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Chemical composition, antioxidant and antibacterial activity of Crataegus monogyna leaves’ extracts



Crataegus monogyna is an important plant of the Rosaceae family, widely used in traditional medicine to treat various conditions such as cardiovascular diseases, cancer, diabetes, asthma, and nephritis. The aim of the current study was to assess the chemical composition, antioxidant, and antibacterial activity of leaves’ extracts against Bacillus cereus, Staphylococcus aureus, Escherichia coli, and Pseudomonas aeruginosa. The total amounts of polyphenols and flavonoids contained in the dry extracts of plants were estimated by colorimetric methods. DPPH assay was utilized to measure the antioxidant activity of C. monogyna. The phytochemical compounds were determined through HPLC technique, and the minimum inhibitory concentration (MIC) of ethanol extract was performed using the broth dilution method. The ethanol extract represented the richest extract in polyphenol with 473.4 mg GAE g⁻¹ and flavonoids 80.9 mg CE g⁻¹ and showed considerable antioxidant potential IC50 =22.50 µg/ml. The antibacterial susceptibility test against Staphylococcus aureus 0.512 mg/mL.
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Natural Product Research
Formerly Natural Product Letters
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Chemical composition, antioxidant and
antibacterial activity of Crataegus monogyna
leaves’ extracts
Fouzia Belabdelli, Nabila Bekhti, Alessandra Piras, Fouad Mekhalef
Benhafsa, Mokhtari Ilham, Selka Adil & Lazzaz Anes
To cite this article: Fouzia Belabdelli, Nabila Bekhti, Alessandra Piras, Fouad Mekhalef Benhafsa,
Mokhtari Ilham, Selka Adil & Lazzaz Anes (2021): Chemical composition, antioxidant and
antibacterial activity of Crataegus�monogyna leaves’ extracts, Natural Product Research, DOI:
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Chemical composition, antioxidant and antibacterial
activity of Crataegus monogyna leavesextracts
Fouzia Belabdelli
, Nabila Bekhti
, Alessandra Piras
Fouad Mekhalef Benhafsa
, Mokhtari Ilham
, Selka Adil
and Lazzaz Anes
Laboratory of Theoretical Chemistry of Bio & Nano-systems, Faculty of Exact Sciences, Djillali Liabes
University of Sidi Bel Abbes, Sidi Bel Abb
es, Algeria;
Department of Pharmacy, Faculty of Medicine,
Djillali Liabes University of Sidi Bel Abbes, Sidi Bel Abbes, Algeria;
Department of Process
Engineering, Faculty of Science and Technology, Mustapha Stambouli University of Mascara, Route
Mamounia, Mascara, Algeria;
Department of Chemical and Geological Sciences, University of
Cagliari, Cittadella Universitaria, Monserrato, Cagliari, Italy;
Center for Scientific and Technical
Research in Physico-Chemical Analysis (CRAPC), Algiers, Algeria;
Department of Pharmacy, Faculty of
Medicine, Abou Bakr Belkaïd University of Tlemcen, Tlemcen, Algeria
Crataegus monogyna is an important plant of the Rosaceae family,
widely used in traditional medicine to treat various conditions
such as cardiovascular diseases, cancer, diabetes, asthma, and
nephritis. The aim of the current study was to assess the chemical
composition, antioxidant, and antibacterial activity of leaves
extracts against Bacillus cereus, Staphylococcus aureus, Escherichia
coli, and Pseudomonas aeruginosa. The total amounts of polyphe-
nols and flavonoids contained in the dry extracts of plants were
estimated by colorimetric methods. DPPH assay was utilized to
measure the antioxidant activity of C. monogyna. The phytochem-
ical compounds were determined through HPLC technique, and
the minimum inhibitory concentration (MIC) of ethanol extract
was performed using the broth dilution method. The ethanol
extract represented the richest extract in polyphenol with
473.4 mg GAE g
and flavonoids 80.9 mg CE g
and showed
considerable antioxidant potential IC
¼22.50 mg/ml. The
antibacterial susceptibility test against Staphylococcus aureus
0.512 mg/mL.
Received 10 April 2021
Accepted 10 July 2021
Crataegus monogyna; HPLC;
DPPH assay; MIC
CONTACT Nabila Bekhti
Supplemental data for this article can be accessed online at
ß2021 Informa UK Limited, trading as Taylor & Francis Group
1. Introduction
Crataegus monogyna species are commonly used in traditional medicine. This medi-
cinal plant constitutes a valuable source of bioactive phytochemicals or bio-nutrients.
Different hawthorn species have been found to exert various effects in all populations.
Those species are usually used in association with other drugs as antispasmodic, diur-
etic, febrifuge, hypertensive, analgesic, sedative, and antidepressant agents (Kirakosyan
et al. 2003; Guo et al. 2008; Zhao et al. 2012; Ku et al. 2015; Li et al. 2015). As shown
by Popovic-Milenkovic et al. 2014,Crataegus monogyna leaves and flowers contained a
high abundance of flavonoids and displayed a significant biological effect (Mudge
et al. 2016). C. monogyna is a species recognized by the European Pharmacopoeia
(2007). Whereas Crataegus monogyna has demonstrated a high antioxidant activity
attributed to flavonoids and procyanidins (Ozyurek et al., 2012).
The investigation of medicinal plants from temperate regions grasped the interest
of both botanists and pharmacologists. In addition to the scientific value, such investi-
gation can provide valuable information on general trends in research on medicinal
plants and on the practical possibilities of their use in modern pharmacopeia. The
therapeutic properties of these plants are due to the presence of natural bioactive
compounds, hawthorn fruits, and leave derivatives (NNHPD 2013).
This plant can grow in several types of soil, especially in glades and forests.
Although it prefers acidic and dry soils, the plant can also grow in neutral and alkaline
soils. This species is well represented in the global temperate zones. In Algeria, the
plant is more frequently found in the forests and the maquis of the Tellian Atlas.
Several studies have investigated the chemical composition and the antioxidant activ-
ity of Crataegus species and different organs of the plant (leaves, flowers, and fruits) of
the fruit Crataegus monogyna from different origins (Bernatonien _
e et al. 2008; Bouzi
et al. 2011). The flavonoids identified in flowers of Mexican hawthorns were the
quercetin 3-O-glucoside, quercetin 3-0-rhamnoside, quercetin 3-O-rhamnosyl-(1!6)-
glucoside, and quercetin 3-O-rhamnosyl-(1!2)-[rhamnosyl-(1!6)] glucoside (Garc
Mateos et al. 2013). Fifteen Crataegus L. species of leaves and flowers in Eurasia and
North America identified chlorogenic acid, hyperoside, Vitexin 2-rhamnoside, vitexin 2-
O-rhamnoside, vitexin, caffeic acid, and triterpenes oleanolic acid, ursolic acid
(Kateryna Khokhlova et al. 2020). Four flavonoids were quantified (naringenin, hypero-
side, rutin, and vitexin-20-O-rhamnoside) and chlorogenic acid in leaf extracts of four
Crataegus species (C. monogyna,C. laevigata,C. douglasti, and C. okanaganensis) (Lund
et al. 2020). Five flavonoids quantified in hawthorn (C. douglasii and C. laevigata
leaves; C. monogyna leaves and flowers) vitexin2-O-rhamnoside, vitexin, isovitexin,
rutin and hyperoside (Mudge et al. 2016).epicatechin] and flavonoid (vitexin 20-O-
rhamnoside, acetylvitexin 20-O-rhamnoside, and hyperoside) (Kirakosyan et al. 2003).
In Turkey, the major compound is rutin in the ethanol extract of the flowers of
Crataegus monogyna Jacq as 2.68 mg/ml and provides considerable antioxidant activity
(78.80 ± 4.09) (Konyalioglu et al. 2017).
However, few studies investigated the Algerian species to reach sufficient data on
the chemical composition and the biological activity of Crataegus monogyna leaves. The
aim of the current study was, on one hand, the determination, with HPLC, of the chem-
ical composition of extracts plants of Crataegus monogyna, leaves growing in Sidi-Bel-
Abbes region (Northwest of Algeria). On the other hand, the assessment of the antioxi-
dant and the antibacterial activity of leavesethanol extract against common pathogens
such as Staphylococcus aureus,Escherichia coli,andPseudomonas aeruginosa.
2. Results and discussion
As the leaves of Crataegus monogyna, in Algeria are not phytochemically common, a
screening was carried out aiming to obtain a first indication of the main available
metabolites. Our results showed that flavonoids, phenol carboxylic acids, tannins, ster-
ols, and triterpene acids were present in the leaves of Crataegus monogyna. However,
saponosides, anthraquinones, alkaloids, anthocyanins, and coumarins were absent as
outlined in Table S1.
The ethanolic extract is considered the richest extract in polyphenol with 473.4 mg
extract and flavonoids 80.9 mg CE g
. The chloroform extract contains a low
content of polyphenols with 17.7 mg GAE g
as shown in Table S2. Results obtained
showed that the total phenolic content and total flavonoid content of C. monogyna
leavesextract were higher than those found in other species of different regions
worldwide. The variation of polyphenols and flavonoids of Crataegus leaves species of
different origins has previously been investigated by other researchers. In 2011, Bouzi
et al. reported in the eastern region of Algeria, that C. monogyna fruit polyphenol and
flavonoids values were 43.92 mg EAG/mg extract and 5.41 ug EQ/mg extract respect-
ively. Coimbra et al. (2020) have obtained in C. monogyna leaves 110.41 mg GAE g
extract and mg 29.94 QE g
extract. However, the extracts of C. monogyna leaves
tested by Iranian researchers Alirezalu et al. 2018, displayed values of 32.34 mg GAEg-
1 and 6.87 mg/g. Several studies have reported that the level of polyphenols varied
from 117.729 to 204.286 mg GAE/g in different regions of aerial parts of nine samples
of C. monogyna (Abuashwashi et al. 2016). Whereas the levels of flavonoids varied
from 2.12-32.62 mg/g in the same previous extracts. The highest phenolic (391.97GAE/
g) and flavonoid (17.60QE/g extract) rates were identified in the fruit C. monogyna
(Bardakci et al. 2019). Regarding the C. monogyna leavesextract, an elevated content
was observed in comparison to those in some studies. These differences in the com-
position of hawthorn vary among species and geographic locations (Jones et al. 2001;
Abuashwashi et al. 2016).
After comparing the retention times of the extracts with those of the controls, an
HPLC separation was performed allowing the identification of nine phenolic com-
pounds: procyanidin (peak1), epicatechin (peak2), catechin (peak3), chlorogenic acid
(peak4), caffeic acid (peak5), vitexin-2-O-rhamnoside (peak6), vitexin (peak7), rutin
(peak8) and hyperoside (peak9), in ethanolic extract from C.monogyna leaves (Figure
S1) and Syringic acid (peak10), myricetin (peak11), quercetin (peak12), naringenin
(peak13), kaempferol (peak14), using chloroformic leaves extract as shown in Figure
S2.C. monogyna of chloroform extract hat the highest level of kaempferol. After
revealing a TLC chromatogram of the chloroform and ethanol extracts with vanillin-
sulfuric acid, two purplish-blue spots one below the other appeared in the middle
part which correspond according to the literature to oleanolic and ursolic acid
(Kateryna Khokhlova et al. 2020) and Caligiani et al. (2013) identified ursolic acid in C.
monogyna leaves.
Bouzi et al. showed that quercetin was present in the fruit of C. monogyna however
rutin and catechin were absent in the extracts. Ziouche et al. (2020) found that the
extracts of leaves of eastern Algeria contained chlorogenic acid, rutin, isoquercetin,
hesperidin, and catechin. Unlike the methanolic fruit extract that contained caffeic
acid and quercetin. Concerning flavonoids, including rutin, apigenin, myricetin, quer-
cetin, naringenin, and kaempferol, they were identified in the leaf hawthorn (Keser
et al. 2014). The NMR technique quantified vitexin-2-O-rhamnoside, hyperoside, and
chlorogenic acid contents and HPLC separated vitexin, vitexin-2-O-rhamnoside, isovi-
texin, rutin, hyperoside in the leaf extract of C. monogyna Lund et al. (2017/2020).
Vitexin-2-O-rhrmnoside, vitexin, isovitexin, rutin, and hyperoside were quantified in
hawthorn leaf and flower by Mudge et al. (2016). Kateryna Khokhlova in 2020 identi-
fied the flavonoids and two triterpenes of 15 various Hawthorn of leaves and flowers
such vitexin2- rhamnoside, hyperoside, rutin, chlorogenic acid, caffeic acid oleanolic,
and ursolic acids. According to Alirezalu et al. 2018, the most abundant phenolic
compounds in the extracts of hawthorn leaves were chlorogenic acid, vitexin, and
vitexin-2-O-rhamnoside. Interestingly, the contents of rutin, vitexin-2-O-rhamnoside,
kaempferol, and chlorogenic acid in our study were the highest concentration ever
quantified in the leaf of C. monogyna. Moreover, the diversity of compounds found in
the current investigation agrees with several previously published studies (Keser et al.
2014; Mudge et al. 2016, Lund et al. 2020).
Furthermore, a very weak anti-radical activity was expressed by the chloroform
extract. Our test showed that ethanolic extract of C. monogyna leaves recorded higher
radical scavenging activity with an IC
value of 22.5 mg/mL than that found by
Ziouche et al. (2020) in leavesextract IC
; 24.52 mg/ml. In 2015, Loubna et al. found
an IC
of the aqueous extract of C. monogyna leaves at different stages of vegetation
ranging from 45 to 725 mg/mL. In 2021,
Urek et al. have shown among the differ-
ent species studied in Turkey, that the C. monogyna sample exhibited significant
antioxidant activity. However, the extracts of C. monogyna recently tested by Coimbra
et al. 2020 have presented an IC
value of 36.11 lg/mL. In our study, the antioxidant
activity in the leaves extract of C. monogyna displayed considerable antioxidant poten-
tial due to the phenolic content of this species extract. Flavonoids possess a much
higher concentration of rutin, vitexin-2-O-rhamnoside, kaempferol, chlorogenic acid,
and other phenolic derivatives.
Concerning the antibacterial activity assessment, the minimum inhibitory concentra-
tion (MIC) extract ethanol of leaves was observed at an interval of 0.512-1.024 mg/mL
against S. aureus. However, this was not active against E. coli and P. aeruginosa. The
extract leaves of C. monogyna of Algeria showed better activity compared to that C.
monogyna leaves observed by Coimbra et al. (2020) with 1 2 mg/mL and MIC of 1 g/
mL identified by Bouzi et al. (2011). Salmanian et al. (2014) found an antibacterial
activity of C. monogyna fruit between 5-10 mg/ml. Our results are in agreement with
those of Yi
git et al. (2014) who found the same MIC of alcoholic and aqueous extracts
against E. coli and S. aureus (1.25 and 0.625 mg/mL respectively).
3. Conclusion
Our results showed that variations were detected in C. monogyna leaves content and
composition compared to other authorsfindings. Leavesextract had strong antioxi-
dant and antibacterial activity, which were correlated with their high level of polyphe-
nols. Most of the substances found in C. monogyna extract of leaves were chlorogenic
acid, rutin, vitexin-2-O-rhamnoside and kaempferol. The variation in the chemical com-
position of C. monogyna might be attributed to the varied agroclimatic conditions of
the regions where it grows. High levels of polyphenolics found in C. monogyna leaves
allow this plant to exhibit its phyto and pharmaceutical potentials.
The authors would like to thank Professor Belhassaini Hachemi from the laboratory of
Biodiversity vegetable Faculty of Biology, Djillali Liabes University, Sidi Bel-Abbes for their scien-
tific collaboration, and Professor Meghit Boumediene Khaled for providing necessary corrections
to the last version of the article.
Disclosure statement
No potential conflict of interest was reported by the author(s).
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Crataegus (Rosaceae; hawthorn), are small trees that grow in the Northern Hemisphere. Plant materials of Crataegus show promising benefits in adjunctive treatment of cardiovascular disorders, primarily attributed to flavonoids and other phenolic derivatives. ¹H NMR was used in quantification of four flavonoids (naringenin, hyperoside, rutin, and vitexin-2″-O-rhamnoside) and chlorogenic acid in leaf extracts of four Crataegus species. The data were validated by comparison to HPLC-DAD. Vitexin and its derivatives were significantly more concentrated in the European (C. monogyna and C. laevigata) leaves and rutin significantly more concentrated in the North American (C. douglasii and C. okanaganensis) leaves. The concentrations of rutin and naringenin reported in this study are the highest reported for Crataegus. This work represents the first quantitative report of flavonoids in the North American hawthorns C. douglasii and C. okanaganensis and a direct comparison with the common European species.
This study was designed to comparatively evaluate the phytochemical composition and antioxidant potentials of fruit extracts from five Crataegus taxa (C. monogyna, C. orientalis, C. pontica, C. rhipidophylla and C. turcicus) growing wild in the flora of Turkey. Antioxidant activities of the samples were investigated using DPPH radical scavenging, FRAP, CUPRAC and total antioxidant capacity tests. Total phenol, phenolic acid, flavonoid, and proanthocyanidin contents were measured spectrophotometrically. Additionally, the presence of some phenolic compounds in the extracts was investigated by LC–MS/MS. Furthermore, the extracts used for the antioxidant activity studies were standardized for chlorogenic acid and hyperoside by HPTLC densitometry. Among the tested extracts, C. turcicus contained the highest phenolic (398.48 ± 0.98 GAE/g extract) and total flavonoid contents (23.87 ± 2.74 QE/g extract) content while C. monogyna contained by far the highest total proanthocyanidin (175.65 ± 10.59 EGCG-E/g extract), hyperoside (0.42%) and chlorogenic acid (0.90%) contents. Crataegus monogyna exhibited the highest antioxidant activity in FRAP, CUPRAC, and TOAC tests. Good correlation was found between the phenolic content and antioxidant parameters. This is the first report related with comparison of these five species in respect to phenolic profile and antioxidant activity.
The Hawthorn (Crataegus L.) is the most commonly used herb for treating cardiovascular diseases. The purpose of this paper was the analysis and comparison of HPTLC chromatographic profiles of flavonoids and triterpenes of leaves and flowers of 15 Crataegus L. species occurring throughout Eurasia and North America, and determination of specific distinguishing markers of its fingerprints. The optimal chromatographical conditions for evaluation of flavonoids and triterpenes of 15 Hawthorn species were proposed, the specific HPTLC fingerprints were obtained. The flavonoids fingerprints were qualitatively much the same for the pharmacopoeial species C.laevigata/oxyacantha and C.monogyna and other related non-pharmacopoeial European and Asian Hawthorn species including C.curvisepala, C.pseudokyrtostyla, C.fallacina, C.leiomonogyna, C.ambigua, C.sanguinea, C.almaatensis, C.turkestanica. The specific distinctive features for Hawthorn species native to North America, including C.punctata var aurea, C.pringlei, C.festiva, C.douglasii and C.holmesiana, were determined. The evaluation of the triterpenes profiles showed that all 15 analyzed Hawthorn species had quite similar fingerprints.
For compliance with US Current Good Manufacturing Practice regulations for dietary supplements, manufacturers must provide identity of source plant material. Despite the popularity of hawthorn as a dietary supplement, relatively little is known about the comparative phytochemistry of different hawthorn species, and in particular North American hawthorns. The combination of NMR spectrometry with chemometric analyses offers an innovative approach to differentiating hawthorn species and exploring the phytochemistry. Two European and two North American species, harvested from a farm trial in late summer 2008, were analyzed by standard 1D (1)H and J-resolved (JRES) experiments. The data were preprocessed and modelled by principal component analysis (PCA). A supervised model was then generated by partial least squares-discriminant analysis (PLS-DA) for classification and evaluated by cross validation. Supervised random forests models were constructed from the dataset to explore the potential of machine learning for identification of unique patterns across species. 1D (1)H NMR data yielded increased differentiation over the JRES data. The random forests results correlated with PLS-DA results and outperformed PLS-DA in classification accuracy. In all of these analyses differentiation of the Crataegus spp. was best achieved by focusing on the NMR spectral region that contains signals unique to plant phenolic compounds. Identification of potentially significant metabolites for differentiation between species was approached using univariate techniques including significance analysis of microarrays and Kruskall-Wallis tests.
Suitably validated analytical methods that can be used to quantify medicinally active phytochemicals in natural health products are required by regulators, manufacturers, and consumers. Hawthorn (Crataegus) is a botanical ingredient in natural health products used for the treatment of cardiovascular disorders. A method for the quantitation of vitexin-2″-O- rhamnoside, vitexin, isovitexin, rutin, and hyperoside in hawthorn leaf and flower raw materials and finished products was optimized and validated according to AOAC International guidelines. A two-level partial factorial study was used to guide the optimization of the sample preparation. The optimal conditions were found to be a 60-minute extraction using 50 : 48 : 2 methanol : water : acetic acid followed by a 25-minute separation using a reversed-phased liquid chromatography column with ultraviolet absorbance detection. The single-laboratory validation study evaluated method selectivity, accuracy, repeatability, linearity, limit of quantitation, and limit of detection. Individual flavonoid content ranged from 0.05 mg/g to 17.5 mg/g in solid dosage forms and raw materials. Repeatability ranged from 0.7 to 11.7 % relative standard deviation corresponding to HorRat ranges from 0.2 to 1.6. Calibration curves for each flavonoid were linear within the analytical ranges with correlation coefficients greater than 99.9 %. Herein is the first report of a validated method that is fit for the purpose of quantifying five major phytochemical marker compounds in both raw materials and finished products made from North American (Crataegus douglasii) and European (Crataegus monogyna and Crataegus laevigata) hawthorn species. The method includes optimized extraction of samples without a prolonged drying process and reduced liquid chromatography separation time.
Context: Crataegus monogyna Jacq L. (Lind.) (Rosaceae) is used in folk medicine as a sedative, aerial parts being rich in polyphenols with antioxidant ability. Objectives: To study the variation in polyphenolic composition and antioxidant ability of spontaneous samples of C. monogyna in order to assess the relationship among these variables. Materials and methods: Aerial parts of C. monogyna were collected from nine different locations in central Spain and extracted with methanol after drying. Total polyphenols were determined by the Folin-Ciocalteu method using gallic acid (GA) as standard. Sixteen polyphenolic compounds (11 flavonoids and 5 phenolic acids) were identified and quantified by reversed-phase HPLC in one single analysis. The antioxidant ability was evaluated by the oxygen radical absorbance capacity (ORAC) and the free radical scavenging activity (DPPH) methods. Linear correlation analysis was used to explore the relationships between the studied variables. Results: Total polyphenol content ranged between 117.729 ± 0.011 and 204.286 ± 0.015 mg GAE/g extract, depending on the geographic origin. No relationship was found between total polyphenols and antioxidant ability by the ORAC or DPPH methods. Chromatographic analysis yielded lower amounts of polyphenols (23.3-143.26 mg/kg), as only flavonoids and phenolic acids were quantified. All the samples exhibited antioxidant activity between 1.32 ± 0.08 and 2.76 ± 0.007 μmol Trolox equivalents/mg and IC50 from 0.82 ± 0.10 to 3.76 ± 0.67 μg/mL. Conclusion: A statistically significant relationship between flavonoids and phenolic acids content and the antioxidant potential obtained by the ORAC method for C. monogyna samples was proven.