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Abstract

Antioxidants are tremendously important substances that possess the ability to protect the body from damage caused by free radicals induced oxidative stress. This study aims to investigate the antioxidant effect of hawthorn (Crataegus monogyna) from the Mid-Atlas Mountains of Morocco as a potential source of new bioactive natural compounds. Hawthorn is a medicinal plant widely used in phytotherapy for the treatment of many cardiovascular diseases. In this study, flowers, leaves, ripe and unripe fruits were analyzed. The antioxidant activity was measured by the 2,2-diphenyl-1-picrylhydrazyl(DPPH) free radical scavenging method. Then, Folin-Denis and aluminum chloride colorimetric assays were used to determine total polyphenol and total flavonoid contents of the plant extracts, respectively. The results obtained showed that all the plant parts studied expressed important antioxidant properties. Unripe fruits and flowers revealed the highest antioxidant activity with IC50 values of 7.3 and 8.3 μg/ml, respectively. Total polyphenol content in different plant parts ranged from 105.1 to 280.4 µg Gallic Acid Equivalent /100 mg Extract and total flavonoid from 4.7 to 70.8 µg Quercetin Equivalent/100 mg Extract. Antioxidant activity presented a significant correlation with total polyphenol content. These results indicate that C. monogyna extracts exhibit an important antioxidant activity and thus can present a great potential as a source of natural antioxidants.
Academia Journal of Medicinal Plants 7(2): 030-035, February 2019
DOI: 10.15413/ajmp.2019.0100
ISSN: 2315-7720
©2019 Academia Publishing
Research Paper
Antioxidant activity of hawthorn (Crataegus monogyna) from Morocco
Accepted 10th January, 2019
ABSTRACT
Antioxidants are tremendously important substances that possess the ability to
protect the body from damage caused by free radicals induced oxidative stress.
This study aims to investigate the antioxidant effect of hawthorn (Crataegus
monogyna) from the Mid-Atlas Mountains of Morocco as a potential source of new
bioactive natural compounds. Hawthorn is a medicinal plant widely used in
phytotherapy for the treatment of many cardiovascular diseases. In this study,
flowers, leaves, ripe and unripe fruits were analyzed. The antioxidant activity was
measured by the 2,2-diphenyl-1-picrylhydrazyl(DPPH) free radical scavenging
method. Then, FolinDenis and aluminum chloride colorimetric assays were used
to determine total polyphenol and total flavonoid contents of the plant extracts,
respectively. The results obtained showed that all the plant parts studied
expressed important antioxidant properties. Unripe fruits and flowers revealed
the highest antioxidant activity with IC50 values of 7.3 and 8.3 μg/ml, respectively.
Total polyphenol content in different plant parts ranged from 105.1 to 280.4 µg
Gallic Acid Equivalent /100 mg Extract and total flavonoid from 4.7 to 70.8 µg
Quercetin Equivalent/100 mg Extract. Antioxidant activity presented a significant
correlation with total polyphenol content. These results indicate that C.
monogyna extracts exhibit an important antioxidant activity and thus can present
a great potential as a source of natural antioxidants.
Key words: C. monogyna, total polyphenol content, total flavonoid content,
antioxidant activity.
INTRODUCTION
Free radicals and their precursors are parts of a reactive
chemical family named reactive oxygen species (ROS)
which are produced constantly by the human body during
its metabolism. ROS have fundamental and positive roles in
some physiological functions such as production of energy
in vivo systems, regulation of cell growth, inter or intra
cellular signal transfer, phagocytosis and synthesis of
important biological compounds (Halliwell, 1991; Keser et
al., 2012). Normally, the rates of generation and
elimination of reactive oxygen species are in equilibrium.
However, an oxidative stress may occur, resulting from a
disequilibrium between pro-oxidant sources of radicals
and antioxidant systems. The main source of free radicals is
endogenous. These radicals are produced from enzymatic
reactions mainly related to breathing and defense
functions. Other exogenous factors may also contribute to
their formation such as UV radiation, Ȣ or X-rays, smoking,
alcohol, prolonged exposure to the sun and intense
physical effort (Pham-Huy et al., 2008; Birben et al., 2012).
Free radicals initiate chain oxidation reactions that have
a detrimental action on the body. All tissues and all their
components can be affected by oxidative stress (lipids,
proteins, carbohydrates and even DNA). Free radicals are
implicated in more than one hundred disorders in humans
(Pourmorad et al., 2006). They are reported to be involved
in triggering several diseases such as cancer, diabetes,
rheumatism, amyotrophic lateral sclerosis, acute
respiratory distress syndrome, pulmonary edema,
Hakima Bahri1,3*, Chaymae Benkirane1,3
and Bouchra Tazi2,3
1Laboratory of Genetic Resources and
Plant Breeding,
EcoleNationaled’Agriculture de Meknes,
Meknes, Morocco.
2Laboratory of Chemistry, Department of
Basic Sciences,
EcoleNationaled’Agriculture de Meknes,
Meknes, Morocco.
3Km 10, Route HajKaddour, BP S-40
Meknes 50000, Morocco.
*Corresponding author. E-mail:
hbahri@enameknes.ac.ma. Tel: +212 661
482 344.
Academia Journal of Medicinal Plants; Bahri et al. 031
restenosis, AIDS, cardiovascular diseases,
neurodegenerative diseases and accelerated aging
(Montagnier et al., 1998; Sohal et al., 2002). Following an
oxidative attack, the body can deploy two strategies, (i)
active detoxification which relies primarily on enzymes
(Superoxide Dismutase (SOD), Catalase, Glutathione
Peroxidase, etc…) and (ii) passive detoxification which
includes all non-enzymatic antioxidants that can neutralize
free radicals (Halliwell, 1991). Recently, many studies have
focused on the high toxicity of synthetic antioxidants and
the potential health problems that may arise from their
long-term use, such as tetragenic, mutagenic and
carcinogenic effects (Chavéron, 1999).
Medicinal plants have played a vital role in protecting
human health for thousands of years through their richness
in bioactive compounds. Natural phytochemicals from
plants have been receiving increased interest from
researchers and consumers for their health benefits and
particularly for their lack of toxicity as compared with
synthetic molecules. Hawthorn (Crataegus monogyna) is a
shrub or small tree belonging to the Rosaceae family and
wide spreading in almost all temperate zones of the
northern hemisphere (Bruneton, 2009). Its flowers, leaves
and fruits are used in phytotherapy for the treatment of
many health problems. It is commonly known for its
cardiovascular, sedative, antioxidant and antibacterial
properties (Nabavi et al., 2015; Walker et al., 2002; Bouzid
et al., 2011; Benmalek et al., 2013).
This study aims to determine the polyphenols and
flavonoids contents of Moroccan hawthorn (C. monogyna)
and to investigate its antioxidant activity as a potential
source of new bioactive natural compounds.
MATERIALS AND METHODS
Plant material and Study area
Samples of C. monogyna were collected from the Middle
Atlas mountain area East of the city of Azrou (Latitude N
33.42°; Longitude W 5.16°; Altitude 1680 m). This areas
hosts a great diversity of spontaneous plant species
collected by the local population for their medicinal vertus.
The plant samples were collected on 2016/2017 season,
from all sides of the tree, on a chronological sequence
according to the organ concerned. Leaves and flowers are
collected at full bloom (mid- may), while immature fruits
(green in color) and ripened fruits(red in color) are
collected in early autumn (September) and late autumn
(November), respectively. Plant samples were air dried in
the shade on a laboratory bench, then powdered and
passed through a 1 mm sieve.
Plant extracts
Extraction was carried out by maceration in methanol, and
extracts were evaporated at 35C under reduced pressure,
dissolved in methanol at 10 mg/ml and stored at 4C for
subsequent use in colorimetric assay and antioxidant
activity.
Total polyphenols and flavonoids
Polyphenols
Determination of total polyphenols was carried out
according to Li et al. (2007) using Folin Denis reagent
instead of Folin Ciocalteu. 75 ml of distilled water, 10 g of
sodium tungstate, 2 g of phosphomolybdic acid and 15 ml
of Phosphoric Acid were mixed and boiled for 2 h. After
cooling, the mixture was completed to 100 ml with
deionised water. 200 μl of each hawthorn extract solution
was mixed with 1 ml of the Folin-Denis solution diluted
ten-fold. After 4 min, 800 μl of sodium carbonate (Na2CO3)
(75 mg/ml in distilled water) was added to the solution
and incubated for 2 h in the dark. Then, polyphenol
absorbance was determined at 765 nm using a Shimadzu
spectrophotometer. Gallic acid solutions ranging from 0 to
200 μg/ml were prepared and used to establish a standard
calibration curve..
Flavonoids
Aluminum Chloride (AlCl3) method was used to quantify
flavonoids according to the method used by Bahorun et al.
(1996). Hawthorn extract solutions, ranging from 0 to 35
μg/ml, were prepared and mixed with AlCl3 (2% in
methanol) (V/V). After 10 min, the absorbance was
measured at 430 nm. A calibration curve was established
with quercetin (0 - 35 μg/ml).
Scavenging of DPPH radicals
Antioxidant power of methanolic extracts of flowers, leaves
and fruits of C. monogyna against DPPH radical was
evaluated by spectrophotometry using the method
described by Selles et al. (2012). A series of dilutions were
performed in order to obtain concentrations ranging from
5 μg/ml to 0.4 mg/ml for hawthorn extracts and from 1
μg/ml to 0.4 mg/ml for ascorbic acid. A methanolic
solution of DPPH 0.8mM was prepared and 0.25 ml of this
solution was added to 3.75 ml of hawthorn extract
solutions. The resulting mixtures were kept in the dark at
room temperature for 30 min. Then absorbance was
measured at 517 nm. The results were compared with the
negative control (for which no plant extract was added).
Ascorbic acid was used as a reference anti-oxydant.
The results were expressed as percent inhibition of
DPPH radical using the formula:
Academia Journal of Medicinal Plants; Bahri et al. 032
Table 1: Polyphenols and flavonoids contents and antioxidant activity of Crataegusmonogynaplant parts(mean ± SD; n=3 , and p <0.05).
Parameter
Extraction yield
(g/100g dry weight)
Polyphenols content
(µg EqGA/mg extract)
Flavonoids content
(µg EqQ/mg extract)
Flower
24.68 ± 1.81 b
244.26 ± 10.68 b
40.78 ± 2.02 a
Leaf
13.79 ± 1.28 c
196.49 ± 04.57 c
38.08 ± 0.73 a
Ripened fruit
34.31 ± 0.91 a
105.10 ± 02.09 d
04.69 ± 0.18 c
Immature fruit
10.74 ± 1.01 c
280.36 ± 02.50 a
14.56 ± 0.46 b
Ascorbic acid
With: Abs Control=Absorbance of the negative control, Abs
Test=Absorbance of the test sample.
The percent inhibition of DPPH radical was plotted
against extract concentration (log scale) and the IC-50
values were determined graphically using GraphPad Prism
8.
Chemical reagents
DPPH (2-2 Diphenyl-1-picylhydrazyl), Quercetin (C15H10O7)
and Methanol (CH3OH) were purchased from Sigma-
Aldrish. Sodium Tungstate-2hydrate (Na2WO4,2H2O) and
Sodium Carbonate (Na2CO3) were purchased from
Polysciences. Gallic Acid (C7H6O5) was purchased from
Fluka. Phosphomolybdic Acid × Hydrate (H3PMo12O40xH2O)
was purchased from Panreac. Ascorbic Acid (C6H8O6) was
purchased from Fisher Scientific. Phosphoric Acid was
purchased from Gerraw. Aluminium Chloride was
purchased from Riedel-deHaën.
Statistical analysis
All tests were conducted in triplicates; the results were
expressed as mean ± standard deviation. A multiple
comparison of means was performed using Tukey-test with
a probability level of 0.05. Correlations between different
parameters were computed as Pearson’s correlation
coefficient (r). Statistical analyzes were performed using
SPSS software version 20.0.
RESULTS
Total polyphenols
Total polyphenol content was derived using the Gallic acid
calibration curve and the absorbance value of each test
extract. The results obtained showed that C. monogyna is
rich in polyphenols with significant differences among
plant parts (Table 1). Immature fruits contained the
highest concentration (280.36 μg GAE/mg extract),
followed by flowers (244.26 μg GAE/mg extract), then
leaves (196.49 μg GAE/mg extract), while ripened fruits
registered the lowest value (105.10 μg GAE/mg extract).
Total flavonoids
Total flavonoid content, derived using the Quercetin
calibration curve and the absorbance value of each test
extract, showed significant differences among plant parts
(Table 1). Flowers and leaves presented the highest values
(40.78 and 38.08 μg QE/mg extract respectively), followed
by immature fruits (14.56 μg QE/mg extract). Mature fruits
presented the lowest value (4.69 μg QE/mg extract).
Scavenging of DPPH radicals
The principle of analyzing antioxidant activity is based on
the color change of diphenyl-picrylhydrazyl (DPPH)
solution from purple to yellow. The intensity of the color
change is proportional to the amount of antioxidants.
Figure 1 shows the antioxidant capacity of methanolic
extracts of hawthorn plant parts. The antioxidant activity
profiles obtained presented a dose-dependent activity.
Inhibition of DPPH radical increased with increasing
concentrations of plant extracts. Inhibition percentages
were stabilized at varying concentrations according to the
organ studied (0.1 mg/ml for immature fruit, 0.05 mg/ml
for flower, leaf and ripened fruit and 0.005 mg/ml for
ascorbic acid). Immature fruit reached the highest percent
inhibition of DPPH radicals (89%) followed by ripened
fruit, flower and leaf (83%). However, the maximum DPPH
radical inhibition of ascorbic acid (76%) was relatively
lower as compared with that exhibited by hawthorn plant
parts.
The IC50 values were obtained graphically using
GraphPad Prism 8 (Table 1).These values are defined as
the inhibitory extract concentration necessary to decrease
by 50% the initial concentration of DPPH and are
expressed in µg/ml. The results obtained showed
significant differences among different plant parts, with
IC50 values ranging from 7.27 to 23.67 μg/ml against 2.83
μg/ml for ascorbic acid. Immature fruits and flowers
% inhibition = (Abs Control Abs Test)
Abs Control 100
Academia Journal of Medicinal Plants; Bahri et al. 033
Figure 1: Percent inhibition of DPPH radical of Crataegus monogyna plant parts and ascorbic acid.
exhibited the lowest IC-50 values (7.27 and 8.27 μg/ml
respectively), followed by leaves (15.47 μg/ml) and then
ripened fruit (23.67 μg/ml).
Polyphenol content of different plant parts presented a
strong and significant correlation with their corresponding
antioxidant activity (r = 0.97), while flavonoid content was
moderately correlated (r = 0.49). This clearly shows that
antioxidant potential of hawthorn extracts is mainly
associated with its polyphenols content.
DISCUSSION
Polyphenols and flavonoids contents
Plants produce accumulate a large variety of secondary
metabolites along their growth and development cycle.
These compounds have potential roles in signalization and
protection against different biotic or abiotic stresses and
represent adaptive traits that allow plants to survive in
their environment. Polyphenols are an important class of
secondary metabolites found ubiquitously in plants.
Our findings showed that C. monogyna from the mid
Atlas Mountains of Morocco contains important amounts of
polyphenols in its reproductive plant parts, with
differential distribution among the different organs. In fact,
several authors (N’Guessan, 2011; Mraihi et al., 2013;
Simirgiotis, 2013) have reported unequal distribution of
polyphenols in different organs of a plant.
A study conducted on C. monogyna collected from
Portugal (Barros et al., 2011) showed that immature fruits
are the richest in polyphenols, followed by flowers and
finally ripened fruits, a trend similar to our findings. The
levels of polyphenols content reported were much higher,
especially in the case of immature fruit (701.65 μg GAE/mg
extract). Similarly, another study on C. monogyna collected
from France (Bahorun et al., 1994) showed that foliar and
reproductive organs were rich in polyphenols. Their
results follow perfectly the same trend as those of our
study, with a maximum polyphenols content for immature
fruits. However, Bouzid et al. (2011), working on C.
monogyna ripened fruits from Algeria, reported lower
polyphenol contents (21.72 μg GAE/mg extract) as
compared with the finding of the present study. The high
content of polyphenols reported specifically for immature
fruits by all studies may be the strategy of the plant to
discourage herbivores, thus avoiding early dispersal of
immature seeds as reported by Barros et al. (2011).
Concerning flavonoids, our results showed that flowers
and leaves are the richest parts of the plant, followed by
fruits. Flavonoid contents obtained in the present study are
very close to those of Bouzid et al. (2011), who reported
that methanolic extract of ripened hawthorn fruits from
Algeria recorded a flavonoids content of 3.2 μg QE/mg
extract. The same trend is also reflected in the results of
Bahorun et al. (1994) who expressed their results in terms
of Vitexin and Hyperoside equivalent. Other studies also
confirm that polyphenols and flavonoids contents of
Academia Journal of Medicinal Plants; Bahri et al. 034
immature fruits are much higher than those of mature
fruits. This could be explained by their use as antioxidants
along fruit maturity, thus resulting in a phenolic content
decrease in advanced maturity stages (Simirgiotis, 2013;
Barros et al., 2011).
Several factors can affect the content of phenolic
compounds. The literature highlights the influence of both
intrinsic and extrinsic factors as well as their interaction.
Some studies suggested that the phenolic content of plants
is influenced mainly by genetic factors (Atanasova and
Ribarova, 2009; Bouzid et al., 2011; Kostić et al., 2012).
Extrinsic factors may also influence phenylpropanoid
metabolism (kostić et al., 2012), such as environment and
its characteristics (altitude, temperature, light, soil nutrient
content, etc.). Indeed, Kirakosyan et al. (2003) showed that
hawthorn plant extracts subjected to drought and cold
stress did not only give higher yields of polyphenolic
compounds but also have greater antioxidant capacity as
compared with control plants. In addition, several authors
linked the variation of phenolic content with the intensity
of the sun (Urbonaviciute et al., 2006; Atanasova and
Ribarova, 2009), and concluded that solar radiation can
induce their biosynthesis. Furthermore, the date of harvest,
the maturity of the plant, the spatial distribution of the
sample, and storage conditions may also exert an
important effect on the observed variations (Proestos and
Komaitis, 2008; Bouzid et al., 2011; kostić et al., 2012;
Rodriguez et al., 2012; Bahorun et al., 1994; Urbonaviciute
et al., 2006). In addition, the extraction methods adopted
and the solvents used also exert an important effect on the
yield of phenolic compounds (Ignat et al., 2013; Tahirović
and Bašić, 2014; Bouzid et al., 2011).
Antioxidant activity
Various hawthorn organs have been described in the
literature as antioxidants in several studies. In terms of IC50
values, a study conducted by Simirgiotis (2013) on
different plant part of C. monogyna reported that: (i)
samples with IC50 values less than 50 µg/ml possess high
antioxidant activity, (ii) those with IC50 values ranging from
50-100 µg/ml are considered as intermediate antioxidant
activity, (iii) while samples with IC50 value greater than
200 µg/ml are considered as no relevant antioxidant
activity.
According to this classification, all hawthorn plant parts
expressed a high antioxidant activity. Since IC50 value is
inversely related to antioxidant capacity, the relative
comparison of the various organs activity allows
concluding that immature fruits and flowers expressed the
highest antioxidant activity (IC-50 of 6.42 and 6.78 µg/ml
respectively); leaves presented an intermediate activity
(11.02 µg/ml), whereas ripened fruits were the lowest
(17.66 µg/ml). A similar trend was reported by Bahorun et
al. (1994) and Barros et al. (2011). Our study revealed
greater DPPH scavenging activities as compared with
hawthorn fruits collected from Serbia (IC50 = 52.04 μg/ml,
Tadić et al., 2008). In contrast, ripened fruits (IC50 = 3.61
μg/ml) and leafy branches (IC50 = 3.34 μg/ml) of chilean C.
monogyna presented a higher antioxidant activity as
compared with the results of our study (Simirgiotis, 2013).
Our results showed that Hawthorn flowers and unripe
fruits exhibited a relatively higher maximum DPPH radical
inhibition activity as compared with that of ascorbic acid
used as a reference antioxydant. This increased intensity
could be attributed to potential synergetic effects among
different compounds contained in the extract
(Bernatonienė et al., 2008; Rodrigues et al., 2012; Ignat et
al., 2013; Simirgiotis, 2013). In addition, the antioxidant
activity of hawthorn extracts presented a strong
correlation with polyphenol content (r = 0.973). This is in
agreement with the reports of other researchers (Tahirović
and Bašić, 2014; Mraihi et al., 2013; Bahorun et al., 1994).
Conclusion
C. monogyna collected from Morocco showed a high DPPH
anti-radical scavenging activity, especially immature fruits
and flowers. These findings substantiate the traditional
uses of C. monogyna in treating various disorders and
increase its interest for potential use as a natural source of
antioxidants.
ACKNOWLEDGMENT
The authors wish to thank the Ecole Nationaled’
Agriculture de Meknes, Morocco for providing the
necessary facilities to carry out this study.
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Cite this article as:
Bahri H, Benkirane C, Tazi B (2018). Antioxidant activity of
hawthorn (Crataegus monogyna) from Morocco. Acad. J. Med.
Plants. 7(2): 030-035.
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http://www.academiapublishing.org/ajmp
... Anti-oxidant activities of phytochemical compounds from a variety of plants are considered to have protective and Academia Journal of Medicinal Plants; Bahri et al. 270 curative effects on many health ailments. Phenolic compounds, particularly the flavonoids, have been established to possess a wide range of biochemical activities, including antioxidant, antimutagenic, anticarcinogenic, antimicrobial, antiarthritic, protein-kinase inhibition, immune-stimulant, etc. (Bahri et al., 2018;Zaidi, 2013;Bendjeddou et al., 2003;Ren et al., 2003;Dalila et al., 2010;Pahuja et al., 2012;Sulaiman and Balachandran, 2012;Jalayer-Naderi et al., 2016;Kumar, 2017;Tungmunnithum et al., 2018). Cancer is a major health concern, and is largely due to lifestyle and environmental factors (Gonzalez and Riboli, 2010). ...
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