by the discharge of
plasma and they can serve as an alternate source of nitrogen for plant
growth. The atmospheric nitrogen/nitrogen gas is captured and con-
verted to other reactive radicals through plasma activation in water.
Takahata et al. (2014) conducted experiments on the application of
PAW produced by magnetic compression type pulsed power generator
for producing bubble discharge in water to enhance the plant growth.
After 63 days of cultivation of the strawberry plants, the height of
plants was observed to be 158 and 175 mm in 15 and 30 min activated
PAW, whereas controlled plant reached 121 mm of height. They also
found similar increase in plant heights of spinach and radish after
cultivating using PAW. The leaf size was also observed to be increased
after the treatment. The authors have concluded that the formation of
nitrate nitrogen in PAW absorbed through the roots as a nutrient is the
main reason for promoting the plant growth. Park et al. (2013) studied
the effect of PAW generated using gliding arc discharge on the growth
of different plant species. It was observed that the Alfalfa root and stem
length increased to 6.2 cm and 5 cm, respectively, in PAW compared to
1 cm for control samples. Similar results were also observed for pole
beans and watermelons plant growth after the PAW treatment. The
authors reported that the formation of nitrates and nitrites in PAW play
an important role in plant growth, along with the formation of hy-
drogen peroxide. They also conducted experiments on the plant growth
using PAW alone and with a combination of fertilizers. For the pepper
and tomato plants, the stem and root length was higher in PAW added
with fertilizers compared to other treatments. Similar results were also
reported by Lindsay et al. (2014) in radish, marigold, and tomato plants
grown using PAW. The authors observed an increase in average height
of the plants grown in PAW compared to control groups. The average
28
Trends in Food Science & Technology 77 (2018) 21–31
length of leaves of radish plants grown in PAW is 100 mm more than
control groups at the end of 15 days of the growth phase. They have
also reported that average shoot masses for plants grown in PAW is
more than the control groups but the average root masses were more for
control groups.
Naumova et al. (2011) observed that the length of roots was double
after treating the rye seeds with 5 min activated PAW. The PAW
treatment also increased the length of germ coleoptiles 1.5 times more
compared to control specimens. Similarly, the length of plant roots of
Zinnia annual after watering with the PAW was increased 1.5–2 fold
times than the control samples. The average plant length for plasma
irradiated radish seeds is found to be higher than the control samples
(Sarinont et al., 2014). The plasma treatment of radish seeds increased
the plant length 3.7 times more than the control. It was observed that
the temperature of seeds after the treatment has a significant effect on
the plant growth. The authors have reported that the interaction be-
tween the ROS and seeds enhanced the growth of plants due to the
intracellular chemical signals and messengers. Takaki et al. (2013)
treated the drainage water with plasma for 10 and 20 min and used the
same water for plant cultivation of Brassica rapa var. perviridis for 28
days. In 20 min activated PAW, the length was observed to be 90 mm
whereas in control groups 40 mm is noted at the end of 28 days of
cultivation. The authors have stated that the PAW supplied the RNS
necessary for plant growth of which nitrate and nitrite species worked
as a fertilizer.
From the above is evident that although PAW has a negative effect
on microbial contaminants that is not the case for the plant cells. The
important difference is the nature of cell wall and thickness. The bac-
terial cell wall is made of peptidoglycan which undergo membrane lipid
peroxidation whereas plant cell walls are made of cellulose and
R. Thirumdas et al.
hemicellulose which are resistant to reactive species. This results in
different electrical conductivity of the cell membranes.
4.4. Effect of PAW on quality attributes of fresh produce
Ma et al. (2015) analyzed the colour of strawberries after the PAW
treatment. The authors did not find any significant change in L*, a*, and
b* values of strawberries after the PAW treatments at 0 day and 4th-day.
In fact, they observed a slight increase in the redness at the end of 4th-
day. Similar increase in L*, a* and b* was observed by Xu et al. (2016)
in PAW treated button mushrooms. The authors have reported that
there is an increase in the whiteness of mushrooms which could be due
to oxidizing and bleaching actions of ROS generated in PAW. The effect
of PAW on the redness of strawberries is similar to the results reported
on direct application of cold plasma. The PAW (i.e generated using
atmospheric plasma jet, voltage - 8 kV, feed gas - 98% Ar and 2% O2 per
volume) treatment increased the firmness of the strawberries with in-
crease in treatment time (Ma et al., 2015). A similar study was con-
ducted by Ma et al. (2016) on the fruit decaying and fresh produce
quality of Chinese bayberry after soaking in PAW which was generated
by air plasma discharge directly into the water using plasma jet. The
authors observed a higher firmness, colour index and total soluble so-
lids in PAW treated berries compared to control samples after the 8 days
of storage. Other potential effects of PAW can be the decrease of the
browning reaction in the cut fruits and vegetables. By the soaking or
treating the cut fruits and vegetables with PAW, the enzymatic
browning enzymes activity can be inhibited (Xu et al., 2016). The au-
thors observed a decrease in the browning after the PAW treatment
compared to water soaked mushrooms.
Till date, there are no reports on the application of PAW to prevent
enzymatic browning reactions (Tappi et al., 2014).
5. Limitations
The complexity of atmospheric pressure plasma devices, differences
in design and operations can lead to different reaction compounds with
different mechanisms. The chemistry of gas plasma is very complex and
controlling the reactions is a major problem. The most important lim-
itation is the short half-life of the reactive species like OH, 1O2 produced
in the PAW. There are some significant differences in the properties of
PAW when activated above the water surface and beneath the water.
These two producing methods of PAW have different biological effects
which need more attention. To know the antimicrobial efficiency of
PAW, the complete diagnostics of plasma and PAW have to be per-
formed which require different radical diagnostic tools. It is very dif-
ficult to differentiate between the physical and chemical properties of
PAW responsible for microbial inactivation. The different oxidizers
formed in PAW, their respective effects and the mechanism of microbial
inactivation process is not known. The end reaction products formed in
the plasma vary with the carrier gas used for PAW generation. The use
of inert gases for the plasma generation increases the operating costs.
Some of the authors have reported that the exact source for the decrease
in pH and the role of acidic PAW on microbial inactivation is not clear.
Many investigations have not provided the link between the basics
properties of plasma and the molecular compounds formed in the PAW
for the same experimental study.
6. Future aspects
Future efforts should focus on the development of PAW applications
to meet the challenges to increase the food production and ensure food
safety. This requires understanding the underlying principles of PAW
generation and action of PAW at micro scale level. Identification of the
reaction intermediates and the end products determination after the
treatment is quite essential. The toxicity determination of different re-
action compounds provides a great means to convey a broad range of
29
Trends in Food Science & Technology 77 (2018) 21–31
relevant applications of PAW. The existence of complex plasma chem-
istry and formation of several ROS and RNS must be examined and
assessed carefully. The plant growth enhancement ability of PAW can
be exploited for hydroponic applications. From the regulatory point of
view, approval of PAW treatment from the different government reg-
ulatory agencies is required to treat it as generally regarded as safe
(GRAS) which is considered as the biggest hurdle for this process. The
success of this technology is dependent on its future scaling up and its
capacity to work continuously with the least possible maintenance.
7. Conclusion
The plasma discharge above the water surface and directly in water
proved to inactivate a wide range of microorganisms. It is clear from
several findings that the chemical and physical properties of PAW in-
duced the microbial inactivation. The fundamentals of the PAW prop-
erties and their actions against the inactivation were discussed. The
formation of ROS and RNS in PAW and their interactions with cellular
components like cell membrane and wall, nucleic acids and internal
proteins are responsible for the microbial cell inactivation. The physical
factors like shock waves, UV-radiation can disrupt the cell membranes
of microbes present during PAW generation. The PAW increases the
shelf-life and quality attributes of the fresh produce. Based on the in-
formation available, it is clear that PAW appears to be a powerful and
useful tool for the enhancement of seed germination and promote the
plant growth. The formation of nitrogen species like nitrates in PAW is
mainly responsible for the plant growth as it serves as the nutrient. The
PAW also has the ability to inhibit the hormones responsible for seed
dormancy and stimulate the growth. The overall effect of PAW shows
similar activity like cold plasma and its utilization in disinfection, de-
contamination, enhancing the seed germination and plant growth.
Thus, it can be concluded that PAW is an eco-friendly disinfectant so-
lution.
Funding
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
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