Title


Science and Technology Indonesia
e-ISSN:2580-4391 p-ISSN:2580-4405
Vol. 8, No. 1, January 2023

Research Paper

The Effects of Reactive Oxygen and Nitrogen Species (RONS) Produced by Surface
Dielectric Barrier Discharge (SDBD) Non-Thermal Plasma with Treatment Time and
Distance Variations to Kill Escherichia coli
Renaldo Apriandi Kasa1*, Unggul Pundjung Juswono2, Dionysius J. D. H. Santjojo2
1Master of Physics Study Program, Universitas Brawijaya, Malang, 65145, Indonesia2Departement of Physic, Universitas Brawijaya, Malang, 65145, Indonesia
*Corresponding author: randi−kasa@student.ub.ac.id

AbstractResearch on the inactivation of Escherichiacoli causing diarrheal disease using non-thermal plasma SDBD has been carried out. SDBDis a new technique for non-thermal plasma generation with several advantages: low power generation, comprehensive treatmentarea coverage, and reducing the potential effects of burning and drying tissue. This study aimed to analyze the effect of treatmenttime variations, namely 0 as control, 60, 75, 90, 105, and 120 seconds and treatment distance variations of 3, 6, 9, 12, and 15 mmof non-thermal plasma treatment of SDBD on E. coli. The results of the non-thermal plasma SDBD treatment with variations intime and distance showed that the longer the treatment time, the more bacterial cells died. Colony counts decreased to 4.33 x 107CFU/mL compared to the control, 409 x 107 CFU/mL, with a treatment time variation of 120 seconds, yielding the best treatmentresults. At the same time, the results of the treatment for variations in the non-thermal plasma distance of SDBD showed that thesmaller the treatment distance, the greater the bacterial death rate, with the best treatment results at a 3 mm treatment interval,with colony counts of 8 x 107 CFU/mL, compared to 409 x 107 CFU/mL in control. Based on these results, SDBD non-thermalplasma treatment can be used to inactivate or kill bacteria with effectiveness in killing bacteria depending on the length of treatmenttime and the distance of treatment.
KeywordsNon-thermal Plasma, SDBD, E. Coli, RONS, Treatment Time, Treatment Distance

Received: 18 September 2022, Accepted: 13 Desember 2022
https://doi.org/10.26554/sti.2023.8.1.45-51

1. INTRODUCTION

Infectious diseases are one of signicant health problems in
almost all developing countries, including Indonesia. One of
the most common infectious diseases is diarrhea. According to
Ragil and Dyah (2017), diarrhea is one of the leading causes
of illness and death in almost all geographic areas, and all age
groups can be aected. In Indonesia, diarrheal disease is a
potential endemic disease of Extraordinary Events (KLB), and
it is frequently fatal. According to Kemenkes RI (2018), the
number of suerers of diarrheal disease based on the results
of the diagnosis by health workers was 6.8%, while based on
the symptoms experienced, 8%. The number of patients with
diarrheal diseases classied according to age found that the
age group of 1 to 4 years had the highest number of suerers,
namely 11.5%. In addition, the age group of 75 years and over
has a relatively high number of suerers, namely 7.2% (Prab-
hakara, 2010). Microorganisms that generally cause disease
are called pathogens. Pathogens include bacteria, protozoa,

viruses, prions, fungi, and worms. These pathogens can cause
various symptoms and diseases, including diarrhea (Levy et al.,
2018). Pathogens that cause diarrheal disease can come from
viruses, for example, Rotavirus (40-60%), Escherichia coli (20-
30%), Shigella sp. (1-2%), and the parasite Entamoeba histolytica
(Ragil and Dyah, 2017).

Several conventional sterilization techniques have been de-
veloped to inactivate disease-causing microorganisms, such
as sterilization using dry heat (oven), moist heat (autoclaving),
and chemicals such as glutaraldehyde and the use of gamma
irradiation (Moisan et al., 2001; Morent and De Geyter, 2011;
Park et al., 2003). This conventional technique that has been
used has several disadvantages, such as high processing temper-
atures, long sterilization times, and the use of toxic chemicals,
resulting in changes to the material during sterilization, and
this technique is quite expensive to use (Moisan et al., 2001;
Morent and De Geyter, 2011). Based on the limitations of con-
ventional methods, it is necessary to have a new and alternative

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Kasa et. al. Science and Technology Indonesia, 8 (2023) 45-51

sterilization method, namely pretreatment with non-thermal
plasma (plasma sterilization) (Hati et al., 2012).

Plasma is the fourth matter after solids, liquids, and gases.
Plasma is dened as an ionized gas of free particles (Putra et al.,
2021; Scholtz et al., 2021; Šimončicová et al., 2019). Based
on the temperature, plasma is divided into thermal plasma
and non-thermal plasma (Morent and De Geyter, 2011). Cold
or non-thermal plasma is produced by applying an electric or
electromagnetic eld to a gas. Plasma contains excited states
of molecules and atoms, cations and anions, free radicals, elec-
trons, UV radiation, ozone, superoxide, hydroxyl radicals, sin-
gleoxygen, atomicoxygen, nitrogenoxides, ornitrogen dioxide
(Puligundla and Mok, 2017; Zheng et al., 2016). These species
exhibit antimicrobial activity against various microorganisms,
including bacteria, yeasts, and even bacterial and fungal spores
(López et al., 2019).

Surface dielectric barrier discharge is a new technique for
non-thermal plasma generation with several advantages: low
powergeneration, comprehensive treatment area coverage, and
reducing the potential eects of burning and drying tissue. Sev-
eral non-thermal plasma sterilization techniques have been
carried out, but further research is needed to optimize non-
thermal plasma techniques. Therefore, this study aimed to an-
alyze the eect of treatment time and distance of non-thermal
SDBD plasma treatment on E. coli.

2. EXPERIMENTAL SECTION

2.1 Materials
The non-thermal plasma system used in this study is a sur-
face dielectric barrier discharge. The non-thermal plasma of
the surface dielectric barrier discharge is generated using a 20
V DC voltage source which is then transformed into a high
voltage source to create the plasma. The scheme used in this
study is shown in Figure 1. The plasma non-thermal discharge
surface dielectric barrier uses two copper electrodes. A dielec-
tric separates two copper electrodes. The two electrodes are
connected to a voltage source, with one electrode connected to
the ground and the other connected to a high-voltage source.
The sample used in this study was E. coli obtained from the
microbiology laboratory, Faculty of Medicine, Brawijaya Uni-
versity. In addition, some materials, namelynutrient agar (NA),
are used as media for bacterial growth and sterile physiological
NaCl for dilution.

2.2 Methods
2.2.1 E. coli Sample Preparation and SDBD Non-thermal

Plasma Treatment
E. coli isolates that had been incubated for 24 hours were di-
luted with serial dilutions up to 10−6 with one loop of bacterial
isolates homogenized with 9 mL of sterile physiological NaCl
(10−1 dilution).1 mL of the 10−1 dilution of bacterial suspen-
sion was homogenized with 9 mL of sterile physiological NaCl
(10−2 dilution). This step was carried out until a dilution of
10−6. The results of the dilution were then treated using non-
thermal plasma with the surface dielectric barrier discharge

Figure 1. Schematic of SDBD Non-thermal Plasma

with variations in treatment time (0 as control, 60, 75, 90, 105,
120 seconds) and treatment distance (3 mm, 6 mm, 9 mm, 12
mm, 15 mm). The results of the treatment were then spidered
using a triangular rod. After that, it was incubated at 37°C
for 24 hours by placing the petri dish in an inverted position.
The next step was to count the number of colonies in each
treatment. Each experiment was repeated three times.

2.2.2 Optical Emission Spectroscopy
Optical emission spectroscopy (OES) was used to characterize
reactive plasma species and to analyze plasma composition,
which can explain the relationship or mechanism between re-
active spaces formed in plasma and the ability to inactivate
bacteria (Wiegand et al., 2014). The optical emission spec-
trum was measured using Aurora 4000 at a wavelength of 200
to 900 nm with an integration time of 5000 ms and 3 repe-
titions of the spectrum capture and then averaged to obtain
the optical emission spectrum from the plasma. The emission
spectrumobtainedwas thenanalyzedqualitativelytodetermine
the chemical species at each wavelength peak. The results of
identifying the wavelength peaks were then analyzed using the
National Institute of Standards and Technology atomic spec-
trum database and previous journal publications to identify
chemically active species (Sarangapani et al., 2016).

2.2.3 Data Analysis
The data obtained were based on the eect of treatment time
(0, 60, 75, 90, 105, 120 seconds) and treatment distance (3,
6, 9, 12, 15 mm) on the number of bacteria, tabulated and
analyzed using ANOVA using SPSS software. 26. If p-value <
0.05 H0 was accepted, then the length of treatment time and
treatment distance aect the number of bacteria.

3. RESULT AND DISCUSSION

3.1 Optical Emission Spectroscopy of SDBD Non-thermal
Plasma

An optical emission spectrum (OES) can measure and analyze
reactive species produced by non-thermal plasma. The spec-
trum results obtained can be analyzed for reactive species by
looking at the spectrum peaks. In the following section, Fig-

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Kasa et. al. Science and Technology Indonesia, 8 (2023) 45-51

Figure 2. OES Spectrum of SDBD Non-thermal Plasma with
Treatment Time Variation and Treatment Distance Variation

ure 2 depicts the spectrum obtained from a surface discharge
dielectric barrier non-thermal plasma.

Spectrum results were obtained using OES for each vari-
ation of treatment time and distance. The time variation is
taken every 60 seconds, 90 seconds, and 120 seconds, while
the distance variation is taken every 3 mm. 6mm, and 9mm.
The spectrum results with time variations show the increasing
intensity with longer treatment time. In contrast, for variations
in the distance, the intensity will be smaller if the distance from
the plasma source is further away.

The resulting spectrum was measured using OES at a wave-
length of 200 to 900 nm from the plasma source. The intensity
emitted from the plasma source is recorded at each wavelength.
In the formation of plasma, various chemical species are in an
excited state. The chemical species produced in the gas phase
were observed using OES during plasma release (Sarangapani
et al., 2016). In the UV region, the emission spectrum shows
that N2 and N2+ excitation species’ emission shows dierent
peaks. A small peaks of OH appear at wavelengths 296,1 nm
(Adhikari et al., 2021; Dhungana et al., 2020; Hosseini et al.,
2018; Naz et al., 2021; Sarangapani et al., 2016). The low
intensity of singlet oxygen is at a wavelength of 777.5 nm
(Sarangapani et al., 2016). At the same time, the N2 Second
Positive System (SPS) has a prominent peak at a wavelength of
313-390 nm, N2 rst negative system (FNS) at a wavelength of
390-450 nm (Akter et al., 2020; Misra et al., 2015). From the
reactive species produced in the gas phase plasma, long-lived or
short-lived reactive species such as hydrogen peroxide (H2O2)
and ozone (O3) are formed as long-lived reactive species, and
short-lived reactive species such as hydroxyl radicals (•OH),
singlet oxygen (1O2), superoxide anion (O2−), atomic oxygen
(O), nitrite oxide (NO), and peroxynitrite (ONOO−), all of

these reactive species exhibit antimicrobial activity (Xu et al.,
2018).

3.2 Eect of Treatment Time and Distance of SBDB Non-
thermal Plasma Teatment on the Number of Colonies

Non-thermal plasma can decontaminate bacteria. The mecha-
nism and level of decontamination capability vary depending
on the length of treatment time, the distance of treatment, the
amount of voltage used, and the source of the gas used. All
play a role in how eective non-thermal plasma is at decontam-
inating bacteria (Amalda et al., 2020). In research on bacterial
inactivation using SDBD non-thermal plasma treatment, vari-
ations in treatment time and treatment distances were used.
For the treatment time, variations in treatment time were used,
namely 60 s, 75 s, 90 s, 105 s, and 120 s. Various treatment
distances were also used, namely 3 mm, 6 mm, 9 mm, 12 mm,
and 15 mm. From the results of the treatment obtained, it can
be seen in Table 1 and Table 2 that non-thermal plasma inu-
ences bacterial inactivation for variations in treatment time and
variations in treatment distance. The longer the treatment time,
the more bacteria are inactivated, or the number of inactivated
bacteria is directly proportional to the length of treatment time.
The eect of treatment time on colony number can be seen in
Figure 3. Meanwhile, treatment results with distance variations
and SBDB non-thermal plasma still aect the inactivation of
bacteria. The smaller the distance of treatment used for treat-
ment, the more bacteria will die, or the ability of the bacteria
to live will be smaller. The eect of treatment distance on the
number of colonies can be seen in Figure 5.

The results of the treatment showed that the treatment
time of 120 seconds had a better ability to inactivate or kill
bacteria than other treatments. The number of bacteria that
grewafterbeing treated for120 seconds was an average of 4.3 x
107 CFU/mL. This number was much lower than the number
of bacteria that grew without non-thermal plasma treatment,
whichwas409x107 CFU/mL.While fortheshorter treatment
time, the number of colonies that grew more and more was
105 s, 90 s, 75s, and 60 s, with the average number of colonies
growing was 11 x 107 CFU/mL, 13 x 107 CFU/mL, 46.33 x
107 CFU/mL, 56 x 107 CFU/mL. Pictures of the number of
colonies before (control) and after treatment with treatment
time variations can be seen in Figure 4.

Meanwhile, from the results of the variation in treatment
distance, 3 mm has a more extraordinary ability to inactivate
bacteria than other treatment distances. The number of bac-
teria that grew after being treated at 3 mm averaged 8 x 107

CFU/mL. This number is much decreased compared to the
number of bacteria that grow when the treatment is carried
out at a longer distance. At the furthest distance carried out in
this study, which was 15 mm, the number of colonies growing
on average was 253 x 107 CFU/mL. At the same time, the
number of bacterial colonies in the control treatment was 409
x 107 CFU/mL. Images of colony count before (control) and
after treatment with treatment distance variations can be seen
in Figure 6.

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Kasa et. al. Science and Technology Indonesia, 8 (2023) 45-51

Table 1. Number of Colonies Before (Control) and After the Treatment with Treatment Time Variations (P < 0.05)

Time (Second) Distance (mm)
Number of Colonies (x 107 CFU/mL)

Treatment I Treatment II Treatment III

Control 410 418 399
60 3 54 46 68
75 3 60 43 36
90 3 13 15 11
105 3 7 3 23
120 3 4 3 6

Figure 3. Graph of the Number of Colonies Before (Control)
and After Treatment with Treatment Time Variations (60 s,
75 s, 90 s, 105 s, 120 s) (R2 = 0.98188)

The treatment of time variation and distance variation
shows that there is an eect of non-thermal plasma treatment
of SDBD. This eect is due to the reactive species formed
during plasma generation. The RONS formed to have an im-
portant role in the inactivation of bacteria. RONS can disrupt
the bonding of microbial cell structures with lipid peroxidation,
damaging the RONS membrane as reactive free radicals (NO,
•OH, and superoxide) or strong oxidizing agents (H2O2 and
O3) can penetrate microorganisms. Furtherchemical reactions
can occur in the cytoplasm that can oxidize cellular proteins or
microbial DNA (Klämp et al., 2012).

One of the molecules that are the main agent of bacterial
inactivation is NO (Nitrogen Oxide). NO can destroy cells by
dimerizing thymine bases on DNA strands, disrupting DNA
replication (Amalda et al., 2020; Tian et al., 2010). Besides
NO, the reactive species formed during plasma formation is
H2O2 which has the potential to cause oxidative damage. Be-
sidesbeingable tocauseoxidativedamage,H2O2 alsofunctions
as a more potent hydroxyl radical (•OH) precursor. The •OH
radical is a reactive oxygen species with excellent reactive abil-

Figure 4. Picture of the Number of Colonies Before (Control)
and After Treatment with Treatment Time Variations

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Kasa et. al. Science and Technology Indonesia, 8 (2023) 45-51

Table 2. Number of Colonies Before (Control) and After the Treatment with Treatment Distance Variations (P < 0.05)

Time (Second) Distance (mm)
Number of Colonies (x 107 CFU/mL)

Treatment I Treatment II Treatment III

Control 410 418 399
120 3 10 6 8
120 6 12 13 14
120 9 49 70 85
120 12 137 109 224
120 15 284 242 233

Figure 5. Graph of the Number of Colonies Before (Control)
and After Treatment with Treatment Distance Variations (3
mm, 6 mm, 9 mm, 12 mm, 15 mm) (R2 = 0.99727)

ity and can produce oxidative damage to cell components (Pai
etal.,2018). The•OHradical is a strongoxidant thatcancause
a decrease in ATP, thereby causing low energy in cells. The
•OH radical can also break the phosphodiester bond of DNA
molecules, which causes DNA fragmentation, and can become
lipids in cell membranes, resulting in cells being unable to repli-
cate or causing cell death (Feng and Wang, 2020). In addition,
another strong oxidizing agent plays a role in the inactivation
of bacteria, namely ozone (O3). Ozone has a considerable ox-
idation potential, which can damage cell walls and bacterial
cytoplasmic membranes, increasing membrane permeability.
As a result, there is a decrease in surface tension which results
in cell leakage. Furthermore, ozone and other reactive species
easily enter the cell and damage bacterial nucleic acids, damag-
ing the pyramidal rings and breaking the bonds between the
pyramidal rings and the sugar groups in nucleic acids. This nu-
cleic acid damage will result in cell death (Kristanti and Dessy,
2012).

The concentration of reactive species formed during non-
thermal plasma treatment signicantly aects the sterilization

Figure 6. Picture of the Number of Colonies Before (Control)
and After Treatment with Treatment Distance Variations

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Kasa et. al. Science and Technology Indonesia, 8 (2023) 45-51

ecacy. The longer the treatment time, the more reactive the
plasma species contains and the more eective it is in killing
bacteria. Similarly, the variation in treatment distance showed
a relationship between the ability of bacteria to survive and
the number of reactive species produced during plasma treat-
ment. The results of the OES spectrum in Figure 3. show that
the farther the treatment distance, the smaller the intensity of
the spectrum, which indicates that the fewer reactive species
formed, the lower the ability to kill bacteria.

4. CONCLUSION

The results of research that have been carried out on the eect
of RONS produced by SDBD non-thermal plasma to kill Es-
cherichia coli show that the time and distance of treatment aect
the numberof colonies that live before and after treatment. For
variations in treatment time, the longer the treatment time, the
more bacteria are inactivated, or the more bacteria die where
the numberof colonies that growwhen treated with a treatment
time of 120 s, which is 4.3 x 107 CFU/mL, is much lower than
the control, which is 409 x 107 CFU/mL. As for variations
in treatment distance, the farther the treatment distance, the
more the number of colonies that live, where the number of
colonies that grow when treated with 15 mm, namely 253 x
107 CFU/mL, signicantly decreased when treated with 3 mm,
namely 8 x 107 CFU/mL. Based on these results, further re-
search can be investigated more deeply by looking at the eect
of non-thermal plasma treatment on DNA, lipids, proteins,
and bacterial cell morphology to determine the mechanism of
non-thermal plasma treatment that kills bacteria. Additionally,
several variations of parameters, such as gas source and volt-
age, can be carried out in order to obtain the most eective
non-thermal plasma composition.

5. ACKNOWLEDGMENT

The author would like to thank Lembaga Pengelola Dana Pen-
didikan (LPDP), which has funded this research, and all parties
who have helped and been involved in completing this research.

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	INTRODUCTION
	EXPERIMENTAL SECTION
	Materials
	Methods
	E. coli Sample Preparation and SDBD Non-thermal Plasma Treatment 
	Optical Emission Spectroscopy
	Data Analysis


	RESULT AND DISCUSSION
	Optical Emission Spectroscopy of SDBD Non-thermal Plasma
	Effect of Treatment Time and Distance of SBDB Non-thermal Plasma Teatment on the Number of Colonies

	CONCLUSION
	ACKNOWLEDGMENT