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© by PSP Volume 23 – No 6. 2014 Fresenius Environmental Bulletin
1
ANTIOXIDANT, ANTI-INFLAMMATORY AND
ANTI-ACETYLCHOLINESTERASE ACTIVITIES
OF ELEVEN EXTRACTS OF MOROCCAN PLANTS
Maria Miguel1, Najat Bouchmaaa2, Smail Aazza1, 2, Farah Gaamoussi1 and Badiaâ Lyoussi2
1 Universidade do Algarve, Faculdade de Ciências e Tecnologia, Departamento de Química e Farmácia,
Instituto de Biotecnologia e Bioengenharia, Centro Biotecnologia Vegetal, Campus de Gambelas 8005-139 Faro, Portugal
2 Laboratory of Physiology, Pharmacology and Environmental Health, Faculty of Sciences Dhar El Mehraz,
BP 1796 Atlas, University Sidi Mohamed Ben Abdallah, Fez 30 000, Morocco
ABSTRACT
The capacity of ethanolic extracts of Haloxylon sco-
parium Pomel, Corrigiola telephiifolia Pourr., Ammodau-
cus leucotrichus Cosson & Durieu subsp. leucotrichus,
Chamaerops humilis L., Sideritis arborescens Salzm. ex
Benth., Ammi visnaga (L.) Lam., Vitex agnus castus L.,
Retama raetam (Forssk.) Webb & Berthel., Berberis
vulgaris L., Viscum album L., and Equisetum arvense L.
from Morocco to prevent lipid peroxidation, scavenging
free radicals, inhibiting lipoxygenase and acetylcholi-
nesterase activities, were evaluated and compared to those
reported in the literature. As far as we know, the present
work was the first reporting on the antioxidant ability of
S. arborescens. The results showed that Equisetum ar-
vense and Sideritis arborescens (stems) possessed the high-
est concentrations of total phenols and flavonoids, respec-
tively, and the extracts of Berberis vulgaris and Viscum
album were the most promising as antioxidants as well as
anti-inflammatory and acetylcholinesterase inhibitors. In
some cases, the activities of B. vulgaris extracts were not
significantly different from those found for positive con-
trol (e.g. capacity for scavenging free radicals, and capac-
ity for inhibiting AChE).
KEYWORDS: Free radicals, lipoxygenase, acetylcholinesterase,
wild plants, Morocco
INTRODUCTION
The history of medicinal and aromatic plants is asso-
ciated with the development of civilizations. China (birth-
place of herbal medicine), India, the Middle East, espe-
cially the Arabo-Muslim world, Egypt, Greece, and Rome
represent civilizations in which aromatic and medicinal
plants had an important role [1].
According to the World Health Organization (WHO)
in 2008, more than 80% of the world's population relies on
* Corresponding author
traditional medicine for their primary healthcare needs.
Herbal-derived compounds are the basis for a large propor-
tion of the commercial medications used today in develop-
ing countries for treatment of several diseases [2-4].
Haloxylon scoparium Pomel [syn. Hammada sco-
paria (Pomel) Iljin.; Arthrophytum scoparium (Pomel)
Iljin.; Salsola articulata Cav.; Haloxylon articulatum
(Cav.)], (Chenopodiaceae) can grow wild in south-east
Spain, North Africa, parts of Iran, Turkey, Iraq and Syria
[5]. This plant is known in Morocco as “âkenoud”, “Rremt”
and “âssây”. In this country, H. scoparium (whole plant) can
be used as cicatrizing agent to treat headaches, for antidia-
betic medications, or in the treatment of hypertension [6, 7].
Corrigiola telephiifolia Pourr. (Caryophyllaceae) is a
Moroccan medicinal plant called “sarghina”. This species
is found in Southern Europe and North Africa. The root is
used to treat flu, dermatological diseases, inflammation,
ulcer, cough, jaundice and diuretics [8]. Root decoction
has been reported to be used in Morocco in the treatment
of cancer (digestive and liver); however, there are studies
showing that extracts of Corrigiola telephiifolia present
toxicological effects [9-11].
Ammodaucus leucotrichus Cosson & Durieu subsp.
leucotrichus (Apiaceae) grows wild in maritime sands of
Morocco, Algeria and Tunisia, extending to Egypt and
tropical Africa [12]. In Morocco, this species is known as
“kamounte ben şofa, kammoun Şofi”. Moroccan people use
the fruits either as a powder or in decoction to treat gastric-
intestinal pain and indigestion. As infusion, this species is
used for some child diseases: nausea, regurgitation, and
vomiting [13]. Other authors also refer that the leaves of
this plant are used by Moroccan people in cases of dehy-
dration, cooling and excessive secretion of urine [14]. The
seeds are used as substitute for ordinary cumin [15, 16].
Chamaerops humilis L. (Arecaceae) (dwarf fan palm,
European fan palm) is known in Morocco as “doum”.
This species is native to the Mediterranean coast, growing
wild, mainly along the Moroccan coast. Fruits are eaten in
Morocco, and an aqueous concoction made from the palm
© by PSP Volume 23 – No 6. 2014 Fresenius Environmental Bulletin
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leaves of this plant, is also used to treat diabetes in this
country [17, 18].
The genus Sideritis (Lamiaceae) comprises more than
150 perennial and annual vegetal species distributed in the
Mediterranean area, including Canary and Madeira islands.
Due to the high number of hybridizations that occur be-
tween species, the taxonomical classification is complex
[19]. Sideritis arborescens Salzm. ex Benth. subsp. arbor-
escens is endemic to Iberian Peninsula, whereas Sideritis
arborescens Bentham subsp. ortonedae (Labiatae) (Font
Quer & Pau) Maire is endemic to Morocco [20, 21].
Sideritis species have been traditionally used as teas
for feeding, flavouring agents, and in folk medicine as
antiinflammatory, antiulcerative, antimicrobial, vulnerary,
antioxidant, antispasmodic, anticonvulsant, analgesic and
carminative agents [19]. In Morocco, Sideritis spp. has
also been used in folk medicine to treat diabetes [6].
Ammi visnaga (L.) Lam. belongs to the Apiaceae fam-
ily and grows wild in the Mediterranean region. In Europe,
this species is known as toothpick herb or Bishop’s weed,
whereas the Arabic name is “khella” and that in Morocco is
“bachnikha” [6, 22-24]. In Morocco, fruit decoction of this
plant is used for hypoglycaemic, diuretic, hypotensive,
hair-care, anthelmintic, antispasmodic, antirheumatic, anti-
septic, tonic, and dental hygiene treatments, as well as
against vertigo and for nephritic colic symptoms [6, 23].
Vitex agnus castus L. (Verbenaceae), with the com-
mon name chastetree, is known in Morocco as “shajarat
mariam”, and is a deciduous shrub that is native to Medi-
terranean Europe and Central Asia. This plant, particu-
larly its fruit extract, has been used in the treatment of
menstrual disorders, including premenstrual symptoms
and spasmodic dysmenorrhoea, for some menopausal con-
ditions, for insufficient lactation, and for the treatment of
acne [25-27]. It was also described as emmenagogue (herb),
carminative, anthelmintic and anti-inflammatory drug [25].
The aromatic leaves are used as a spice [28]. In the Imouzzer
Ida Outanane region, Vitex agnus castus is used for burns,
colds, headache (leaves, seeds) and as fumigant. In this
region, this species is known as “angarf-lkrwaa” [29].
Retama raetam (Forssk.) Webb & Berthel. (Fa-
baceae), commonly known as ‘raetam’, is a desert shrub
native to several countries of North-Africa (Algeria, Egypt,
Libya, Morocco and Tunisia), temperate Asia (Israel, Jor-
dan, Lebanon, Palestine and Syria), and south-eastern
Europe (Sicily in Italy) [30]. In Morocco, it is largely
spread in desert regions and Middle Atlas. Ethnobotanical
studies made in south-eastern region of Morocco (Ta-
filalet) revealed that R. raetam is used for diabetes and
hypertension control [7]. In Morocco, the stems and
leaves are also used after being crushed and mixed with
honey as an emetic. A decoction of the leaves is given as
purgative and anthelmintic. The powdered leaves and flow-
ers are used to heal circumcision wounds and as antiseptic
for wounds, skin rash and pruritus [13]. An ethnobotani-
cal survey made by [31] also revealed that a decoction
obtained from leaves and flowers of R. raetam is used
against skin diseases in Taounate province of Northern
Morocco.
Berberis vulgaris L. (Berberidaceae), known as bar-
berry, grows in Asia and Europe [32]. Berberis is the
Arabic name of the fruit that means a shell [33]. Diverse
parts of this plant have been used to treat diarrhea, gall-
bladder and liver disfunctions, malaria, leishmaniasis, stom-
ach problems, and urinary tract disease [24, 33]. Imansha-
hidi and Hosseinzadeh [32] reviewed the pharmacological
and therapeutics effects of B. vulgaris L. and its protober-
berine alkaloid (berberine), one of the isoquinoline alka-
loids present in this plant. In the south-eastern Morocco,
seeds, fruit and leaves of this plant, known as “hamida”,
are used in folk medicine for the treatment of hyperten-
sion and cardiac disease [7].
Viscum album L. (Loranthaceace) is a semiparasitic
plant, commonly known as European Mistletoe, that can be
found from northern Europe to northwest Africa, going east
from Europe, through Southwest and Central Asia to Japan
[35, 36]. Several therapeutic applications in folk medicine
of V. album have been reported, such as diabetes mellitus,
chronic cramps, stroke, stomach problems, heart palpita-
tions, to lower blood pressure, difficulties in breathing, and
hot flushing in menopause, asthma, vertigo, lumbago, epi-
lepsy, atherosclerosis, and cancer [35-37]. The aerial parts
of V. album, known in the south-eastern Morocco as
“dbake”, have been reported to be useful in the treatment of
cardiac diseases and hypertension [7].
Equisetum arvense L. (Equisetaceae) is a European
herb but also commonly found in America, Northern Africa
and Asia [38]. The ancient Greeks used E. arvense in the
treatment of wounds, whereas the Romans used it as a
vegetable, an animal feed and a medicine [39]. E. arvense
is used in traditional medicine as a diuretic, and in treatments
of urethritis, jaundice, hepatitis, stomach diseases, internal
bleeding, and respiratory tract infections [40]. Other authors
also referred that E. arvense has been recommended by
herbalists as haemostatic [41]. According to Eddouks et
al. [7], the aerial parts of E. arvense (“Dnab l’khil”) have
also been used by populations of the south-east region of
Morocco in cardiac diseases and as hypotensor.
The current work intends to evaluate the antioxidant
(in vitro) capacities, the anti-inflammatory effects, through
the ability for inhibiting in vitro lipoxygenase, and also the
capacities for inhibiting acetylcholinesterase of these plants
collected in Morocco. Some of them are already known to
possess antioxidant ability (Tables 2, 3 and 4). In this case,
comparisons will be performed. Due to the fact that herein
work other techniques were performed, the data obtained
will complement those found in other works.
2. MATERIALS AND METHODS
2.1 Plant material
Aerial parts of the plants were harvested in Morocco,
and identified and authenticated by Prof. M. Fennane of
© by PSP Volume 23 – No 6. 2014 Fresenius Environmental Bulletin
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the Scientific National Institute (Rabat, Morocco). Voucher
specimens are kept at the Herbarium of the Faculty of
Science Dhar Mahraz (Acronym: C3).
2.2 Extraction of phenols
Extraction of phenols was performed by sonication
on an ice-bath for 6 min using a VC300 Vibracell sonica-
tor (Sonics and Materials, USA) with a 20 kHz frequency.
One gram of dried powder in 10 ml of a hydro-alcoholic
solution (70%) was used. After sonication, the samples
were centrifuged for 5 min at 2000 g and 20 °C, and the
supernatant was removed and kept at −20 °C until deter-
mination of total phenols.
2.3 Determination of total phenols (Folin-Ciocalteau)
The total phenol contents of extracts were determined
using the Folin-Ciocalteau reagent and gallic acid as stan-
dard (described by Boulanouar et al. [42]). Tests were
carried out in triplicate.
2.4 Flavone and flavonol contents
Flavone and flavonol contents were quantified as de-
scribed by Boulanouar et al. [42]. Briefly, 0.5 ml of 2%
AlCl3-ethanol solution was added to 0.5 ml of sample or
standard. After 1 h at room temperature, the absorbance
was measured at 420 nm. Quercetin was used as standard
for the construction of calibration curves.
2.5 Thiobarbituric acid reactive species (TBARS)
The ability of samples to inhibit malondialdehyde for-
mation and, therefore, lipid peroxidation, was determined by
using a modified thiobarbituric acid reactive species
(TBARS) assay. Egg yolk homogenates were used as a
lipid-rich medium obtained as described by Boulanouar et
al. [42]. All of the values were based on the percentage
antioxidant index (AI %), whereby the control was com-
pletely peroxidized, and each oil demonstrated a degree of
change. The percentage inhibition was calculated using
the formula [(Ao−A1/Ao)×100], where Ao is the absorb-
ance of the blank sample and A1 is the absorbance of the
sample. It was plotted against sample concentrations and
IC50 was determined (concentration of extract able to
prevent 50% of lipid oxidation). Butylated hydroxytolu-
ene (BHT) was used as positive control.
2.6 ABTS free radical-scavenging activity
The determination of ABTS•+ radical scavenging was
carried out as reported by Boulanouar et al. [42]. The
values of IC50 were determined as reported above. Tests
were carried out in triplicate. BHT was used as positive
control.
2.7 Free radical scavenging activity (DPPH)
A methanolic stock solution (50 µl) of each sample at
different concentrations was placed in a cuvette, and 2 ml
of 60 µM methanolic solution of DPPH (2,2-diphenyl-1-
picrylhydrazyl) was added [42]. Absorbance measurements
were made at 517 nm (Shimadzu 160-UV spectropho-
tometer, Tokyo, Japan) after 60 min of reaction at room
temperature. The values of IC50 were determined as re-
ported above. Tests were carried out in triplicate, and BHT
was used as positive control.
2.8 Chelating metal ions
The degree of chelating ferrous ions by samples was
evaluated according to the method described by Bou-
lanouar et al. [42]. Tests were carried out in triplicate.
Sample concentration providing 50% inhibition (IC50) was
obtained plotting the inhibition percentage against sample
concentrations. EDTA was used as positive control.
2.9 Hydroxyl radical scavenging activity
The assay of OH scavenging activity was developed
according to Boulanouar et al. [42]. The OH-scavenging
activity (%) was calculated using the following equation:
Inhibition (%) = [(Ao−A1)/Ao]×100, where Ao is the
absorbance of the control (without sample) and A1 is the
absorbance in the presence of the sample. Tests were car-
ried out in triplicate. The sample concentration providing
50% inhibition (IC50) was obtained by plotting the inhibi-
tion percentage against extract concentrations. Mannitol
was used as positive control.
2.10 5-Lipoxygenase assay
The 5-lipoxygenase assay followed the procedure de-
scribed by Boulanouar et al. [42]. The percentage inhibi-
tion of enzyme activity was calculated by comparison with
the negative control: % = [(Ao−A1)/Ao]×100, where Ao is
the absorbance of the blank sample and A1 is the absorb-
ance of the sample. Tests were carried out in triplicate.
Sample concentration providing 50% inhibition (IC50) was
obtained plotting the inhibition percentage against sample
concentrations. Nordihydroguaiaretic acid (NDGA) was
used as positive control.
2.11 Acetylcholinesterase inhibition
The acetylcholinesterase inhibition assay was per-
formed according to that reported by Boulanouar et al.
[42]. The percentage inhibition of enzyme activity was
calculated by comparison with the negative control: % =
[(Ao – A1) / Ao]x100, where Ao is the absorbance of the
control without extract and A1 is the absorbance of the
sample. Tests were carried out in triplicate. Sample con-
centration providing 50% inhibition (IC50) was obtained
plotting the inhibition percentage against sample (essen-
tial oil or extract solution) concentrations. Galantamine
was used as positive control.
2.12 Statistical analysis
Statistical analysis was performed with the SPSS 18.0
software (SPSS Inc.). Statistical comparisons were made
with one-way ANOVA, followed by Tukey`s multiple
comparisons. The level of significance was set at p<0.05.
Correlations between phenol or flavonoid content and
© by PSP Volume 23 – No 6. 2014 Fresenius Environmental Bulletin
4
antioxidant activity were achieved by the Pearson correla-
tion coefficient (r) at a significance level of 99% (p<0.01)
and 95% (p<0.05).
3. RESULTS AND DISCUSSION
Table 1 depicts the total phenol and flavonoid con-
tents as well as the antioxidant activities of the extracts
obtained from plants harvested in Morocco. The lipoxy-
genase and acetylcholinesterase inhibition activities are
also presented in Table 1. Tables 2-4 review the antioxi-
dant activities found in the literature of those plants re-
ferred in the Introduction, as well as the capacities for
inhibiting lipoxygenase and acetylcholinesterase activities
in vitro. Some methods in these tables were not performed
by us; nevertheless, they were compiled therein, inde-
pendent of their citations, or not along with the Results
and Discussion section.
3.1 Phenols
Equisetum extracts had significantly higher amounts
of phenols than the remaining samples, immediately fol-
lowed by the extract of Chamaerops humilis. Haloxylon
scoparium extract along with Ammodaucus leucotrichus
had the lowest concentrations of phenols (Table 1). This
species had also the lowest amounts of total flavonoids
along with two other extracts, Sideritis arborescens (stems)
and Ammi visnaga. In contrast to the lowest concentra-
tions of flavonoids found in the stems of S. arborescens,
the leaves presented the highest concentration of flavon-
oids among the samples surveyed (Table 1). Comparing
the phenol content found for Equisetum in the present
work with those reported by other authors (see Table 2), it
was within the range found by some authors [43, 44], but
significantly inferior to those reported by Milovanović et
al. [45] and Kurkić et al. [46], which may be attributed to
several factors divided in two major groups [47]. One
group is in relation with the extraction and isolation of
phenols (plant parts used, extraction time, temperature,
solvent-to-sample ratio, the number of repeated extrac-
tions of the sample, solvent type, particle size), and the
second group is related to the plant: genetic heritage,
growth phase as well as soil and climatic conditions at the
growth area [48]. Differences of phenol content depending
on the different parts of the plant used were also observed
herein with S. arborescens. In this case, a significant differ-
ence was observed between leaves and stems, and such a
dissimilarity was more significant in flavonoid content than
in total phenols (Table 1). For other plants, some authors
also reported higher concentrations of flavonoids in leaves
than in other plant parts (for example, stems) [49].
The concentration of flavonoids in E. arvense extracts
found in the present work was substantially superior to
those observed by Štajner et al. [39] (Table 2).
3.2 Antioxidant activity
3.2.1 Lipid peroxidation
The capacity for preventing lipid peroxidation, evalu-
ated by the method of TBARS, showed that all samples
had such a capacity; nevertheless, it was significantly
inferior to that of the positive control (BHT) (Table 1).
Berberis vulgaris extract was the best extract for prevent-
ing lipid oxidation of egg yolk, in contrast to the extracts
obtained from the following plants: Haloxylon scoparium,
Ammodaucus leucotrichus, Chamaerops humilis, Equise-
tum arvense and Sideritis arborescens (leaves). Other
authors also reported onb lipid peroxidation capacity for
some plants studied herein, although using different tech-
niques, lipidic sources and unities (Table 3). Such facts
make it difficult to compare results.
Two works were found in which the unities for pre-
senting antioxidant activity (Table 3) were IC50 values as
presented herein (Table 1). In both cases, the values re-
ported by the authors [50, 51] for Vitex agnus-castus fruits
and Equisetum arvense stems, respectively, were signifi-
cantly inferior to our values, which means higher activity
TABLE 1 - Phenol and flavonoid contents (mg/g, dry weight), and antioxidant activities, lipoxygenase and acetylcholinesterase inhibition
activities of extracts of Moroccan plants, expressed as IC50 (mg/ml).
Plant Phenols* Flavonoids** TBARS ABTS DPPH Hydroxyl Chelating Lipoxygenase Acetylcholinesterase
Haloxylon scoparium 12.338±0.942f 4.500±0.215de 1.925±0.120a 1.018±0.079a 1.867±0.061a 0.3492±0.0040b 0.034±0.013h 1.911±0.030a 4.169±0.080a
Corrigiola tolephiifolia 14.593±0.942def 3.843±0.215e 1.154±0.120b 0.737±0.079ab 0.673±0.061b 0.1792±0.0040e 0.287±0.013b 1.523±0.030c -
Ammodaucus leuco-
trichus
12.947±0.942f 2.255±0.215f 2.254±0.120a 0.524±0.079bc 0.658±0.061b 0.1614±0.0040f 0.261±0.013bc 0.621±0.030f -
Chamaerops humilis 30.864±0.942ab 5.966±0.215c 2.163±0.120a 0.035±0.079e 0.035±0.061d 0.4220±0.0040a 0.217±0.013cde 0.616±0.030f -
Sideritis arborescens
(leaf) 26.806±0.942c 9.285±0.215a 1.822±0.120a 0.110±0.079de 0.104±0.061d 0.2226±0.0040d 0.256±0.013bcd 0.932±0.030d -
S. arborescens (stem) 13.625±0.942ef 2.076±0.215f 0.541±0.120cd 0.289±0.079cde 0.378±0.061c 0.2636±0.0040c 0.368±0.013a 1.908±0.030a -
Retama reatam 27.819±0.942bc 4.428±0.215de 1.054±0.120b 0.237±0.079cde 0.477±0.061bc 0.1438±0.0040g 0.134±0.013g 0.421±0.030g -
Ammi visnaga 15.107±0.942def 2.705±0.215f 0.871±0.120bc 0.268±0.079cde 0.129±0.061d 0.1828±0.0040e 0.214±0.013de 0.262±0.030h 2.126±0.080c
Viscum album 28.141±0.942abc 5.998±0.215c 0.575±0.120cd 0.038±0.079e 0.046±0.061d 0.0586±0.0040h 0.241±0.013bcd 0.236±0.030h 1.712±0.080d
Berberis vulgaris 16.923±0.942de 6.974±0.215b 0.426±0.120de 0.049±0.079e 0.111±0.06d 0.0061±0.0040i 0.188±0.013ef 0.266±0.030h 0.013±0.080e
Vitex agnus castus 17.133±0.942d 3.908±0.215e 1.145±0.120b 0.340±0.079cd 0.467±0.061bc - 0.266±0.013b 0.689±0.030b ND
Equisetum arvense 31.386±0.942a 4.885±0.215d 2.206±0.120a 0.065±0.079de 0.049±0.061d - 0.168±0.013fg 0.787±0.030e 3.134±0.080b
BHT
0.097±0.120e 0.004±0.079e 0.089±0.061d ND ND ND ND
Mannitol ND ND ND
0.0007±0.0040i ND ND ND
EDTA ND ND ND ND
0.061±0.013h ND ND
NDGA ND ND ND ND ND 0.020±0.030i ND
Galanthamine ND ND ND ND ND ND
0.003±0.080e
* Concentration in mg GAE (gallic acid equivalents)/g; ** concentration in mg QE (quercetin equivalents)/g; values in the same column followed by the same letter are not significantly different by
the Tukey’s multiple range test (p<0.05); data are the means of at least three replicates.
© by PSP Volume 23 – No 6. 2014 Fresenius Environmental Bulletin
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TABLE 2 - Review of the phenol contents found for the plants studied in the present work.
Plant Plant part used Phenols Tannins o-diphenols Flavonoids Anthocyanins References
Haloxylon scoparium (1) Leafy stems 110.92 mg GAE/g ND ND 38.90 mg CE/g ND [72]
Haloxylon scoparium (1) Aerial parts 4.34-37.31 mg GAE/g ND ND 0.004-12.3 mg RE/g ND [73]
Haloxylon scoparium (1) Aerial parts 108.41 mg/GAE/g ND ND 15.58 mg QE/g ND [42]
Corrigiola tolephiifolia (2) Aerial parts ND ND ND ND ND [74]
Ammodaucus leucotrichus (3) Aerial parts 46.77 mg GAE/g ND ND 15.48 mg CE/g ND [72]
Chamaerops humilis (4) Leaves 26.8 mg GAE/g* ND ND 38.1 mg CE/g* ND [55]
Sideritis arborescens (leaf) (5) - - - - - - -
Sideritis arborescens (stem)
(5)
- - - - - - -
Retama reatam (6) Roots-stems
Flowers
11.11-25.19 mg GAE/g
51.68 mg GAE/g
ND ND ND ND [75]
Retama reatam (6) Flower (essential oils) ND ND ND ND ND [76]
Retama reatam (6) Flowers 129.49-220.81 mg CE/g** 303.94-379.12 97 mg
CE/g**
ND 41.58-54.97 mg CE/g** ND [77]
Retama reatam (6) Leaves-seeds ND ND ND ND ND [78]
Retama reatam (6) Whole plant ND ND ND ND ND [79]
Ammi visnaga (7) Aerial parts ND ND - - ND [60]
Viscum album (8) Leaves and stems 114.57-134.18 mg GAE/g ND ND ND ND [52]
Viscum album (8) Leaves
Stems
31.32-200.51 18 mg
GAE/g
27.96-189.77 18 mg
GAE/g
ND ND ND ND [53]
Viscum album (8) Leaves
Stems
Hydrophilic: 0.44-0.65 mg
GAE/g
Lipophilic: 0.003-
0.006 mg GAE/g
Hydrophilic: 0.40-0.55 mg
GAE/g
Lipophilic:
0.002-0.015 mg GAE/g
ND ND ND ND [80]
Viscum album (8) Leaves ND ND ND ND ND [81]
Viscum album (8) Fruits ND ND ND ND ND [82]
Viscum album (8) Aerial parts 6.33 mg CAE/g ND ND 9.72 µg QE/g ND [64]
Viscum album (8) Whole plant ND ND ND ND ND [83]
Viscum album (8) Lectins ND ND ND ND ND [58]
)Viscum album (8) Aerial parts 19.43 mg GAE/ g ND ND ND ND [84]
Viscum album (8) Leaves 160-182 mg TAE/100 g ND ND ND ND [56]
Viscum album (8) Leaves, stems, fruits ND ND ND ND ND [35]
Viscum album (8) Leaves ND ND ND ND ND [57]
Viscum album (8) Plant material ND ND ND ND ND [37]
Berberis vulgaris (9) Root bark ND ND ND ND ND [65]
Berberis vulgaris (9) Fruits 2512-3629 mg GAE/L ND ND ND 506.7-803.6 mg
Cy-3-Glu/L
[54]
Berberis vulgaris (9) Root
Twigs
Leaves
10.34 mg GAE/g
12.53 mg GAE/g
52.54 mg GAE/g
ND ND 0.24 mg QE/g
0.50 mg QE/g
4.23 mg QE/g
ND [59]
Berberis vulgaris (9) Leaves, stems
Fruits
273.1.2 mg/g
178.1 mg/g
ND ND ND ND [69]
Berberis vulgaris (9) Leaves, fruits ND ND ND ND ND [85]
Vitex agnus castus (10) Leaves
Seeds
Roots
46.85 mg CAE/g
25.87 mg CAE/g
8.81 mg CAE/g
ND 43.44 mg CAE/g
18.42 mg CAE/g
6.45 mg CAE/g
42.29 mg CE/g
16.00 29 mg CE/g
2.92 29 mg CE/g
0.38 mg ME/g
0.60 mg ME/g
0.52 mg ME/g
[86]
Vitex agnus castus (10) Leaves
Fruits
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
[87]
Vitex agnus castus (10) Leaves 48.05 mg GAE/g ND ND 27.45 mg QE/g ND [88]
Vitex agnus castus (10) Aerial parts ND ND ND ND ND [89]
Vitex agnus castus (10) Fruits 21.73 µg GAE/g (hexane)-
112.46 µg GAE/g (water
ND ND
7.12 µg QE/g (ethyl acetate-
43.5 µg QE/g (dichloro-
methane)
ND [26]
Vitex agnus castus (10) Fruits ND ND ND ND ND [50]
Vitex agnus castus (10) Aerial parts ND ND ND ND ND [67]
Vitex agnus castus (10) Leaves
Fruits
123.9 mg GAE/g
114.5 mg GAE/g
ND ND Vitexin: 0.252%
Vitexin: 0.342%
ND [90]
Vitex agnus castus (10) Flowers, leaves and twigs ND ND ND Isoorientin
2’’-O-trans-
caffeoylisoorientin
6’’-O-trans-
caffeoylisoorientin
Luteolin-7-O-glucoside
ND [91]
Equisetum arvens (11) Leaves 20.49-182.80 mg GAE/g ND ND ND ND [44]
Equisetum arvens (11) Stems 355.80 mg GAE/g ND ND ND ND [46]
Equisetum arvens (11) Plant material ND ND ND 0.905 mg/g ND [39]
Equisetum arvens (11) Aerial parts 1.73-96.4 mGAE/g ND ND ND ND [43]
Equisetum arvens (11) Stems ND ND ND 4.89-135.01 mg RE/g ND [51]
Equisetum arvens (11) Stems 92 µmol ChlE/g ND ND ND ND [45]
Equisetum arvens (11) Stems ND ND ND ND ND [92]
Equisetum arvens (11) Aerial parts ND ND ND ND ND [ 61]
Equisetum arvens (11) Plant material ND ND ND ND ND [63]
AAE: ascorbic acid equivalents; Cy-3-Glu: cyanidin-3-glucoside; GAE: gallic acid equivalents; CE: catechin equivalents; RE: rutin equivalents; QE: quercetin equivalents; ME: malvidin equivalent;
TAE: tannic acid equivalent; ND: not determined; -: not found.
* The values of flavonoids are superior to those of total phenols according to the results of the authors. The sum of tannins and flavonoids is higher than the total phenols according to the results of the
authors. Letters in parenthesis correspond to the reference which will be cited in the following Review Tables. Numbers in parenthesis correspond to the name of the plant which will be cited in the
following Review Tables.
© by PSP Volume 23 – No 6. 2014 Fresenius Environmental Bulletin
6
TABLE 3 - Review of the capacity for preventing lipid peroxidation, inhibiting some enzymes and chelating activity found for the plants
studied in the present work.
Plant Plant part used β-carotene
bleaching test
Inhibition of lipid
peroxidation
(lipid source)
Levels of GSH
(glutathione)
Xanthine
oxidase
(inhibition)
Lipoxygenase
(inhibition)
Acetylcho-
linesterase
(inhibition)
Myeloperoxi-
dase-catalysed
guaiacol
oxidation
(inhibition)
Chelating
activity
Ref.
1 Leafy stems + (TLC) ND ND ND ND ND ND ND [72]
1 Aerial parts 23.69-39.02%
(100 µg/mL)
ND ND 1.85-26.11 %
(100 µg/mL)
ND ND ND ND [73]
1 Aerial parts ND ND ND ND ND ND ND ND [42]
2 Aerial parts ND ND ND ND ND ND ND ND [74]
3 Aerial parts + (TLC) ND ND ND ND ND ND ND [72]
4 Leaves ND ND ND ND ND ND ND ND [55]
5 (leaf) - - ND - - - - - -
5 (stem) - - ND - - - - - -
6 Roots-stems
Flowers
ND ND ND ND ND ND ND ND [75]
6 Flower (essential oils) ND ND ND ND ND ND ND ND [76]
6 Flowers ND 75.53-81.47% (linoleic
acid emulsion)
ND ND ND ND ND ND [77]
6 Leaves-seeds ND 0.078-0.250% (lipo-
somes)
ND ND ND ND ND ND [78]
6 Whole plant ND ND ND ND ND ND ND [79]
7 Aerial parts ND ND ND ND ND ND ND [60]
8 Leaves
stems
ND ND ND ND ND ND ND ND [52]
8 Leaves
Stems
ND ND ND ND ND ND ND ND [53]
8 Leaves
Stems
ND ND ND ND ND ND ND ND [80]
8 Leaves ND ND ND ND ND ND ND ND [81]
8 Fruits ND (MDA in peripheral
blood lymphocytes) +
ND ND ND ND ND ND [82]
8 Aerial parts ND ND ND ND ND ND ND 54.68% [83]
8 Whole plant ND ND ND ND ND ND ND ND [67]
8 Lectins ND TBARS (LLC-PK1
renal epithelial cells) +
ND ND ND ND ND ND [58]
8 Aerial parts 82.23% ND ND ND ND ND ND ND [84]
8 Leaves ND ND ND ND ND ND ND + [56]
8 Leaves
Stems
Fruits
ND TBARS:
98.7% (1.65 mg/ml)
(liver homogenate
Wister albino rats)
90.5% (1.65 mg/mL)
(liver homogenate
Wister albino rats)
89.9% (1.65 mg/ml)
(liver homogenate
Wister albino rats)
ND ND ND ND ND ND [35]
8 Leaves ND + Ferric thiocyanate
(linoleic acid)
+ TBA
ND ND ND ND ND ND [57]
8 Plant material ND + TBA (liver, kidney,
heart tissues)
+ (liver, kidney, heart
tissues)
ND ND ND ND ND [37]
9 Root bark ND ND ND ND ND ND ND ND [65]
9 Fruits ND ND ND ND ND ND ND ND [54]
9 Root
Twigs
Leaves
59.99%
73.00%
89.26%
ND ND ND ND ND ND ND [59]
9 Fruits ND + MDA ND + ND + + ND [69]
9 Leaves, fruits ND ND ND ND ND ND ND ND [85]
10 Leaves
Seeds
Roots
ND ND ND ND ND ND ND ND [86]
10 Leaves
Fruits
ND ND ND ND ND ND ND ND [87]
10 Leaves ND ND ND ND ND ND ND + [88]
10 Aerial parts ND ND ND ND ND ND ND ND [89]
10 Fruits 18.10% (ethyl
acetate)
(0.4 mg/mL)-
94.07% (water)
(2.0 mg/mL)
ND ND ND ND ND ND [26]’
10 Fruits ND IC50=14-125 µg/ml (rat
brain homogenate)
Casticin:
IC50=0.049 mM (rat
brain homogenate)
ND ND ND ND ND ND [50]
10 Aerial parts ND ND ND ND Artemetin: IC50=54.6 µM
Casticin: IC50=26.0 µM
3,3′-Dihydroxy-5,6,7,4'-
tetramethoxy fla-
vone: IC50>400 µM
Penduletin: IC50>400 µM
Methyl 4-
hydroxybenzo-
ate: IC50>400 µM
p-Hydroxybenzoic
acid: IC50=197.37 µM
ND ND ND [67]
© by PSP Volume 23 – No 6. 2014 Fresenius Environmental Bulletin
7
Methyl 3,4-
dihydroxybenzo-
ate: IC50>400 µM
5-Hydroxy-2-
methoxybenzoic
acid: IC50>400 µM
Vanillic
acid: IC50=85.59 µM
3,4-Dihydroxybenzoic
acid: IC50>400 µM
10 Leaves
Fruits
ND ND ND ND ND ND ND ND [90]
10 Flowers, leaves and
twigs
ND ND ND ND ND ND ND ND [91]
11 Leaves ND ND ND ND ND ND ND ND [44]
11 Stems ND ND ND ND ND ND ND ND [46]
11 Plant material ND ND ND ND ND ND ND ND [39]
11 Aerial parts ND ND ND ND ND ND ND ND [43]
11 Stems ND IC50=14.50-
>192.31 µg/mL
(liposomes)
ND ND ND ND ND ND [51]
11 Stems ND ND ND ND ND ND ND ND [45]
11 S tems ND + TBARS (brain of
Naïve Wistar rats)
ND ND ND ND ND ND [93]
11 Stems ND ND ND ND ND ND ND ND [61]
11 Plant material ND ND ND 50-79% ND ND ND ND [63]
MDA: malonaldehyde; ND: not determined; -: not found; TBA: thiobarbituric acid; TBARS: thiobarbituric acid reactive species; TLC: thin layer chromatography; +: positive activity
than the extracts of the present work. The lipidic source
and the parts of plant used were different which may
partly explain these differences. Unfortunately, there were
no references for the total phenol content in the extracts
which could help to clarify these differences. In E. ar-
vense extracts, Mimica-Dukic et al. [51] reported a range
of activities depending on the type of solvent used for the
extraction of bioactive compounds. The concentrations of
flavonoids found in these extracts were also different, and
the highest activity found in one extract was attributed to
the higher levels of flavonoids in the extract. This may
also explain the lower antioxidant activity of our extracts
of E. arvense (Table 1), since the content of flavonoids
found in the extracts was inferior to those reported by
Mimica-Dukic et al. [51] (Table 3), although we did not
find a correlation between phenol or flavonoid concentra-
tion and the capacity for preventing the lipid peroxidation
of egg yolk (Table 5).
3.2.2 Capacity for scavenging free radicals
The capacity for scavenging free radicals of extracts
was examined by three methods: the capacity for scaveng-
ing ABTS, DPPH and hydroxyl-free radicals (Table 1).
The extracts of Chamaerops humilis, Viscum album
and Berberis vulgaris presented the highest capacity for
scavenging ABTS free radicals. Such ability was not sig-
nificantly different from that of BHT, the positive control
(Table 1). These extracts were also good scavengers of
DPPH radicals along with the extracts of Sideritis arbores-
cens (leaves), Ammi visnaga and Equisetum arvense (Ta-
ble 1). Herein, all of these extracts presented a good anti-
oxidant capacity, with regard to the positive control (BHT)
(Table 1).
For Chamaerops humilis, references about the capac-
ity of extracts of this species for scavenging ABTS radi-
cals were not found (Table 4). For Viscum album [52, 53]
and Berberis vulgaris [54], ABTS scavenging ability was
presented as Trolox Equivalent but herein as IC50 value.
This fact does not permit to compare the results. For Vis-
cum album extracts, Vicaş et al. [52, 53] reported on the
importance of collection season, host trees from which
samples were harvested, and plant parts used. In B. vul-
garis fruits, Özgen et al. [54] showed that different fruit
accessions possessed diverse antioxidant abilities. In this
case, the authors found a correlation between total phe-
nols, flavonoids, and particularly, anthocyanins when ex-
amining the capacity of samples for scavenging free radi-
cals. In the present work, a correlation was also found
between the concentration of total phenols, flavonoids and
the capacity for scavenging ABTS free radicals (Table 5).
The capacity for scavenging DPPH of Chamaerops
humilis extracts was reported by Benahamed-Bouhafsou
[55], and the IC50 value found was 180.71 µg/ml (Table 4),
being higher than in our sample (35 µg/ml) (Table 1) and,
therefore, with lower activity. For Viscum album, several
authors [52, 53, 56, 57] assayed the capacity of their sam-
ples for scavenging the DPPH free radicals, but only Kim
et al. [58] presented their results as IC50 values for lectins,
closer to our results.
Different parts of Berberis vulgaris possess different
IC50 values according to the work of Končić et al. [59];
they observed that the leaf extracts were most active (IC50
value 65 µg/ml) (Table 4), close to B. vulgaris extract
obtained from the aerial parts herein (49 µg/ml) (Table 1).
According to the results reported by Bencheraiet et
al. [60], the aerial parts of Ammi visnaga had higher abil-
ity for scavenging DPPH radicals (8.77 µg/ml) than our
sample (0.129 µg/ml), which may partly be explained by
the different types of solvents used for the extraction and,
therefore, different types of compounds isolated. A great
difference was also detected between the activity found in
the current work for E. arvense extract (Table 1) and
those reported by other authors [46, 51] (Table 5), possi-
bly caused by the higher amounts of phenols and flavon-
oids found by these authors (Table 2) compared to our
© by PSP Volume 23 – No 6. 2014 Fresenius Environmental Bulletin
8
TABLE 4 - Review of the capacity for scavenging free radicals and reducing power found for the plants studied in the present work.
Plant Plant part
used
ABTS DPPH Hydroxyl Superoxide Nitric
oxide
ORAC Reducing
power
Scavenging H2O2 Ref.
1 Leafy stems ND + (TLC) (IC50=54.53 µg/ml) ND ND ND ND ND ND [72]
1 Aerial parts ND IC50=8.78-133.78 µg/ml ND ND ND ND 6.27-90.89%
(100 µg/mL)
IC50=11.24-53.18 µg/mL [73]
1 Aerial parts IC50=0.027 mg/ml IC50=0.044 mg/ml ND ND ND ND ND [42]
2 Aerial parts ND IC50=10.53-12.06 µg/mL ND ND ND ND ND ND [74]
3 Aerial parts ND + (TLC) (IC50=45.73 µg/ml) ND ND ND ND ND ND [72]
4 Leaves ND + (TLC);
IC50=180.71 µg/ml
ND ND ND ND ND ND [55]
5 (leaf) - - - - - - - - - -
5 (stem) - - - - - - - - - -
6 Roots-stems
Flowers
ND 4.20-14.06% (1000 mg/l)
11.96% (1000 mg/l)
ND ND ND ND ND 24.64% (1000 mg/L)
54.44% (1000 mg/L)
[75]
6 Flower
(essential
oils)
ND IC50=0.8 mg/ml ND ND ND ND ND ND [76]
6 Flowers ND IC50=400-550 µg/ml ND ND ND ND ND ND [77]
6 Leaves-seeds ND IC50=0.059-0.122% ND ND ND ND ND ND [78]
6 Whole plant ND 78.1-80.2% (100 µg/ml) ND ND ND ND ND ND [79]
7 Aerial parts ND IC50=8.77 µg/ml ND ND ND ND ND ND [60]
8 Leaves
stems
1.7 mM TE/g 10.97-77.19% ND ND ND 0.17-9.64 mM
TE/g
ND ND [52]
8 Leaves
Stems
215.28-678.72 mM
TE/g
209.59-577.94 72 mM
TE/g
2.22-70.19%
Without activity
ND ND ND 1.87-9.97 mM
TE/g
1.52-9.79 mM
TE/g
ND ND [53]
8
Leaves
Stems
ND ND ND ND ND FRAP:
Hydro-
philic:0.08-
0.14 AAE/g
Lipophilic:
0.003-
0.012 AAE/g
Hydro-
philic:0.13-
0.14 AAE/g
Lipophilic:
0.005-
0.012 AAE/g
ND [80]
8 Le aves ND ND ND FRAP: + ND [81]
8 Fr uits ND ND ND ND ND [ 82]
8 Aerial parts 7.20% 34.44% 16.66% 28.43% 0.10 Equiv
1 mM FeSO4
0.37% [64]
8 Whole plant ND ND ND 3-(4-acetoxy-3,5-
dimethoxyphenyl-
2-E-propenyl-β-
Dglu-
copyranoside:
IC50=211.69 µM
4’,5-dimethoxy-7-
hydroxyflavanone:
IC50=58.36 69 µM
ND ND ND ND [ 83]
8 Lectins IC50=42.6 µg/ml + + + ND ND ND [58]
8 Ae rial parts ND ND ND ND ND ND ND ND [84]
8 Le aves ND + ND ND ND ND ND ND [56]
8 Leaves,
stems, fruits
ND ND ND ND ND ND + phospho-
molybdenum
ND [35]
8 Le aves ND + ND ND ND ND + Ferric
thiocyanate
ND [57]
8 Pl ant material ND ND ND ND ND ND ND ND [37]
9 Root bark ND ND N-(p-trans-coumaroyl)-
tiramine: IC50>40 µg/ml
Cannabisin G:
IC50=2.7 µg/ml
(±)-lyoniresinol:
IC50=1.4 µg/ml
ND ND ND ND ND [65]
9 Fruits 41.1-49.3 TE mmol/L ND ND ND ND ND FRAP: 41.0-
57.4 TE
mmol/L
ND [54]
9 Root
Twigs
Leaves
ND IC50=1293 µg/ml
IC50=692 µg/ml
IC50=65 µg/ml
ND ND ND ND + ND [59]
9 Fr uits ND + ND ND ND ND ND ND [69]
9 Le aves, fruits ND + ND ND ND ND ND ND [85]
10 Leaves
Seeds
Roots
Anti-radical power:
178.5 µL/µg DPPH
ND ND ND ND ND ND [86]
10 Leaves
Fruits
0.27-2.5 mM Trolox
0.097-2.27 mM Trolox
ND ND ND ND ND ND ND [87]
10 Leaves ND ND ND ND ND ND + (CUPRAC) 93.5% [88]
10 Aerial parts ND Casticin 1 mM: 24.27%
Penduletin 1 mM: 48.75%
Methyl-3,4-dihydroxy
benzoate 1 mM: 89.34%
Vanillic acid 1 mM: 43.38%
3,4-dihydroxybenzoic acid
1 mM: 94.73%
ND ND [ 89]
10 Fruits ND 0.51% (essential oil)
(0.2 mg/mL)-82.72%
(water) (1 mg/mL)
ND ND ND ND Absorbances at
700 nm: 0.021
(hexane)
(0.4 mg/ml)-
0.751 (water)
1 mg/ml
ND [26]
10 Fruits ND IC50=68-3643 µg/mL
Casticin: without activity
ND ND ND ND ND ND [50]
10 Aerial parts ND ND ND ND ND ND ND ND [67]
© by PSP Volume 23 – No 6. 2014 Fresenius Environmental Bulletin
9
10 Leaves
Flowers
ND IC50=0.449 mg/mL
IC50=0.612 mg/mL)
ND ND ND ND ND ND [90]
10 Flowers,
leaves and
twigs
ND Isoorientin:
IC50=16.9 µg/mL
2’’-O-trans-
caffeoylisoorientin:
IC50=23.6 µg/mL
6’’-O-trans-
caffeoylisoorientin:
IC50=23.4 µg/mL
Luteolin-7-O-glucoside:
IC50=21.8 µg/mL
ND ND ND ND ND ND [91]
11 Leaves 292.75-1270.79 µM
TE/mg
ND ND ND ND ND ND [44]
11 Stems ND IC50=13.5 µg/mL ND ND ND ND FRAP:
28.7 mM
Fe(II)/g
ND [46]
11 Plant material ND ND 73.5% ND ND ND FRAP:
2.85*100 µM
Fe(II)
[39]
11 Aerial parts ND IC50=0.64-2.27 mg/g
Protocatechuic acid:
IC50=0.04*10-3 mg/g
Vanilic acid:
IC50=1.72 mg/g
Caffeic acid:
IC50=0.01*10-3 mg/g
Syring acid:
IC50=0.05*10-3 mg/g
(-)Epicatechin:
IC50=0.09*10-3 mg/g
p-Coumaric acid:
IC50>2.5 mg/g
Ferulic acid:
IC50=0.09*10-3 mg/g
Rutin: IC50=0.07*10-3 mg/g
IC50=0.74-3.29 mg/g
Protocatechuic acid:
IC50=0.05*10-3 mg/g
Vanilic acid:
IC50=2.08 mg/g
Caffeic acid:
IC50=0.02*10-3 mg/g
Syring acid:
IC50=0.07*10-3 mg/g
(-)Epicatechin:
IC50=1.02 mg/g
p-Coumaric acid:
IC50>2.5 mg/g
Ferulic acid:
IC50=1.21 mg/g
Rutin:
IC50=0.09*10-3 mg/g
ND ND ND ND ND [43]
11 Stems ND IC50=2.37-37.20 µg/mL ND ND IC50=90.07-
>333.33 µg/
mL
ND ND ND [51]
11 Stems ND ND ND ND ND ND 10487 µmol
TAE/g
(molybdate
ammonium)
ND [45]
11 Stems ND ND ND ND ND ND ND ND [92]
11 Aerial parts Onitin: IC50=35.8 µM
Onitin-9-O-glucoside:
IC50=>100 µM
Apigenin: IC50=>100 µM
Luteolin: IC50=22.7 µM
Kaempferol-3-O-glucoside:
IC50= >100 µM
Quercetin-3-O-glucoside:
IC50=91.8 >100 µM
Onitin:
IC50=35.3 µM
Onitin-9-O-
glucoside:
IC50=>100 µM
Apigenin:
IC50=>100 µM
Luteolin:
IC50=5.9 >100 µM
Kaempferol-3-O-
glucoside:
IC50=>100 >100 µ
M
Quercetin-3-O-
glucoside:
IC50=11.2 >100 µ
M
[61]
11 Plant material ND 20-49% 50-79% >80% ND ND ND ND [63]
ABTS: 2,2'-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid); CUPRAC: cupric reducing antioxidant capacity; DPPH: 2,2-diphenyl-1-picrylhydrazyl; FRAP: ferric reducing antioxidant power; ND:
not determined; -: not found; ORAC: oxygen ; TAE : α-tocopherol acetate equivalents; TE: Trolox equivalents; +: positive activity
samples (Table 1). In fact, our results showed the exis-
tence of a correlation between the capacity for scavenging
DPPH free radicals and the contents of phenols and fla-
vonoids (Table 5). In addition, other authors were able to
identify the components present in the extracts of E. ar-
vense with the best activity [43], namely, protocatechuic
acid, caffeic acid, syringic cacid, epicatechin, ferulic acid,
and rutin. However, the IC50 values found for these com-
pounds were significantly inferior to those found in the
extracts. The same authors also reported on the impor-
tance of extraction solvent to determine the content of
phenols and antioxidant activity. Onitin and luteolin were
two other compounds detected in extracts of E. arvense
by Oh et al. [61], with higher activity than some other
phenols identified in the same extract (glucosides of onitin,
kaempferol and quercetin, apigenin).
A strong correlation was found between the activities
obtained by DPPH and ABTS methods (Table 5), which
means that the mechanisms involved in both methods are
practically the same: electron transfer from the compo-
nents of the extracts to ABTS or DPPH radicals [62].
Two plant extracts did not present a capacity for scav-
enging hydroxyl radicals: Vitex agnus-castus and Equise-
tum arvense (Table 1). B. vulgaris extract with the lowest
IC50 value was closest to the positive control (mannitol)
(Table 1). The absence of activity of E. arvense extract is
in contrast to that reported by other authors [39, 43, 63].
Canadanović-Brunet et al. [43] also assayed some indi-
vidual components present in the extract of E. arvense,
and they concluded that protocatechuic acid, caffeic acid,
syringic acid and rutin presented the best activities, even
better than that of the extract.
V. album extract and its lectins also had capacity for
scavenging hydroxyl radicals as reported by Papuc et al.
[64] and Kim et al. [58], respectively. Cannabisin G and
lyoniresinol present in the root bark of B. vulgaris had also
such a capacity according to some authors [65] (Table 4).
© by PSP Volume 23 – No 6. 2014 Fresenius Environmental Bulletin
10
TABLE 5 - Pearson correlation coefficients among compounds and activities, and among the activities.
Phenol Flavonoid TBARS ABTS DPPH Hydroxyl Chelating Lipoxygenase Acetylcholinesterase
Phenol 1 0.623** - -0.804** -0.765** - -0.380* -
Flavonoid 0.623** 1 - -0.675** -0.597** -0.402* - -0.668**
TBARS - - 1 - - 0.551** - - 0.879**
ABTS -0.804** -0.675** - 1 0.936** - - 0.616** 0.700**
DPPH -0.765** -0.597** - 0.936** 1 - - 0.491* -
Hydroxyl - - 0.551** - - 1 - 0.691** 0.930**
Chelating - -0.402* - - - - 1 - -0.689**
Lipoxygenase -0.380* - - 0.616** 0.491** 0.691** - 1 0.725**
Acetylcholinesterase - -0.668** 0.879** 0.700** - 0.930** -0.689** 0.725** 1
–: Not significant; * correlation is significant at the P < 0.05 level; ** correlation is significant at the P < 0.01 level
As reported for TBARS, the capacity for scavenging
hydroxyl radicals did not correlate neither with phenols
nor flavonoids (Table 5).
3.2.3 Capacity for chelating metal ions
Haloxylon scoparium extract was the best for chelat-
ing metal ions in contrast to that of S. arborescens (stem
extract). The chelating activity of H. scoparium was as
good as the positive control (EDTA) (Table 1). This ability
was already reported by Boulanouar et al. [42] for ethano-
lic extracts of H. scoparium collected in Algeria, although
with lower activity. This property was also reported for V.
album [56, 64] (Table 3).
3.2.4 Capacity for inhibiting lipoxygenase
Lipoxygenase catalyses the addition of molecular
oxygen to fatty acids containing a cis,cis-1,4-pentadiene
system originating from unsaturated fatty acid hydroper-
oxides. Due to the production of these peroxides, com-
pounds which are able to inhibit that enzyme can be con-
sidered as antioxidants. At the same time, those products
are converted into others that play a key role in inflamma-
tory processes [66]. Therefore, such compounds, which
are able to inhibit this enzyme, also possess anti-
inflammatory properties.
The extracts obtained from A. visnaga, V. album and
B. vulgaris had the best capacity for inhibiting lipoxy-
genase, due to the lowest IC50 values found (Table 1). In
contrast, the extracts with the weakest ability included
those obtained from H. scoparium and S. arborescens
(stems) (Table 1). Despite de highest activity found for
those samples, they were significantly inferior to that
detected for the positive control (NDGA).
According to Choudhary et al. [67], the capacity of
Vitex agnus-castus extracts for inhibiting lipoxygenase is
due predominantly to two compounds, artemetin and
casticin (Table 3). For the other plants, references about
the inhibition of lipoxygenase were not found.
The inhibition of lipoxygenase promoted by the ex-
tracts correlated well with the capacity for scavenging all
free radicals assayed (ABTS, hydroxyl and DPPH)
(Table 5). Only phenol content correlated with the capac-
ity of extracts for inhibiting lipoxygenase. A positive
correlation was found between lipoxygenase inhibition
and acetylcholinesterase inhibition (Table 5).
3.2.5 Capacity for inhibiting acetylcholinesterase
Acetylcholine (ACh) is delivered in the synapses and
rapidly hydrolyzed into choline and acetate by acetylcho-
linesterase (AChE). The deficit of ACh causes diseases
that are treated with AChE inhibitors [68]. Only H. sco-
parium, A. visnaga, V. album, B. vulgaris and E. arvense
extracts had ability for inhibiting acetylcholinesterase
(Table 1). B. vulgaris extract was the most active among
the extracts studied whereas that of H. scoparium was the
worst (Table 1). This property has been already previ-
ously reported for B. vulgaris extracts [69], but only in
qualitative terms. For the remaining plants, not any in-
formation was found (Table 3).
Flavonoids may have an important role in the acetyl-
cholinesterase inhibition because a negative correlation
was found between the amount of flavonoids and the IC50
values (Table 5). Uriarte-Pueyo and Calvo [70] referred to
the AChE inhibitory activity of flavonoids which can be
potential natural compounds for treating Alzheimer’s
disease, since the therapy for this illness involves the
increasing of acetylcholine levels.
A very strong correlation was also found between the
AChE inhibition and the capacity for scavenging hy-
droxyl free radicals as well as the capacity for preventing
lipid peroxidation (Table 5). This correlation may strengthen
the results obtained by some authors [71] for ginger extracts.
Ginger has been reportedly used for the management or
treatment of Alzheimer's disease in folklore medicine;
according to these authors, a possible mechanism could
be through the inhibition of acetylcholinesterase activities
and prevention of lipid peroxidation in the brain.
4. CONCLUSION
Equisetum arvense and Sideritis arborescens (stems)
possessed the highest concentrations of total phenols and
flavonoids, respectively.
Among the extracts studied, Berberis vulgaris and
Viscum album were the most promising as antioxidants,
anti-inflammatory and acetylcholinesterase inhibitors.
© by PSP Volume 23 – No 6. 2014 Fresenius Environmental Bulletin
11
In some cases, the activities of B. vulgaris extracts
were not significantly different from those found for the
positive controls (e.g. capacity for scavenging free radi-
cals, and capacity for inhibiting AChE).
The capacity for scavenging ABTS and DPPH free
radicals of V. album and Chamaerops humilis extracts
were also not significantly different from those of the
positive controls. Viscum album extract had also an im-
portant capacity for scavenging hydroxyl radicals.
The capacity of the samples for scavenging DPPH
and ABTS are mainly due to the phenol and flavonoid
contents, whereas the inhibitions of lipoxygenase and
AChE are mainly due to the phenol and flavonoid con-
tents, respectively, and also due to the correlations ob-
served between these variables.
Those properties, observed for B. vulgaris, V. album
and C. humilis, can constitute a good source of natural
antioxidants. In addition, due to the correlation between
flavonoid content with antioxidant and AChE inhibitory
activities could make this group of compounds to be use-
ful for treatment of Alzheimer’s disease as well as those
illnesses with cognitive decline and mental deterioration
symptoms, in which the increase of ACh levels is the
determinant.
The authors have declared no conflict of interest.
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Received: September 05, 2013
Accepted: December 02, 2013
CORRESPONDING AUTHOR
Maria da Graça Costa Miguel
Universidade do Algarve
Faculdade de Ciências e Tecnologia
Departamento de Química e Farmácia
Instituto de Biotecnologia e Bioengenharia
Centro Biotecnologia Vegetal
Campus de Gambelas
8005-139 Faro
PORTUGAL
E-mail: mgmiguel@ualg.pt
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