Received: 27/10/2024 Accepted: 10/01/2025 Published: 23/03/2025 1 of 7
https://doi.org/10.52973/rcfcv-e35548 RevistaCientíca,FCV-LUZ/Vol.XXXV
ABSTRACT
Klaxon pesticide represents a novel generation of insecticide
employed in the control of diseases, pests and weeds in select
agricultural regions. Pesticides that enter the aquatic environment
indirectly have a detrimental impact on the organisms that inhabit
this environment, and humans are ultimately exposed to these
chemicals through the food chain. The present study investigated
the toxicity of the klaxon pesticide in Dreissena polymorpha, a
suitable bioindicator of water pollution, through the analysis of
oxidative stress and metabolic biomarkers. The effects of klaxon
at concentrations of 0.01, 0.15 and 0.30 mg·L
-1
on oxidative stress
and antioxidant changes in D. polymorpha were determined over a
24 – and 96–hour period. Enzyme–linked immunosorbent assay
(ELISA) kits were employed to quantify the activities of superoxide
dismutase (SOD), glutathione peroxidase (GPx), catalase (CAT)
and thiobarbituric acid (TBARS), as well as to assess the levels
of reduced glutathione (GSH). ELISA kits were used to determine
results. Statistical evaluation of biomarker analyzes was performed
using the SPSS 24.0 package program one–way ANOVA (Duncan
0.05) test. Signicant decreases in GSH levels (P<0.05); signicant
increases in TBARS levels (P<0.05) were observed. Signicant
decreases (P<0.05) in SOD, CAT and GPx activities were observed.
Considering the study data, it was determined that the klaxon
pesticide penetrating the body of the living organism caused
oxidative stress and changes in enzyme activities in D. polymorpha.
Key words: Klaxon; Dreissena polymorpha; oxidative stress;
antioxidant response
RESUMEN
El pesticida Klaxon representa una nueva generación de insecticidas
empleados en el control de enfermedades, plagas y malezas en
regiones agrícolas seleccionadas. Los pesticidas que ingresan al
ambiente acuático indirectamente tienen un impacto perjudicial
en los organismos que habitan este ambiente, y los humanos
están nalmente expuestos a estos químicos a través de la cadena
alimentaria. El presente estudio investigó la toxicidad del pesticida
Klaxon en Dreissena polymorpha, un bioindicador adecuado de la
contaminación del agua, a través del análisis del estrés oxidativo
y biomarcadores metabólicos. Se determinaron los efectos del
klaxon en concentraciones de 0,01; 0,15 y 0,30mg·L
-1
sobre el
estrés oxidativo y los cambios antioxidantes en D. polymorpha
durante un período de 24 y 96 horas. Se emplearon kits de ensayo
inmunoabsorbente ligado a enzimas (ELISA) para cuanticar las
actividades de superóxido dismutasa (SOD), glutatión peroxidasa
(GPx), catalasa (CAT) y ácido tiobarbitúrico (TBARS), así como para
evaluar los niveles de glutatión reducido (GSH). Se utilizaron kits
ELISA para determinar los resultados. La evaluación estadística
de los análisis de biomarcadores se realizó utilizando la prueba
ANOVA unidireccional (Duncan 0,05) del paquete SPSS 24.0.
Se observaron disminuciones signicativas en los niveles de
GSH (P<0,05); aumentos signicativos en los niveles de TBARS
(P<0,05). Se observaron disminuciones signicativas (P<0,05) en
las actividades de SOD, CAT y GPx. Considerando los datos del
estudio, se determinó que el pesticida klaxon que penetró en el
cuerpo del organismo vivo causó estrés oxidativo y cambios en
las actividades enzimáticas en D. polymorpha.
Palabras clave: Klaxon; Dreissena polymorpha; estrés oxidativo;
respuesta antioxidante
The effect of the pesticide Klaxon on the oxidative stress and the
antioxidant responses of the Zebra mussel (Dreissena polymorpha)
El efecto del pesticida Klaxon sobre el estrés oxidativo y las respuestas
antioxidantes del mejillón cebra (Dreissena polymorpha)
Ebru Ifakat Ozcan
Munzur University, Faculty of Fisheries. Tunceli, Türkiye.
*Corresponding author: ebruozer@munzur.edu.tr
Used of Klaxon pesticide over Zebra mussel / Ozcan ___________________________________________________________________________________
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INTRODUCTION
Environment is the physical, chemical, biological, social,
economic and cultural context in which humans and other living
things relate and interact throughout their lives. Pollution affects
the entire ecosystem, including humans, and occurs mainly in
nature in the form of air, soil and water pollution. The processes
of industrialisation, technological development and population
growth are having a detrimental impact on the natural environment,
with pollution levels rising at an alarming rate. In both urban and
rural environments, contamination of air, soil and water—natural
assets—arises for a variety of reasons, affecting the survival of
flora and fauna and, through the food chain, human health [1].
Pesticides are dened as chemicals used during the production,
storage and consumption of agricultural products in order to
destroy insects, animals, microorganisms, weeds and other
harmful organisms that damage agricultural products or to
reduce that damage or have the potential to damage agricultural
products [2, 3]. Persistent pesticides, although they have a low
concentration in the water matrix, are more dangerous due to their
high stability and bioaccumulation properties. The main reason for
high bioaccumulation in aquatic organisms is the high solubility
of certain pesticide groups in water [4]. Klaxon 20 SC is a new
generation insecticide used against diseases, pests and weeds in
integrated control programs with 200 g·L-1 Chlorantraniliprole as
active ingredient. It is used for harmful organisms such as Cydia
pomonella, Leucoptera scitella, Lobesia botrana, Anarsia lineatella,
Cydia molesta, Agrotis ipsilon, Agrotis segetum, Sesamiaspp.,
Ostrinia nubilalis, Earias insulana, Spodoptera littoralis and
Helicoverpa armigera [5]. Concurrent with the rapid growth of the
global population, concerns about food security and malnutrition
have emerged as signicant challenges, particularly in developing
countries. This situation has brought along the necessity of using
agricultural areas in the most efcient way. In addition to the
use of new technologies in agriculture, another way to increase
yield is to protect plants from all kinds of pests that prevent the
development of plants and reduce their yield by using pesticides.
For this purpose, pesticides are widely used for preventive
purposes in the ght against pests in agricultural areas. The fact
that pesticides have high efcacy against harmful organisms, give
fast results, protect the product from toxin–secreting organisms
and are economical when used consciously and in a controlled
manner causes them to be widely used [6].
After pesticide practices, the pesticide mixtures used do not
remain in the plant, but mix into the soil and air. The spread of
pesticides in the aquatic ecosystem varies depending on the
environmental conditions, physical, chemical and formulation
structure of the pesticide. In addition, soil type, slope, vegetation
cover and rainfall also play a role in the contamination of water by
pesticides. This contamination can have an acute or chronic toxic
effect on aquatic organisms, negatively affecting their reproductive
abilities and causing a decrease in their populations [7]. Pesticides,
which degrade very slowly due to their molecular structure, can
reach harmful and even toxic values through biological and physical
accumulation even if they diluted to low concentrations in the
aquatic environment. Pesticides in water accumulate in the fat
tissues of living organisms and their concentrations always increase
when they pass to sh and birds feeding on them through the
food chain [8]. Even trace amounts of pesticide residues in water
can prevent the development of zooplankton and phytoplankton,
which are very important in the food chain of aquatic organisms [9].
Dreissena polymorpha is one of the most important invasive
species living in freshwater. They are both economically and
ecologically damaging as they cause corrosion, clog water lters,
restrict the lives of other living organisms, block water flow and
cause corrosion with the community they form in their environment.
However, the life tolerance of zebra mussels is quite high. They can
adapt to very low and very high temperatures, prolonged starvation,
different levels of dissolved oxygen and calcium [10, 11]. The
widespread and reliable use of these creatures in toxicological
studies can be attributed to their long life span, limited movement
and lter feeding. In addition, although it is known as an invasive
species, it is also suitable as a biological monitoring and model
species and is easily used in the investigation of anthropoenic
stress effects in aquatic environments [11, 12, 13].
This study will be an original study to determine the changes in
TBARS and GSH levels and SOD, CAT and GPx enzyme activities of
zebra mussels (Dreissena polymorpha) in Keban Dam Lake (Elazığ)
due to the use of the pesticide klaxon in agricultural spraying.
It is thought that the ndings of the research will direct on the
impact of agricultural activities, which are becoming more and
more widespread around our reservoir, and will make an important
contribution to future planning.
MATERIALS AND METHODS
Test organism
Zebra mussel (Dreissena polymorpha) is a reference species for
ecotoxicological studies in aquatic ecosystems [14]. These mussels
are mainly distributed in lakes and reservoirs in Turkey. As a species
that is not endangered and can encountered continuously in nature,
has stable behavior and sufcient body size, it is easier to sample
than other species [15, 16, 17] and has been preferred because it
is not selective in food intake [16]. D. polymorpha was collected by
hand from the cages of an aquaculture company in Keban Dam Lake
and brought to Munzur University Faculty of Fisheries in plastic box.
Adaptation of test organisms to the laboratory environment
D. polymorpha were brought to the laboratory alive and placed in
80×40×25 cm aquariums. A photoperiod (12 hours (h) of light and
12 h of dark illumination) was applied. Ambient temperature was
maintained at 18°C. Cultured plankton (Chlorella vulgaris + Navicula
cryptocephala) was given as D. polymorpha food. An external lter
and an air motor were used to ensure adequate oxygen supply in
the aquaria. During this adaptation process, the health status of the
organisms was observed and noted. Metric–meristic measurements
of the species were taken before starting the experimental study.
Organisms with similar size (W:1.01 ± 0.25 g, L:20.34 ± 2.04 mm,
h:9.80 ± 1.08 mm, w:10.10 ± 1.01 mm) and characteristics were
used to avoid misleading experimental results. Healthy individuals
that reacted to light and sound by closing their shells were selected.
Chemical
Klaxon 20 SC active ingredient pesticide used in the study was
purchased from Agrofarm Kimya Comp. registered trademark
Used of Klaxon pesticide over Zebra mussel / Ozcan ___________________________________________________________________________________ _________________________________________________________________________________________________Revista Cientica, FCV-LUZ / Vol.XXXV
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Suspension Concentrate (SC) 200 g·L
-1
Chlorantraniliprole
was purchased.
Determination of sublethal concentrations
To determine non–lethal concentrations, a comparison of the
concentrations obtained in practice with the values of the rates of
diffusion into the environment was taken into account.
Research design
Five healthy models of the same size were placed in separate 30 L
glass tanks. Air motors were installed to meet their oxygen needs. For
the experimental study, 4 groups were formed with 1 control group
(14 individuals were placed in each group, including replications).
Set to two time periods (24 or 96 h) in all four groups. Acute toxicity
tests were not performed considering the environmental effects of
xenobiotic substances such as pesticides. Sublethal concentrations
were determined by scanning the literature for experimental groups
and considering the concentration values used in toxicological
studies [18].
○Group A (Control); practice group: group without any klaxon.
○
Group B; was exposed to klaxon concentrations of 0.01 mg·L
-1
for 24 and 96 h.
○
Group C; was exposed to klaxon concentrations of 0.15 mg·L-1
for 24 and 96 h,
○
Group D; was exposed to klaxon concentrations of 0.30 mg·L
-1
for 24 and 96 h.
All stages in the experimental practices were performed in
three repetitions.
Biochemical evaluation
Three test organisms were randomly selected from the aquaria
and separated with a scalpel. The organisms were subjected to
cold shock treatment (ice water for 30 min), 0.5 g of sample was
taken from each organism to evaluate the antioxidant properties,
homogenized (Daihan brand, Hg-15D Digital ultraturax model,
Korea) and 1/5 w/v phosphate buffered saline solution (PBS buffer)
was added. After homogenization, the samples were centrifuged
(NUVE brand, NF1200R model centrifugal, Turkiye) at 17,000
rpm in a refrigerated centrifuge for 15 min, and the supernatants
were stored in the deep freezer (Daihan brand, Wisd ultra freezer
model, Korea) at -86°C until measurement was taken.
In this study, GSH and TBARS levels as well as SOD, CAT and GPx
activities were measured using an ELISA kit (Agilent brand, BioTek
800 TS Absorbance Reader, USA) for the biochemical response
of D. polymorha mussel individuals exposed to klaxon pesticide.
TBARS (Catalog No. 10009055), GSH (Catalog No. 703002), SOD
(Catalog No. 706002), CAT (Catalog No. 707002) and GPx (Catalog
No. 703102) levels in tissues were found with the kits bought from
CAYMAN Chemical Company.
Statistical analysis
Statistical evaluation of biomarker analyzes was performed using
the SPSS 24.0 package program one–way ANOVA (Duncan 0.05) test.
RESULTS AND DISCUSSION
Aquatic ecosystems can be contaminated with pesticides
through a variety of means, including overflows, agricultural
runoff, spray drifts, wastewater discharge, and seepage. Due to
the accumulation of toxic substances in various tissues and organs
of aquatic organisms, the concentration of pesticides in aquatic
organisms is several times higher than in the aquatic ecosystem
[19]. Aquatic ecosystems are adversely affected by high levels of
pesticide residues in water and sediments. This leads to signicant
loss of biodiversity [20].
TBARS level
The TBARS level increased with increasing concentration
compared to the control (A). While groups C and D showed a
statistically signicant (P<0.05) increase in both 24 and 96-h
practice groups compared to the control, the increase in group B
was found statistically insignicant (P>0.05) (FIG. 1).
Lipid peroxidation, which affects polyunsaturated fatty acids
(in membrane phospholipids), is a degenerative process that
results in the formation of toxic aldehydes. These react with
protein and non–protein substances to cause widespread
varies in cell membranes [21]. If antioxidant defences are
insufficient to neutralise excess ROS that may be generated
during biotransformation, end product of lipid peroxidation, MDA
(malondialdehyde) can ocur [22]. TBARSs are used to survey
lipid peroxidation produce body fluids, in cells and tissues [23].
24 h 96 h 24 h 96 h 24 h 96 h 24 h 96 h
A B C D
0
20
40
60
80
100
120
TBARS Level (µΜ)
e e de
cde
cd c
b
a
FIGURE 1. TBARS (µM) levels of Dreissena polymorpha exposed to different
concentration of klaxon. Dierent letters on the bars indicate a statistically
signicant dierence between the groups within same treatment period (P<0.05)
Used of Klaxon pesticide over Zebra mussel / Ozcan ___________________________________________________________________________________
4 of 7 5 of 7
A review of the literature reveals that various pesticide species
have been shown to induce alterations in TBARS levels in aquatic
organisms, thereby corroborating the ndings of this study. Ji et al.
[24] reported increases in TBARS levels in Carassius auratus as a
result of medium–time exposure to Benzo(k)fluoranthene (BkF)
alone and together PCB118 and dichlorodiphenyltrichloroethane
(DDT). Marins et al. [25] observed increases in TBARS levels
in Rhamdia quelen species exposed to imidacloprid (IMI) and
propoxur (PRO), an N–methylcarbamate compound. Nwani et al.
[26] reported that TBARS levels increased in Channa punctatus
individuals as a result of atrazine exposure. Sinhorin et al. [27]
reported increases in TBARS levels in Pseudoplatystoma sp. as a
result of glyphosate exposure. Rossi et al. [28] followed increase
in TBARS levels in Markiana nigripinnis and Astyanax lacustris
species with the effect of herbicide glyphosate (GLF), insecticide
bifenthrin (BFT), cyproconazole (CYP) mixtures and fungicides
azoxystrobin (AZ). Serdar et al. [21] observed increase in TBARS
levels in D. polymorpha with the impact of Dimethoate (DMT)
and Malathion (MLT) pesticides. Serdar [29] Dimethoate (DMT)
pesticide observed increases in TBARS levels in G. pulex. Serdar
et al. [30] determined increases in MDA levels in D. polymorpha
due to dimethoate (DM) induced toxicity. Söylemez et al. [31]
determined that beta–cyfluthrin (β–CF) produced increase in MDA
levels in D. polymorpha. Bhattacharyaetal. [32] determined that
sodium laureth sulfate (SLES) caused increases in MDA levels in
Tubifex tubifex. Increases in TBARS levels in D. polymorpha after
klaxon exposure are thought to be related to the concentration
and duration of exposure.
GSH level
GSH level decreased with increasing concentration compared
to control (A). Groups B, C and D showed a statistically signicant
(P<0.05) decrease in both 24 and 96–h practice groups compared
to the control (FIG. 2).
Oxidative stress can be caused by a decrease in cellular GSH
contents below a critical levels, which prevents xenobiotics
from conjugating such as klaxon to GSH and thus allows them
to freely associate covalently linked to cell proteins [33]. Ji et al.
[24] reported decrease in GSH levels in C. auratus as a result of
medium–term exposure to BKF alone and in combination with
PCB118 and DDT. Ferreira et al. [34] reported that sublethal
concentrations of tebuconazole (Teb), methyl parathion (MP)
and a glyphosate–based herbicide (Gly) decreased GSH levels in
R.quelen (Teleostei). Serdar et al. [21] observed decrease in GSH
levels in D. polymorpha with the impact of DMT and MLT pesticides.
Serdar [29] stated that DMT pesticide decreases caused in GSH
levels in G. pulex. Serdar et al. [30] reported decrease in GSH
levels in D. polymorpha due to DM–induced toxicity. Söylemez
et al. [31] reported that beta–cyfluthrin (β–CF) caused decrease
in GSH levels in D. polymorpha. In this study, decreases in GSH
levels were detected with claxone exposure, which is in parallel
with the studies in the literature.
SOD activity
SOD activity decreased as concentration increased compared to
control (A). While groups C and D showed a statistically signicant
(P<0.05) decrease in both 24 and 96–h practice groups compared
to control group, the decrease in group B was found statistically
insignicant (P>0.05) (FIG. 3).
Superoxide dismutase (SOD) is an important enzyme in the
antioxidant defense line and catalyzes the conversion of superoxide
anion to hydrogen peroxide [22]. It is thought that the decreases
in SOD activity in D. polymorpha at the end of klaxon exposure is
due to catalyzing the conversion of superoxide anion to hydrogen
peroxide. The results were tried to be supported by literature
studies showing similar results. Rossi et al. [28] observed decreases
24 h 96 h 24 h 96 h 24 h 96 h 24 h 96 h
A B C D
0.0
0.5
1.0
1.5
2.0
2.5
3.0
GSH Level (µΜ)
aa
b
b
b
bb
b
24 h 96 h 24 h 96 h 24 h 96 h 24 h 96 h
A B C D
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
4.0
4.5
5.0
SOD Activity (U·mL-1)
a a ab
ab
c
bc
bc
d
FIGURE 2. GSH (µM) levels of Dreissena polymorpha exposed to different
konsantrasyon of klaxon. Dierent letters on the bars indicate a statistically
signicant dierence between the groups within same treatment period (P<0.05)
FIGURE 3. SOD (U·ml-1) activities of Dreissena polymorpha exposed to dierent
concentration of klaxon. Dierent letters on the bars indicate a statistically
signicant dierence between the groups within same treatment period (P<0.05)
Used of Klaxon pesticide over Zebra mussel / Ozcan ___________________________________________________________________________________ _________________________________________________________________________________________________Revista Cientica, FCV-LUZ / Vol.XXXV
5 of 7
in SOD activities in M. nigripinnis and A. lacustris species with the
effect of GLF, BFT, AZ and CYP mixtures. Serdar et al. [21] observed
decrease in SOD activities in D. polimorpha with the effect of DMT
and MLT pesticides. Serdar [29] stated that DMT pesticide caused
decreases in SOD activities in G. pulex. Serdar et al. [30] reported
decreases in SOD activities in D. polymorpha due to DM–induced
toxicity. Cikcikoglu Yildirim et al. [35] observed that SOD activity
increased with the effect of ibuprofen (IBU) and propranolol (PRO)
using Gammarus pulex.
CAT activity
CAT activity decreased as concentration increased compared to
control (A). While the 24–hour practice groups in group D showed
a statistically signicant (P<0.05) decreases compared to the
control, the decreases in groups B and C was found statistically
insignicant (P>0.05) (FIG. 4). In the 96–hour practice groups,
statistically signicant decreases (P<0.05) were detected in all
groups compared to the control (A).
in C. punctatus individuals as a result of atrazine exposure. Rossi
et al. [28] observed decreases in CAT activities in M. nigripinnis
and A. lacustris species with the effect of GLF, BFT, AZ and CYP
mixtures. Serdar et al. [21] observed decreases in CAT activities in
D. polimorpha with the effect of DMT and MLT pesricides. Serdar
[29] stated that DMT pesticide caused decreases in CAT activities
in G. pulex. Serdar et al. [30] reported decreases in CAT activities
in D. polymorpha due to DM–induced toxicity. Aydın et al. [39]
reported decreases in CAT activities in D. polymorpha due to the
effect of Gamma Cyhalothrin (GCH) pesticide. CAT activity in D.
polymorpha individuals exposed to klaxon was signicantly lower
in all experimental groups compared to control group organisms.
This decrease is also supported by the literature.
GPx activity
GPx activity decreased as concentration increased compared
to control (A). Groups B, C and D showed a statistically signicant
(P<0.05) decrease in both 24 and 96 hour practice groups
compared to the control (FIG. 5).
Catalase catalyses the conversion of H
2
O
2
, produced during
various metabolic processes, into less toxic molecules of water and
oxygen [36, 37]. Concentration – and time–dependent decreases
in CAT activity were detected in D. polymorpha individuals
exposed to klaxon. In studies similar to these results, Marins
etal. [38] examined the effect of pesticides in different tissues of
Oreochromis niloticus and observed decreases in CAT activities.
Marins et al. [25] observed increases in TBARS levels in Rhamdia
quelen species exposed to imidacloprid (IMI) and propoxur (PRO),
an N–methylcarbamate compound. Marins etal. [25] observed
decreases in CAT activities in Rhamdia quelen species under
IMI and PRO exposure. Ferreira et al. [34] reported decreases
in GSH levels at sublethal concentrations of MP, Gly and Teb
pesticides. Nwani et al. [26] reported increases in CAT activities
GPx is a catalyst for the reduce of lipid peroxides and hydrogen
peroxide [40]. It has been shown that negative feedback caused
by excess substrate or damage from oxidative modification
reduces the activity of this enzyme. The inhibition of GPx activity
could reflect a failing antioxidant system in the presence of
plant protection products [41] or a direct effect of superoxide or
plant protection products on enzyme synthesis [42]. Serdar [29]
reported that DMT pesticide caused decreases in GPx activity
in G. pulex. Serdar et al. [30] reported decreases in GPx activity
in D. polymorpha due to DM–induced toxicity. Aydın et al. [39]
reported changes in GPx activity in D. polymorpha due to the
effect of Gamma Cyhalothrin (GCH) pesticide. GPx activity in D.
polymorpha individuals exposed to klaxon was signicantly lower
24 h 96 h 24 h 96 h 24 h 96 h 24 h 96 h
A B C D
0
50
100
150
200
250
300
CAT Activity (mol·min-1·mL-1)
a
a
abc
d
ab d
cd
bcd
24 h 96 h 24 h 96 h 24 h 96 h 24 h 96 h
A B C D
0
50
100
150
200
GPx Activity (mol·min-1·mL-1)
aa
bc
bc
cd
d
d
b
FIGURE 4. CAT (nmol·min-1·ml-1) activities of Dreissena polymorpha exposed to
dierent concentration of klaxon. Dierent letters on the bars indicate a statistically
signicant dierence between the groups within same treatment period (P<0.05).
FIGURE 5. GPx (nmol·min-1·ml-1) activities of Dreissena polymorpha exposed to
dierent doses of klaxon. Dierent letters on the bars indicate a statistically
signicant dierence between the groups within same treatment period (P<0.05)
Used of Klaxon pesticide over Zebra mussel / Ozcan ___________________________________________________________________________________
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in all experimental groups compared to control group organisms.
This decrease may indicate that hydroperoxide product synthesised
by lipid peroxidation exceeds the antioxidant capacity.
CONCLUSION
In this study, some antioxidant enzymes and various markers of
oxidative stress were evaluated and examined in D. polymorpha
exposed to the xenobiotic klaxon. Klaxon exposure caused changes
in the antioxidant defense system. In D. polymorpha, exposure
to sublethal concentrations of klaxon, an increases in TBARS
level, and decreases in GSH level, SOD, CAT, GPx activities were
observed. These biomarkers were determined to be effective
biomarkers in D. polymorpha with klaxon exposure.
Conflict of Interests
The author declare no competing interests
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