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Free Radical Scavenging and Antioxidant Activities of

Different Parts of Nitraria schoberi L.
Javad Sharifi Rad

abc

, Seyedeh Mahsan Hoseini Alfatemi , Majid Sharifi Rad & Marcello Iriti

Zabol Medicinal Plants Research Center, Zabol University of Medical Sciences, P.O. Box:
61615-585 Zabol, Iran
b

Cereal Health Research Center of Zabol, Zabol University of Medical Sciences, P.O. Box:
61615-585 Zabol, Iran
c

Department of Pharmacognosy, Faculty of Pharmacy, Zabol University of Medical Sciences,

P.O. Box: 61615-585 Zabol, Iran
d

Department of Bacteriology and Virology, Shiraz Medical School, Shiraz University of

Medical Sciences, Shiraz, Iran
e

Department of Range and Watershed Management, Faculty of Natural Resources, University

of Zabol, Iran
f

Department of Agricultural and Environmental Sciences, Milan State University, via G.

Celoria 2 - 20133 Milan, Italy
Published online: 04 Mar 2014.

To cite this article: Javad Sharifi Rad, Seyedeh Mahsan Hoseini Alfatemi, Majid Sharifi Rad & Marcello Iriti (2014) Free Radical
Scavenging and Antioxidant Activities of Different Parts of Nitraria schoberi L., Journal of Biologically Active Products from
Nature, 4:1, 44-51, DOI: 10.1080/22311866.2014.890070
To link to this article: http://dx.doi.org/10.1080/22311866.2014.890070

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TBAP 4 (1) 2014 pp 44 - 51

44
ISSN Print: 2231-1866
ISSN Online: 2231-1874

Free Radical Scavenging and Antioxidant

Activities of Different Parts of Nitraria schoberi L.
Javad Sharifi Rad 1, 2, 3, Seyedeh Mahsan Hoseini Alfatemi 4*,
Majid Sharifi Rad 5 and Marcello Iriti 6

Downloaded by [Javad Sharifi Rad] at 09:14 06 March 2014

Zabol Medicinal Plants Research Center, Zabol University of

Medical Sciences, P.O. Box: 61615-585 Zabol, Iran
2
Cereal Health Research Center of Zabol, Zabol University of
Medical Sciences, P.O. Box 61615-585 Zabol, Iran
3
Department of Pharmacognosy, Faculty of Pharmacy, Zabol University
of Medical Sciences, P.O. Box: 61615-585 Zabol, Iran
4
Department of Bacteriology and Virology, Shiraz Medical School,
Shiraz University of Medical Sciences, Shiraz, Iran
5
Department of Range and Watershed Management,
Faculty of Natural Resources, University of Zabol, Iran
6
Department of Agricultural and Environmental Sciences,
Milan State University, via G. Celoria 2 - 20133 Milan, Italy
Received 28 November 2013; accepted in revised form 19 December 2013

Abstract: This study represents the first report on antioxidant and free radical scavenging activities of
different extracts of Nitraria schoberi L. (Nitrariaceae). Antioxidant phytochemicals may play a protective
role in human, counteracting free radical damage and oxidative stress. The aim of this study was to assess the
free radical scavenging and antioxidant capacities of N. schoberi fruits, leaves and roots by ad hoc in vitro
assays. Aqueous, chloroform and methanol extracts were analyzed. Our results showed that, in general, the
maximum free radical and antioxidant activities were measured in the methanol extracts, decreasing from
fruits to leaves and roots, thus suggesting that N. schoberi may be considered a novel and effective source of
healthy antioxidants and bioactive phytochemicals.
Key words: Nitraria schoberi L., antioxidants, free radicals, radical scavenging activity,
bioactive phytochemicals.
Introduction
Oxygen is essential for aerobic organisms.
However, in particular conditions, reactive
oxygen species (ROS), byproducts of molecular
oxygen including both radical and non-radical
species, can damage macromolecules and
detrimentally affect human health 1. ROS are
highly unstable and harmful molecules, which

have the capacity to donate their unpaired electron to cell molecules or to extract electrons from
other molecules to reach stability 2. Therefore,
ROS are able to damage biomolecules (lipids,
proteins and nucleic acids), activate oncogenes,
trigger immune response and increase the cellular
aging processes 3. In living organisms, ROS can
be neutralized by a plethora of ad hoc defense

*Corresponding author (Seyedeh Mahsan Hoseini Alfatemi)

E-mail: < m.hoseinialfatemi@gmail.com >

2013, Har Krishan Bhalla & Sons

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Javad Sharifi Rad et al., / TBAP 4 (1) 2014 44 - 51

systems, consisting of both enzymatic and nonenzymatic antioxidants able to protect human
from chronic-degenerative diseases such as
cardiovascular and neurodegenerative disorders,
certain types of cancer and aging 4,5. Medicinal
and food plants may decrease the oxidative
burden in the human body, by virtue of their pool
of antioxidant compounds. The latter may protect
against ROS toxicity by different mechanisms:
i) avoiding ROS generation; ii) scavenging ROS
and their byproducts; iii) exchanging ROS with
less reactive molecules; or iv) improving the
resistance of sensitive biological targets to ROS
damage 6.
Despite plants are greatly exploited in traditional healing systems, only in some cases their
therapeutic potential in human has been
substantiated. The need of herb-based medicines,
cosmetics, food supplements, pharmaceuticals
and health products is progressively increasing
worldwide, because, in some cases, natural
products i) are non or low toxic, ii) have low side
effects and iii) are available at affordable costs 7.
Because, as previously introduced, free-radicals
and other ROS are mechanistically involved in
the pathogenesis of chronic-degenerative diseases
8,9
, recently an increasing interest has been
recorded in the research of new phytochemicals
able to inhibit the production of oxidants at
sensitive target sites and to defend cells and
tissues from injury 9. One of the most effective
approaches for discovering new antioxidants is
the screening of plant extracts used in traditional
medicine. Since years, plant antioxidants, such
as toco-pherols, ascorbic acid, carotenoids and
poly-phenols attract the food industry as alternatives to synthetic products, whose consumption
is restricted because of safety concerns 10.
Nitraria schoberi L. is a member of the genus
Nitraria (Nitrariaceae), widely distributed in the
Middle East, central Asia and northwest China.
Due to its drought-resistance and salt-tolerance,
N. schoberi possesses remarkable eco-physiological traits 11. Leaves, seeds and fruits of this
plant are often used in traditional medicine as an
antineuropathic, antiarrhythmic and antispasmodic agent 12. Senejoux et al., showed that the
fruits of Nitraria sibirica are a source of phenolic
compounds 13, powerful antioxidants which may

45

protect cells and tissues from oxidative stress 14.

Because of the paucity of data on antioxidant
capacity of N. schoberi, the present study was
carried out to provide in vitro results to support
the use of this plant as antioxidant agent. To the
best of our knowledge, this study represents the
first report on the free radical scavenging and
antioxidant activities of fruits, leaves and roots
of N. schoberi.
Materials and methods
Fresh and soft fruits, leaves and roots of
Nitraria schoberi L. (Nitrariaceae) were collected
from Hamoon International Wetland, Zabol, Iran.
Plant species was determined at the Department
of Botany of Shahid Beheshti University of
Medical Sciences, Iran, and a specimen voucher
was conserved in the Department of Range and
Watershed Management, Faculty of Natural
Resources, University of Zabol, Iran. All parts of
plant were thoroughly washed in distilled water
for three times and, then, they were placed in an
oven at 75C for 48 hours. Extraction with
organic solvents was carried out, and methanol
and chloroform extracts were evaporated to
dryness. The residue was dissolved in dimethysulphoxide (DMSO) at concentration of 30 mg/6
l. In addition, fresh aqueous extract was also
used for the study.
ABTS radical-scavenging assay
The antiradical activity of N. schoberi fruit, leaf
and root extracts was investigated by 2,2azinobis 3-ethylbenzothiazoline-6-sulphonate
(ABTS) radical cation decolourisation assay
according to the method of Anagnostopoulou et
al.,15. Radical cation was produced by reacting
an ABTS aqueous solution (7 mmol/L) with
K2S2O8 (2.45 mmol/L, final concentration), in the
dark for 12-15 hours. Then, extract samples (15
mL) were diluted with 1.485 mL ABTS.+ solution
and absorbance at 734 nm was recorded 1 min
after initial mixing and at 1 min intervals (for 30
min). The percentage of inhibition was plotted
as a function of concentration.
DPPH radical-scavenging assay
The scavenging capacity of N. schoberi fruit,
leaf and root extracts against the stable free

Javad Sharifi Rad et al., / TBAP 4 (1) 2014 44 - 51

radical 2,2-diphenyl-1-pycrylhydrazyl (DPPH)
was measured according to the method of Mensor
et al.,16. One mL of 0.3 mM DPPH methanol
solution was added to 2.5 mL sample or control.
The solution was vigorously mixed and left to
stand at 25C for 30 min in the dark. The mixture
was spectrophotometrically measured at 518 nm,
and the percentage of inhibition was determined.
The radical-scavenging capacity was calculated
as below:

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AA% = 100 - [(Abssample - Absempty sample)/Abscontrol

x 100]
where: Abs is absorbance; empty sample = 1
mL methanol + 2.5 mL extract; control sample =
1 mL 0.3 mM DPPH + 2.5 mL methanol.
Hydrogen peroxide-scavenging test
The capacity of N. schoberi fruit, leaf and root
extracts to scavenge hydrogen peroxide was
assessed by the method of Ruch et al., 17. A
solution of hydrogen peroxide (30 mM) was
prepared in phosphate buffer (pH 7.4). Hydrogen
peroxide concentration was spectrophotometrically measured by absorption at 230 nm.
Extracts (50-250 g) in distilled water were added
to hydrogen peroxide solution (0.6 mL, 40 mM).
Absorbance of hydrogen peroxide at 230 nm was
determined after 10 minute against a blank
solution containing only phosphate buffer without
hydrogen peroxide. The percentage of hydrogen
peroxide scavenging was determined by the
following equation:
Percent scavenged [H 2 O 2 ] = [(Abs control Abssample)/Abscontrol] 100
where Abs is absorbance 18.
Nitric oxide-scavenging activity
Inhibition of nitric oxide radical generation in
vitro was measured by the method of Green et
al., 19. One mL of each plant extract was mixed
with 1 mL of the reaction solution containing
sodium nitroprusside (10 mmol/L) in phosphate
buffer (50 mmol/L, pH 7.0). After incubation at
35C for 1 hour, a 0.5 mL aliquot was mixed with

46

0.5 mL of Griess reagent. The absorbance at 540

nm was measured.
Superoxide anion-scavenging activity
Superoxide anion scavenging ability of the
fruit, leaf and root extracts of N. schoberi was
assessed by the method of Winterbourn et al., 21.
The test mixture included samples with 0.1 mL
nitroblue tetrazolium (1.5 mM) solution, 0.2 mL
EDTA (0.1 M), 0.05 mL riboflavin (0.12 mM)
and 2.55 mL phosphate buffer (0.067 M). The
reaction mixture was illuminated for 30 min and
the absorbance at 560 nm was measured. The
percentage inhibition was calculated.
Hydroxyl radical-scavenging activity
The capacity of N. schoberi fruit, leaf and root
extracts to scavenge hydroxyl radical (OH.) was
determined by 2'-deoxyribose oxidative
degradation assay as previously described 20. Test
is based on quantification of the degradation
product of 2-deoxyribose by condensation with
TBA. Hydroxyl radical was generated by the Fe3+ascorbate-EDTA-H2O2 system (Fenton reaction).
The reaction mixture included 0.1 mL 2deoxyribose (2.7 mM), 0.1 mL EDTA (0.1 mM),
0.1 mL H2O2 (1 mM), 0.1 mL ascorbate (0.1 mM),
0.1 mL KH2PO4-KOH buffer (20 mM, pH 7.4)
and various concentrations of plant extracts in a
final volume of 1 mL. The reaction mixture was
incubated for 1 h at 35C. 2-Deoxyribose
degradation was measured as thiobarbituric acid
reactive substances (TBARS) and the percentage
inhibition was calculated.
Statistical analysis
All tests were carried out in triplicate and the
results reported as mean standard error (SE).
Data were subjected to analysis of variance
(ANOVA) following a completely random design
to determine the least significant difference
(LSD) and t-test at P < 0.05 using SPSS v. 11.5.
Results
In this study, the radical scavenging and antioxidant activities of fruit, leaf and root aqueous,
methanol and chloroform extracts of N. schoberi
were measured on the basis of their ability to

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Javad Sharifi Rad et al., / TBAP 4 (1) 2014 44 - 51

scavenge stable free radicals and ROS.
The results on DPPH assay showed that
methanol extracts of fruits, leaves and roots exhibited the maximum scavenging activities (inhibition of 86 %, 45 % and 25 %, respectively) (Fig.
1). Aqueous extracts of fruits, leaves and roots
inhibited DPPH radical by 70 %, 32 % and 14 %,
respectively, whereas the lowest inhibitions were
measured in chloroform extracts (57 %, 28 % and
9 % for fruits, leaves and roots, respectively) (Fig.
1). Similar results were reported on ABTS
radical- and H2O2-scavenging activities (Fig. 1).
Fruit, leaf and root methanolic extracts showed
the highest ABTS radical-scavenging capacities
(inhibition of 90 %, 52 % and 19 %, respectively)
(Fig. 1). For the aqueous extracts, inhibitions
were 79 %, 30 % and 12 % for fruits, leaves and
roots, respectively, whereas chloro-form extracts
of fruits, leaves and roots inhibited ABTS radical
by 70 %, 27 % and 8.5 %, respectively (Fig. 1).

47

The results on H2O2 scavenging activity also

showed the maximum inhibitions in methanol
extracts of fruits, leaves and roots (83 %, 42 %
and 23 %, respectively) (fig. 1). For fruits, leaves
and roots, aqueous extracts exhibited inhibitions
of 73 %, 35 % and 15 %, respectively, and chloroform extracts inhibited H2O2 by 63 %, 29 % and
9 %, respectively (Fig. 1).
Methanol extracts were the most effective
against the in vitro generation of nitric oxide (NO)
radical and superoxide anion (Fig. 2). In NO
radical assay, the inhibitions of methanol extracts
were 68 %, 35 % and 25 % in fruits, leaves and
roots, respectively (Fig. 2) Aqueous extracts
obtained from fruits, leaves and roots inhibited
by 63 %, 32 % and 15 %, respectively, the NO
generation, whereas the minimum inhibitions of
NO radical were determined by chloroform
extracts (59 %, 28 % and 12 % for fruits, leaves
and roots, respectively) (Fig. 2). In superoxide

Figure 1. DPPH-, ABTS- and H 2O2-scavenging activities of Nitraria schoberi fruit, leaf
and root extracts (FA, fruits-aqueous; FM, fruits-methanol; FCh, fruits-chloroform; LA,
leaves-aqueous; LM, leaves-methanol; LCh, leaves-chloroform; RA, roots-aqueous;
RM, roots-methanol; RCh, roots-chloroform).

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Javad Sharifi Rad et al., / TBAP 4 (1) 2014 44 - 51

anion assay, 82 %, 39 % and 29 % inhibitions
were measured with fruit, leaf and root methanol
extracts, respectively (Fig. 2). In fruits, leaves and
roots, for aqueous extracts, inhibitions were 73
%, 29 % and 13 %, respectively, while chloroform
extracts inhibited superoxide radical generation
by 69 %, 36 % and 10 %, respectively (Fig. 2).
The protective effects of N. schoberi extracts
on hydroxyl radical (OH.)-induced oxidative
degradation of 2-deoxyribose were assessed as
production of thiobarbituric acid reactive
substances (TBARS) (Table 1). All root extracts
exhibited the maximum inhibition of TBARS
formation (28 %, 29 % and 32 % in methanol,
aqueous and chloroform extracts, respectively)
(Table 1). Finally, in both leaf and fruit samples,
the highest efficiency of TBARS inhibition was
measured by methanol extracts (32 % and 39 %,
respectively) (Table 1).
Discussion
The assessment of both DPPH radical- and
ABTS radical-scavenging capacities of a natural
product represents a reliable index of its

48

antiradical potential. Belaya et al., reported that

DPPH radical-scavenging capacity was higher in
fresh orange and grape juices than in their
concentrated form 22. Saha et al., found that the
methanol extract of Mimusops elengi L. leaves
exerted a dose-dependent DPPH radicalscavenging activity 23. Mahjoub et al., reported
that extracts of Rhus tripartitum from four
different solvents, namely chloroform, ethyl
acetate, methanol and ethyl acetate/methanol,
possessed different ABTS radical-scavenging
activity 24. Similarly, Khajeddini et al., found that,
in N. schoberi fruits, the highest DPPH radicalscavenging activity was measured in methanolic
extract, possibly due to the phenolic compounds
mainly accumulated in polar extracts 25 .
Mayakrishnan et al., demonstrated that Lagenaria
siceraria (Molina) fruit extracts exerted both
DPPH radical- and ABTS radical-scavenging
activities, with IC50 values of 1.95 mg/mL and 19
mg/mL, respectively, suggesting that L. siceraria
fruits could be impor-tant sources of natural
radical scavengers 10.
As regards other assays, Sreelatha and Padma

Figure 2. Inhibition (%) of nitric oxide and superoxide anion generation by Nitraria schoberi
fruit, leaf and root extracts. (FA, fruits-aqueous; FM, fruits-methanol; FCh, fruits-chloroform;
LA, leaves-aqueous; LM, leaves-methanol; LCh, leaves-chloroform; RA, roots-aqueous;
RM, roots-methanol; RCh, roots-chloroform).

Javad Sharifi Rad et al., / TBAP 4 (1) 2014 44 - 51

49

Table 1. Hydroxyl radical (OH.)-scavenging activity of

Nitraria schoberi fruit, leaf and root extracts

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Sample

No extract
Fruits Aqueous
Fruits Methanol
Fruits Chloroform
Leaves Aqueous
Leaves Methanol
Leaves Chloroform
Roots Aqueous
Roots Methanol
Roots Chloroform

TBARS (%)
Control
OH.
25.00 0.01A
46.23 0.01B
42.73 0.01C
48.14 0.01D
32.01 0.01E
28.00 0.00F
36.14 0.02G
21.12 0.01H
19.14 0.01K
25.00 0.00AL

100.00 0.01a
55.23 0.00b
39.14 0.01c
58.00 0.01d
46.00 0.01e
32.05 0.00f
49.01 0.01g
29.00 0.01h
28.21 0.00k
32.00 0.01l

Results are expressed as mean SE of three replicates;

Means with different letters are significantly different (LSD test and t-test were used to calculate differences
among plant extracts and between control and OH. treatment, respectively, at P < 0.05).

reported that the extracts of both mature and

young leaves of Moringa oleifera Lam. possessed
a relevant superoxide anion-scavenging activity
26
. In a cell free system, Lee et al., documented a
high NO-scavenging capacity of the aqueous
extract of Wasabia japonica 27. NO-scavenging
assay was also used by Deepa et al., to compare
the antioxidant effects of the ethanolic extracts
from leaves of Commiphora caudate and Commiphora pubescens 28.
Antioxidants can also block the formation of
OH. radical and free radical chain reactions 29.
Interestingly, Jimenez et al., reported that samples
from both unprocessed and processed apricot
(Prunus armeniaca var. bulida) exhibited a
relevant OH. radical-scavenging activity, which
was higher than that of the standard antioxidants
BHT and BHA 30.
Our results are in accordance with these data,
demonstrating that the N. schoberi fruits, roots
and leaves possess significant antiradical and
antioxidant activities, in particular their methanol
extracts. Furthermore, among the various parts

of N. schoberi assayed, fruits showed higher

activities compared with roots and leaves, in all
tests with the exception of the hydroxyl radicalscavenging assay, where root extracts were the
most effective.
Conclusions
In conclusion, despite the free radical scavenging and antioxidant activities of different N.
schoberi parts, the use of fruit extracts as
nutraceuticals, in particular, seems to be reasonable. However, further in vivo studies are needed
in order to confirm in vitro results and to evaluate
putative toxicological risks, and it would be of
interest to isolate and identify the specific compounds responsible for the antioxidant activity
of N. schoberi fruits, leaves and roots. Not the
least, the accessibility and everlasting growth of
this plant represent an appreciable resource in
traditional Iranian medicine.
Conflict of interest statement
No conflict of interest by authors.

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