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Evaluation of Antibacterial and Antioxidant Properties of Urtica urens

Extract Tested by Experimental Animals

Article in International Journal of Pharmacology · March 2017

DOI: 10.3923/ijp.2017.332.339

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 OPEN ACCESS International Journal of Pharmacology

ISSN 1811-7775
DOI: 10.3923/ijp.2017.332.339

Review Article
Evaluation of Antibacterial and Antioxidant Properties of
Urtica urens Extract Tested by Experimental Animals
1
Taha Barkaoui, 1Raoudha Kacem, 1Fatma Guesmi, 2Ahlem Blell and 1Ahmed Landoulsi

1
Laboratory of Biochemistry and Molecular Biology, Faculty of Science of Bizerta, Bizerta, Tunisia
2
Pathological Anatomy Service, Regional Hospital of Menzel Bourguiba, Republic of Tunisia

Abstract
Background and Objective: Many plant extract have been reported to have an antimicrobial and antioxidative activities, for instance,
Salmonella typhimurium, recognized as the main causes of food contaminations and may induce various human infections. In addition,
hydrogen peroxide (H2O2) induced reactive oxygen species and the absence of their scavenge systems in cells leads to oxidative stress.
The present study is focused on an essay to determine the antimicrobial and antioxidant properties of aqueous extract of Urtica urens.
Materials and Methods: The antibacterial activity was tested in albino rats as a model using S. typhimurium infection. Mice were initially
infected by S. typhimurium and then treated with Urtica urens-extract. Oxidative stress was induced in male Wistar rats by a single
intraperitoneal injection of 1 mM of H2O2. Results: The extract (3 mg kgG1 b.wt.) treated animals was found to have significant effects on
mortality and the numbers of viable S. typhimurium recovered from feces. The extract was fed to albino rats, followed by H2O2.
Biochemical evaluation of the treatment has been tested at different enzymatic levels, such as glutathione (GSH), superoxide dismutase
(SOD) and lipid peroxidation (MDA). The antioxidant assay showed a significant decrease of the MDA level and increase in the GSH and
SOD. Although, clinical signs and histological damage were rarely observed in the treated mice, the controls showed a signs of lethargy
and histological damage in the liver, spleen and intestine. Conclusions: Urtica urens-extract has the potential to provide an effective
treatment for salmonellosis and oxidative stress.

Key words: Urtica urens-extract, antibacterial and antioxidant activities, lipid peroxidation, SOD, GSH

Received: January 31, 2016 Accepted: November 04, 2016 Published: March 15, 2017

Citation: Taha Barkaoui, Raoudha Kacem, Fatma Guesmi, Ahlem Blell and Ahmed Landoulsi, 2017. Evaluation of antibacterial and antioxidant properties
of Urtica urens extract tested by experimental animals. Int. J. Pharmacol., 13: 332-339.

Corresponding Author: Taha Barkaoui, Laboratory of Biochemistry and Molecular Biology, Faculty of Science of Bizerta, 7021 Zarzouna, Tunisia
Tel: +21697736328

Copyright: © 2017 Taha Barkaoui et al. This is an open access article distributed under the terms of the creative commons attribution License, which
permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.

Competing Interest: The authors have declared that no competing interest exists.

Data Availability: All relevant data are within the paper and its supporting information files.
 Int. J. Pharmacol., 13 (3): 332-339, 2017

INTRODUCTION Preparation of crude plant extracts: For aqueous extraction,

10 g of air-dried powder was boiled on slow heat in distilled
Primary civilizations have used medicinal plants as the water for 30 min. The extract then filtered using Whatman
1
ultimate source of therapeutic aids . In spite of the huge filter paper No. 1 and centrifuged at 5000×g for 10 min as
synthetic products into modern medicine, almost half of them discussed by Folcara et al.12. The extract supernatant was
are directly obtained from plants, many plants exhibit a collected each 30 min and concentrated to a final volume
unique complex combination of secondary metabolites which equal to one fourth of the original one. The final solution was
give an effective effect in therapy process for instance, used to perform antibacterial and antioxidant activities.
caffeoylmalic acid, organic acid, chlorogenic acid, flavonoids, Finally, the supernatant was recovered and stored at -4EC
2
coumarins, steroids and scopoletin . Moreover, aerial parts of until it is used.
plants are rich in inorganic minerals and vitamins etc. Which
have significant antioxidant and antibacterial properties3,4. Determination of in vivo antibacterial activity
Many modern drugs which have contributed well in medical Animal: Eighteen male Wistar rats (50-70 g) aged between
interventions were based or extracted from medicinal plants. 8 and 10 weeks mice were purchased from the Pasteur
Adequate drugs include the curare alkaloids, penicillin and Institute (Tunisia) to perform all in vivo experiments. They
other antibiotics, cortisone, reserpine, podophyllotoxin and were kept in a temperature-controlled room under a 12 h light
other therapeutic agents5. 12 h dark cycle. Animals had free access to commercial solid
Urtica urens (UU), which belongs to the family of food and water ad libitum and were acclimatized for at least
Urticaceae and commonly known as nettle apple has been 1 week prior to beginning the experiments. All mice
used extensively as a traditional medicine in many countries6 experiments in this study were approved by the Bizerte
for the treatment of anemia, rheumatism and arthritis, eczema, University Animal Ethics Committee in accordance with the
asthma, urinary gravel, stomach complaints, skin infections guidelines of the Tunisia Council on Animal Care.
and as an anti-haemorrhagic 7.
Furthermore, Urtica urens is reported by an antioxidant Preparation of bacteria: Salmonella typhimurium (ATCC
and antibacterial effects8,9. The constituents of UU include 14028) was used in this study. This strain was purchased from
caffeoylmalic acid, flavonoids, chlorogenic acid, gallic acid and Institute Pasteur Tunis, stored at -80EC in glycerol stocks and
caffeic acid which are well known for their therapeutic used as required during different experiments.
properties2,10. The main medicinal uses of nettles historically
were internally as a tonic and highly nutrient food11. However, In vivo assay using mice: Mice were divided into the
till the date, no studies regarding the antimicrobial and following groups: Control (CON), Salmonella-infected (SI) and
antioxidant activity of Urtica urens have been conducted. Salmonella-infected+UU-extract (SIUU). Each group contained
Therefore, the objective of the present study was to determine six mice. The growth inhibition of the test organisms in mice
the protective effect of feeding the aqueous extract of was then determined by monitoring S. typhimurium in the
U. urens to albino rats of the Wistar strain against feces of the mice. Briefly, S. typhimurium was grown
S. typhimurium and the toxic effects of H2O2 by biochemical overnight in Luria‒Bertani broth (Difco), centrifuged, washed
and histopathological methods. in phosphate-buffered saline (PBS) and then diluted into
20% sucrose solution to achieve a final concentration of
MATERIALS AND METHODS 1×105 CFU mLG1. The SI and SIUU groups were then
inoculated using gavage needle orally with 0.1 mL of already
Plant material: Urtica urens is a perennial plant with stinging prepared bacterial suspension. Each day, 1 h after infection,
hairs belonging to the family Urticaceae, under the division 2 mL of UU aqueous extract were orally administered to all
Spermatophyta, subdivision of Angiospermae, class animals of the SIUU group (using gavage needle), whereas
Dicotyledonae, group Apetalae, order Urticales. Urtica urens CON and SI animals were not. Fecal samples were then
were collected from the Bizerta region of Tunisia on April, 2014 collected at 0, 1, 2, 3, 4, 5, 6 and 7 days after the bacterial
(South Mediterrranean). The botanical identification of suspensions were administered and the numbers of the
U. urens was carried out by Professor Ben Nasri-Ayachi, bacteria per gram of feces were determined. Aliquots (100 µL)
Sciences Faculty of Tunisia. of fecal suspensions were serially diluted in PBS and then

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 Int. J. Pharmacol., 13 (3): 332-339, 2017

plated on duplicate Salmonella-Shigella agar plates (Difco), Lowry et al.19. Measurements of glutathione were performed
which were subsequently incubated overnight at 37EC. Typical according to the method of Ellman20 and superoxide
colonies were counted using the method of Lee et al. 13
on dismutase concentration was determined according to the
plates that contained between 30 and 300 colonies, after method of Marklund21, using a teflon tissue homogenizer.
which confirmation of S. typhimurium was performed by a
PCR assay using a previously described method14. At day 4 Tissue processing: Liver, spleen and intestine were flushed
post-infection, the mice were sacrificed and tissue specimens with chilled 1.15% (w/v) KCl solution. A 10% (w/v)
of the liver, spleen and intestine organs were transferred homogenate was prepared in 50 mM phosphate buffer,
to 10% buffered neutral formalin for histopathologic pH 7.4 and centrifuged at 8000×g for 15 min at 4EC.
examinations and then processed using standard procedures. Experiment were carried out according to the method
Sections of paraffin-embedded tissues were then stained with described by Sen et al.22. The supernatant so obtained were
hematoxylin and eosin. used for the estimation of lipid peroxidation (MDA),
glutathione (GSH) and superoxide dismutase (SOD). The
Determination of in vivo antioxidant activity protein content was determined by the method of
Experimental procedure: Hydrogen peroxide (H2O2) is a Lowry et al.19, using bovine serum albumin as the standard.
selectively toxic chemical agent. The H2O2 induced Reactive
Oxygen Species (ROS) and/or a decrease the antioxidant Statistical analysis: The results are expressed as Mean±SD of
15
defense mechanisms . The ROS include free radicals. at least three sets of triplicate determinations for each data
However, the increase in ROS and free radicals secretion point. One-way ANOVA, Tukey and Dunnett tests were applied
was revealed to be an important cause among different for analyzing the significance of difference between and
biochemical manifestations in various diseases 16. among different groups.
Stress was induced in male Wistar rats (50-70 g) by a
single intraperitoneal injection according to Donnini et al.17 of RESULTS
hydrogen peroxide (H2O2) at a dose of 1 mmol LG1 in 0.5 mL
PBS. The animals were grouped into three groups containing In vivo antibacterial activity: The in vivo antibacterial
six animals in each group. The first group served as control, activity of UU-extract was examined using a mouse
the second group was administered H2O2 by intraperitoneal S. typhimurium infection model. Briefly, mice were infected
injection (negative control). The animals of the 2nd and with 1×105 CFU of S. typhimurium SI, 1 h late.
3rd groups were given dose of H2O2 at 1 mmol LG1 until the The UU-extract was orally administered to the mice.
14th day and the 3rd group was administered the aqueous Table 1 shows that treatment with the extract of UU was
extract of UU via oral route at 3-5 mg kgG1 b.wt., for 14 days. found to have marked effects on mortality and on the number
The dose was selected on the basis of the LD50 at the of viable S. typhimurium recovered from feces. At day 1
equivalent of up to 2 g dried drug kgG1 b.wt.3. Some of rats in post-infection, 10 mice in the SI and SIUU group did not shed
first group were treated with physiological saline, daily for viable S. typhimurium in feces, whereas the feces of mice in
14 days. They were housed at University Animal House in the SI group being found to contain bacteria at a
standard conditions and fed with standard diet with water concentration of 1×102 to 2×103 CFU gG1 and feces of mice
ad libitum. At the end of experimental period, animals were in the SIUU group being found to contain bacteria at a
sacrificed and the liver, spleen and small intestine were concentration of 0-4.3×103 CFU gG1. In addition, at day 6
isolated to prepare homogenate. post-injection, one of the mice in the SIUU group had died,
while all six mice in the SI group had succumbed.
Markers of oxidative stress: Animals were sacrificed and
tissue was collected and then washed with ice-cold saline, Organ histopathologic changes: Salmonella typhimurium
weighed and minced, 10% homogenate was prepared in infected mice that did not receive the UU-extract were
0.15 M ice-cold KCl for TBARS (thiobarbituric acid-reactive showed signs of histological damage in the liver, spleen and
substances), a marker for lipid peroxidation was estimated intestine. The central veins of the liver showed congestion
with the method of Ohkawa et al.18 and protein was with focal necrotic emboli-like materials. In spleen, an
determined according to the method reported by extensive hemorrhagic necrosis was detected in the red pulp

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 Int. J. Pharmacol., 13 (3): 332-339, 2017

Table 1: Effects of treatment with UU-extract on fecal shedding of S. typhimurium (CFU gG1) by mice
Day of post-feeding
------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------
Groups 0 1 2 3 4 5 6 7
SI1 0 1.8×103 8.9×106 2.5×107 3.7×107 4.7×107 Death Death
SI2 0 2.4×103 1.5×104 1.6×106 2.6×105 1.2×106 8.6×106 Death
2 5 6 6 7
SI3 0 1.2×10 4.8×10 2.6×10 3.6×10 1.9×10 Death Death
SI4 0 1.3×103 6.4×105 3.2×107 Death Death Death Death
SI5 0 1.38×103 1.9×104 5.8×106 3.26×107 Death Death Death
SI6 0 1.7×103 5.2×104 1×104 1.8×105 2.8×105 3.2×106 Death
SIUU1 0 0 0 2.6×102 6×105 3×103 7×102 1.7×102
SIUU2 0 1.4×102 5.2×103 9.8×103 2.4×103 2.8×102 1×102 0
SIUU3 0 0 2×103 8×103 3×103 6×102 3×102 2×102
SIUU4 0 1×103 2.3×103 5.3×103 4.6×104 2.3×103 9.4×102 1.4×102
3 4 6 6 7 8
SIUU5 0 4.3×10 2.9×10 1.3×10 6.5×10 2.3×10 1.8×10 Death
SIUU6 0 0 3.2×103 1×104 1.9×104 1.4×103 3.2×103 1.2×102
SI: Salmonella-infected, SIUU: Salmonella-infected+UU

Table 2: Level of MDA in liver, spleen and small intestine of control and experimental animals in each group
TBARS (nmol gG1 tissue)
--------------------------------------------------------------------------------------------------------------------
Parameters Liver Spleen Small intestine
Group I: Control rats 51.23±4.9 8.34±0.91 17.19±2.68
Group II: Rats intoxicate with H2O2 123.32±11.5*** 17.31±0.80*** 28.76±4.93***
Group III: Rats intoxicate then treated with aqueous extract(UU) 55.45±5.51 10.32±2.30 14.42±2.30
Values are expressed as Mean±SD (n = 6). ***Significantly different from control at p<0.001

Table 3: Level of GSH in liver, spleen and small intestine of control and experimental animals in each group
GSH (µmol gG1 tissue)
---------------------------------------------------------------------------------------------------------------
Parameters Liver Spleen Small intestine
Group I: Control rats 42.66±2.86 21.63±2.32 43.23±2.65
Group II: Rats intoxicate with H2O2 12.22±1.46*** 7.32±0.72*** 16.74±1.14***
Group III: Rats intoxicate then treated with aqueous extract (UU) 31.99±4.42 18.23±2.84 40.83±2.44
Values are expressed as Mean±SD (n = 6), ***Significantly different from control at p<0.001

with multiple apoptotic bodies in the white pulp. In addition, may induce the protection against the H2O2 induced oxidative
destruction and atrophy with ischemic necrosis and stress by reducing the lipid peroxidation.
edematous changes with polymorphonuclear leukocyte
infiltration within the mucosal layers of the small intestine Effect of UU-extract on GSH status: Table 3 shows the level of
were evident. In contrast, clinical signs and histological non-enzymic antioxidant (GSH) in liver, spleen and small
damage were rarely observed in S. typhimurium-infected intestine of control as well as treated animals. The GSH status
mice fed the extract of UU-extract (Fig. 1). was found to be significantly lowered in H2O2 alone treated
animals (Group II) when compared with control animals
In vivo antioxidant activity: Effect of UU-extract on lipid (Group I). The alterations of GSH-levels were reverted to nearly
peroxidation status: Table 2 represents the levels of lipid control values on the administration of UU-extract treated
peroxidation (TBARS) in the liver, spleen and small intestine of animals (groups III) when compared with (group I) animals.
control and experimental animals. A significant increase in the Animals intoxicate then treated with UU-extract (Group III) did
levels of TBARS was observed in the hydrogen peroxide (H2O2) not show any significant variations when compared to control
alone treated animals (Group II) when compared with control (Group I) animals.
animals (Group I). This was significantly reversed to near
normal levels in Urtica urens (3 mg kgG1 b.wt.) treated animals Effect of UU-extract on superoxide dismutase (SOD): Rats
(Group III). The UU-extract treated animals (Group III) did not intoxicate with H2O2 had significantly low levels of SOD
show any significant variations when compared to control activity compared to the control rats. However, Animals
(Group I) animals. According to these observations UU-extract intoxicate then treated with UU-extract (Group III) to show a

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 Int. J. Pharmacol., 13 (3): 332-339, 2017
In vivo antibacterial activity
Histopathological observation
(a)

CON-A SI-A SIUU-A

(b)

CON-B SI-B SIUU-B

(c)

CON-C SI-C SIUU-C

Fig. 1(a-c): Histopathological changes in organs in CON, SI and SIUU. (a) Liver (×200), (b) Spleen (×200) and (c) Small intestine
(×200). CON-A control: Normal hepatocytes showing normal architecture with portal tried, showing portal veins,
hepatic artery and vein. SI-A congestion and edematous changes within the central and portal veins of the liver and
severe hemorrhagic necrosis was also observed within the red pulp of the (SI-B). In addition, destruction and atrophy
with ischemic necrosis within the mucous layers of the small intestines where observed (SI-C). Urtica urens-fed mice
(test group) infected with S. typhimurium. Histological damages in the above organs were rarely observed in these
mice (SIUU)

significant (p<0.001) increase in SOD levels when observed in group III animals. In addition, destruction, atrophy
compared with the control group (Table 4). and edematous changes with polymorphonuclear leukocyte
infiltration within the mucous layers of the small intestines
Organ histopathologic change: Group II animals were were observed. Conversely, clinical signs and histological
lethargic and showed signs of histological damage in the liver, damage were rarely observed in H2O2 intoxicated-mice fed
spleen and small intestine. The central and portal veins of the with the UU-extract (Fig. 2).
liver showed congestion with focal necrotic emboli-like
materials. The histological photomicrographs of the spleen DISCUSSION
sections are shown in Fig. 2. The congestion of the spleen
tissue was showed in the H2O2-treated group, while no severe In the present study, Urtica urens-extract was screened
damages and lymph nodule proliferation of spleen tissue were for antibiotic activity against several pathogenic Salmonella

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 Int. J. Pharmacol., 13 (3): 332-339, 2017
In vivo antioxidant activity
Histopathological analysis
(a)

CON-A RI-A RIUU-A

(b)

CON-B RI-B RIUU-B

(c)

CON-C RI-C RIUU-C

Fig. 2(a-c): Histopathological changes in organs in CON, RI and RIUU. (a) Liver, (b) Spleen and (c) Small intestine, CON: Control rat,
RI: Rats intoxicate with H2O2 alone (negative control), RIUU: Rats intoxicate with H2O2 then treated with aqueous extract
of Urtica urens, (H and E X200)

Table 4: Level of SOD in liver, spleen and small intestine of control and experimental animals in each group
SOD (U mgG1 protein)
-----------------------------------------------------------------------------------------------------------------
Parameters Liver Spleen Small intestine
Group I: Control rats 17.37±2.27 8.22±0.63 15.95±0.14
Group II: Rats intoxicate with H2O2 4.88±0.71*** 2.17±0.15*** 7.60±1.16***
Group III: Rats intoxicate then treated with aqueous extract (UU) 13.75±2.26 7.00±0.31 14.89±0.36
Values are expressed as Mean±SD (n = 6). ***Significantly different from control at p<0.001

serotypes. The in vivo antibacterial assay revealed that the describe the antibacterial activity of UU-extract against
extract showed the effective inhibition of S. typhimurium S. typhimurium. Based on this promising in vivo assay
growth and significantly reduced mice mortality (Table 1). results it is clearly proved that UU-extract can be considered
Furthermore, clinical infection signs and histological damage like a novel antimicrobial treatment for salmonellosis. The
were rarely observed in the SIUU-group (Fig. 1), whereas UU-extract has been reported only to show the antibacterial
infected mice SI showed severe clinical signs and histological activity against Staphylococcus aureus, Streptococcus
damage in the considered organs. This is the first report to pyogenes, Escherichia coli and Pseudomonas aeruginosa

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 Int. J. Pharmacol., 13 (3): 332-339, 2017

delivery as reported by Leven et al.23. The antibacterial activity antioxidant defense system in the controls groups. This result
of UU-extract may be indicative of the presence of some was in agreement with that reported by Zheng et al.29.
metabolic toxins or broad-spectrum antibiotics. Several Histopathological studies carried out for the liver, spleen and
metabolites from herb species, such as, alkaloids, tannins, small intestine of control group, H2O2 treated and UU-extract
saponins and sterols have been previously associated with treated results are given in Fig. 2. The massive generation of
antimicrobial activity reported by Taguri et al.24. The major free radical in the H2O2-induced tissues damages provokes a
chemical constituents of Urtica urens are flavonoids, sharp increase of lipid peroxidation. On the other hand, it
caffeoyl-esters, caffeic acid, scopoletin (cumarin), sitosterol reduces significantly the of GSH and SOD levels in liver, spleen
(-3-O-glucoside), polysaccharides, fatty acids (e.g., and intestine, respectively.
13-hydroxy-octadecadienoic acid), minerals (herba: up to 20% The results of this study were supported by similar
leaves: 1-5%) as discussed by Doukkali et al.25 And the aerial observation in the others researchers30,31 that H2O2 was able to
parts are rich in minerals and vitamins and Urtica urens was induce oxidative stress in these tissues. In case of H2O2-treated
reported to show anti-food-borne pathogens. rats, strong modification in organ architecture and areas of
Furthermore, antioxidant activity is one of the most hemorrhage and necrosis were seen. However, in the case of
intensively studied subjects in aqueous plant extract. In this group III, the liver, spleen and small intestine were shown to
study, the therapeutic effects of UU-extract were studied by retain normal architecture with few areas of hemorrhage
examining the prevention of hydrogen peroxide induced (Fig. 2).
stress in rats. The H2O2 is one of the most widely used toxicant In this study, the results showed that UU-extract
for experimental induction of liver, spleen and intestine in treatment prevented H2O2-induced stress in rats by
strengthening the antioxidant defense system. Therefore,
laboratory animals.
these results demonstrated that the UU-extract has protective
Malondialdehyde is generated from the degradation of
function against H2O2 toxicity in rat liver, spleen and small
polyunsaturated lipids by ROS. It is one of the most frequently
intestine. Similar results have been reported for some other
used indicators of lipid peroxidation26, in this study we have
ethnobotanical fruits and herbs, in agreement with the
demonstrated that elevated levels of MDA in H2O2-induced
analysis of Kim et al.32. The results of the present study may
rats were reduced after the treatment with UU-extract
have very important implications for the chemopreventive
(Table 2).
potentials antibacterial and antioxidant profiles of aqueous
Glutathione is the major endogenous antioxidant
extract of U. urens as a traditional herbal medicine.
produced by the cells, participating directly in the
neutralization of free radicals and reactive oxygen
CONCLUSION
compounds, it is noteworthy to cite the study of Swaroop
and Ramasarma27. In the present study, significantly low
This study may suggest new treatments in the curative of
GSH levels were observed in rats intoxicated with H2O2 as
salmonellosis and oxidative stress reveals the importance of
compared to the control. While UU-extract treatment showed
scientific research on miscellaneous plants with various
significant increase above normal level. Thus, we noted that
medicinal properties. Further studies are required to evaluate
UU-extract may offer better antioxidant effect by scavenging
the possible interactions of U. urens with therapeutic drugs
free radicals and restoring the imbalance between
and/or other dietary components in order to clarify its possible
oxidant/antioxidant homeostasis developed during stress use as traditional medicinal herb.
condition (Table 3).
Antioxidant enzymes such as SOD have been shown vital ACKNOWLEDGEMENT
to eliminate ROS. The SOD is the most important antioxidant
enzyme that inhibit free radical formation and is usually used We thank Prof. Ben Attia Msaddek from Science of live
as biomarker to indicate ROS production28. The SOD is one of department of Faculty of Science of Bizerta, for scientific
the important enzymes that scavenges superoxide radical discussion and advice.
(O2  ) to H2O2 and molecular oxygen29. Table 4 depicts the
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