Phytochemistry and medicinal values of Mahonia bealei: A review

Abstract

Traditional Chinese medicine (TCM) has been used since long for medicinal purposes. Plant sources are a major part of TCM. Species belonging to genus Mahonia had been used for disorders like inflammation, pharyngolaryngitis, stomach disorders, infections like hepatitis and diseases like those of the skin, besides various other purposes. We have reviewed medicinal uses of an important member of genus Mahonia belonging to family Berberidaceae named Mahonia Bealei (Beale's barberry). Several useful compounds have been extracted from this plant including alkaloids, triterpenes, flavonoids, phytosterols and lignan. The sources of extraction of these compounds have been leaves, stem and roots. This specie has its own importance among other members of genus as it has been traditionally used to treat dysentery, diarrhea, inflammation, etc. Compounds from this plant were extracted and studied by various researchers globally using in vitro and in vivo techniques to find out scientific evidences of medicinal importance of this plant. We have reviewed research carried out on this specie and found that antibacterial, anti-inflammatory, antitumor, antioxidant and anti-gastrin ability of different parts of this plant has been proven and reported. Still parts of this plant remain underexplored. Moreover, a comparison of activities of isolated compounds must be found because synergistic effect of extracts of different parts of this plant has been proposed but is to be explored scientifically. Therefore, future research should be carried out on different parts of this plant which can be a useful addition to our knowledge of different therapeutic agents.

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Kakar et al
Trop J Pharm Res, October 2019; 18(10):2219
Tropical Journal of Pharmaceutical Research October 2019; 18 (10): 2219-2227
ISSN: 1596-5996 (print); 1596-9827 (electronic)
© Pharmacotherapy Group, Faculty of Pharmacy, University of Benin, Benin City, 300001 Nigeria.
Available online at http://www.tjpr.org
http://dx.doi.org/10.4314/tjpr.v18i10.31
Review Article
Phytochemistry and medicinal values of Mahonia bealei: A
review
Mohib Ullah Kakar1,2, Muhammad Saeed3, Ke Luo1, Imran Suheryani1, Wu
Shuang1, Yulin Deng1, Rongji Dai1*
1School of Life Sciences and Technology, Beijing Institute of Technology, Beijing 100081, PR China, 2Faculty of Marine
Sciences, Lasbela University of Agriculture, Water and Marine Sciences, Uthal, Balochistan, 3Faculty of Animal Production &
Technology, The Cholistan University of Veterinary and Animal Sciences, Bahawalpur, Pakistan
*For correspondence: Email: dairongji@bit.edu.cn; Tel: 0086-01068949331
Sent for review: 30 May 2019 Revised accepted: 25 September 2019
Abstract
Purpose: To review the medicinal uses of Mahonia bealei, an important member of the genus Mahonia,
with a focus on its various applications in Traditional Chinese Medicine, as well as published scientific
evidence on its effectiveness.
Methods: Information in all available literature was retrieved using different search engines including
NCBI, ISI Web of Knowledge and Google.
Results: Several compounds have been extracted from M. bealei. These include alkaloids, triterpenes,
flavonoids, phytosterols and lignans. Traditionally, the plant is used to treat dysentery, diarrhea and
inflammation. Globally, scientists have used in vitro and in vivo techniques to evaluate the usefulness of
compounds extracted from M. bealei with respect to their antibacterial, anti-inflammatory, antitumor,
antioxidant as well as anti-gastrin properties.
Conclusion: Different parts of this plant still remain underexplored. Moreover, comparison of the
properties of the isolated compounds has not been carried out, nor are there reports on the synergistic
effects of extracts of the plant. Therefore, future research to address these areas may be useful in the
discovery of new therapeutic agents.
Keywords: Berberidaceae, Mahonia bealei, Traditional Chinese Medicine, Alkaloids, Flavonoids, Anti-
inflammatory activity, Anti-tumor activity
This is an Open Access article that uses a fund-ing model which does not charge readers or their
institutions for access and distributed under the terms of the Creative Commons Attribution License
(http://creativecommons.org/licenses/by/4.0) and the Budapest Open Access Initiative
(http://www.budapestopenaccessinitiative.org/read), which permit unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly credited.
Tropical Journal of Pharmaceutical Research is indexed by Science Citation Index (SciSearch), Scopus,
International Pharmaceutical Abstract, Chemical Abstracts, Embase, Index Copernicus, EBSCO, African
Index Medicus, JournalSeek, Journal Citation Reports/Science Edition, Directory of Open Access Journals
(DOAJ), African Journal Online, Bioline International, Open-J-Gate and Pharmacy Abstracts
INTRODUCTION
Mahonia bealei belongs to the family
Berberidaceae and genus Mahonia.
Geographically, this evergreen shrub is widely
distributed in America, Europe and Asia [1].
Mahonia is a genus containing more than 60
species, and more than 30 species of this genus
grow in the southwest area of China [2]. The
genus Mahonia is a member of basal eudicots
which consists of coriaceous (sclerophyllous)
evergreen small trees or shrubs with compound
leaves [2,4]. It has been revealed that 20 species
of this genus are distributed in southwestern
parts of the United States of America [4]. Some
of the species are also present in Europe as
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© 2019 The authors. This work is licensed under the Creative Commons Attribution 4.0 International License

Kakar et al
Trop J Pharm Res, October 2019; 18(10):2220
invasive plants [5].
Traditional Chinese Medicine (TCM) has a long
history of usage of materials derived from
botanical, animal as well as mineral resources.
These agents have been classified according to
their sources, color, habitats, way of collection,
parts of the plant collected and the methods of
prescription, by Li in his famous work Ben Cao
Kong Mu (The Classical TCM Pharmacopeia) [6].
In TCM, the roots, stem and leaves of Mahonia
have been used for the treatment of different
diseases such as diarrhea and dysentery for
centuries. These plants are recognized by the
Chinese Pharmacopeia Commission for their
moisturizing effects, heat-clearing properties, and
as detoxifying agents [7].
Another important species with similar properties
reported in TCM is bai-yang-jie (Arundina
graminifolia) [8]. In TCM, Mahonia Caulis which
comprises dried stem of Mahonia bealei (Fort.)
Carr. and M. fortune (Lindl.) Fedde is an
important medicine. It has been used for long for
treating icteric hepatitis, conjunctivitis, ulcers,
boils, carbuncles, toothache, and ailments that
were thought to be due to fire of stomach [9]. The
leaves of Mahonia bealei have been used to
produce bitter tea, and are rich in polyphenolic
compounds with potent antioxidant properties
[10]. There have been numerous reports showing
the antioxidant potential of the leaves when
consumed in the form of tea like black tea which
is used worldwide [11].
Studies have shown that the chemical
composition of different compounds from
Mahonia bealei is important for their use in
pharmaceutical industry [1,12,13]. The leaves of
Mahonia bealei are an important source of
beneficial natural compounds that need to be
explored [14]. Phytochemical studies have
revealed that the stem and roots of M. bealei are
rich in cerebrosides and alkaloids [15]. Different
parts of the genus Mahonia, such as stem, bark,
leaves and fruits of have been extensively used,
and possess a long history of application in TCM
[16-20]. Phytochemical studies on Mahonia
species have been very beneficial in the isolation
of sterols, alkaloids, flavonoids and glycosides
[1].
The present study summarized the number of
useful compounds isolated from Mahonia bealei
and their structures. In addition, the medicinal
uses of these compounds were reviewed, and a
comparison of the medicinal uses of the plant in
TCM, in relation to experimental findings was
made. Future prospects regarding studies of this
species were also proposed in this review.
Morphology and distribution of Mahonia
bealei
Mahonia bealei (also called leatherleaf Mahonia)
is an evergreen shrub that grows to a height of
about 5 to 10 feet (1.5 to 3 m). Pinnately
compound leaves are present which are 18
inches (46 cm) long and contain 9 - 13 holly-like
leaflets 1 to 2 inches (2.5 to 5.1 cm) wide, and 2
to 4 inches (5 to 10 cm) long. The time of
flowering of this plant is from late winter to early
spring. The flowering starts with the development
of fragrant, lemon-yellow flowers. The fruits are
green berries which later turn to blue black color
and increase in size to half an inch, while
hanging from the plant. Although the plant is
native to China, it is an invasive plant in parts the
United States of America, especially the southern
region, and it has been categorized as an
ornamental shrub [21]. Figure 1 shows the
different parts of this plant.
Figure 1: Mahonia bealei. (a): The arial parts of
Mahonia bealei growing among other plants; (b):
leaves of M. bealei; (c): roots of Mahonia bealei; (d):
fruits of Mahonia bealei
Compounds isolated from Mahonia bealei
The extraction of compounds from medicinally
important plants and investigations of their
medicinal uses are important areas of scientific
research. Different parts of Mahonia bealei have
been studied. In this section, the number, nature
and structure of compounds isolated from this
species to date, are summarized.
Alkaloids
Studies have shown that isoquinoline alkaloids
constitute a major subclass of alkaloids isolated
from the genus Mahonia. These compounds are
responsible for many properties exhibited by
plants of this genus. A study has shown that the
roots, stem and leaves of M. bealei contain the
three alkaloids berberine, palmatine, and
jatrorrhizine [22]. The major alkaloid found in
leaves was berberine, while the roots and stem
contained jatrorrhizine and berberine [23]. The
structures of these alkaloids are given in Figure 2
and Figure 3 [30].

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Trop J Pharm Res, October 2019; 18(10):2221
Figure 2: Structures of alkaloids isolated from
Mahonia bealei
Figure 3: Structures of alkaloids isolated from
Mahonia bealei
Triterpenes
To the best of our knowledge, so far, only three
triterpenes have been isolated from the leaves of
M. bealei. These compounds, identified as
ursolic acid, oleanolic acid and oleanolic acid 3-
O-β-D-glucopyranoside, were for the first time
isolated from the species of the genus Mahonia
[15]. Later-on, 3-O-β-D-glucopyranoside was
isolated from the branches of this plant [24]. The
structures of these triterpenes are given in Figure
4.
Flavonoids
Certain flavonoids have been isolated from the
leaves and branches of M. bealei. These
flavonoids are quercetin and quercetin 3-O-β-D-
xylopyranoside [25]. Later studies also reported
the isolation of tamarixetin 3-O-β-D-
glucopyranoside, quercetin 3-O-β-D-
xylopyranoside, isorhamnetin 3-O-α-L-
rhamnopyranoside, luteolin, isorhamnetin, tricin,
and chryseriol. The structures of these flavonoids
are shown in Figure 5.
Figure 4: Structures of triterpenes isolated from
M. bealei
Figure 5: Flavonoids from M. bealei
Phytosterols
Two phytosterols have been isolated from
Mahonia bealei. A stigmasterol was reported
after NMR and MS spectroscopic studies of
methanol extract of the plant [25]. In another
study, 70 % ethanol extract of the stem of
Mahonia bealei yielded β-sitosterol [26]. The
structures of these phytosterols are shown in
Figure 6.
Figure 6: Phytosterols isolated from M. bealei
Lignans
Four lignans have been isolated from Mahonia
bealei. A study of 70 % ethanol extract of the

Kakar et al
Trop J Pharm Res, October 2019; 18(10):2222
stem of Mahonia bealei using chromatographic
separation techniques yielded episyringaresinol
which was characterized by mass spectrometry
[26]. Later on, another study conducted on the
ethyl acetate fraction of the trunk of M. bealei
yielded three more lignans identified as
yangambin, epiyangambin and bishexadecyl
epiphyllate [25]. The structures of these lignans
are given in Figure 7.
Figure 7: Lignans isolated from M. bealei
Other compounds isolated from M. bealei
In addition to the classes of compounds already
presented, several compounds from other
classes have been isolated, although in less
abundant amounts, from different parts of M.
bealei. Erythro-syringoyl glycerol 8-O-β-D-
glucoside; 3, 4, 5-trimethoxyphenyl-1-O-β-D-
glucoside, and 5,5/-dimethoxylariciresinol- 4/-O-
β-D-glucoside were identified from the stem
extracts of M. bealei [26]. Another study isolated
three compounds belonging to phenolic, steroidal
and phenylpropanoid groups. These were
identified as methyl syringate, daucosterol, and
3-(4-hydroxy-3, 5- dimethoxyphenyl)-3-ethoxy-2-
sulfopropane-1-ol, respectively. Later on, gallic
acid and trans-cinnamic acid were identified from
extracts of the branches of Mahonia bealei after
isolation, purification and characterization [24].
The structures of these compounds are given in
Figure 8.
MEDICINAL USES OF COMPOUNDS
ISOLATED FROM M. BEALEI
Several medicinal uses of the compounds
extracted from M. bealei have been reported.
These are reviewed below.
Figure 8: Other groups of compounds isolated from
M. bealei
Antimicrobial properties
In TCM, the plants from genus Mahonia are
known to inhibit bacteria. Mahonia caulis consists
of M. bealei (Fort). Carr and M. fortune (Lindl.)
Fedde. These plants were used as anti-
pneumoconiosis, anti-nociceptive, as well as
antipyretic agents [27,28]. Studies have shown
that ethanol extracts of stems and leaves of M.
bealei are effective against Staphylococcus
aureus, Bacillus thuringiensis and Bacillus
subtilis, but not effective against gram positive
bacteria. The stem extract of M. bealei was more
effective than the leaf extract. The most effective
antimicrobial activity exhibited by the stem
extract was against Staphylococcus aureus, with
minimum inhibitory concentration (MIC) of 0.58
mg/ml, relative to the leaf extract with MIC of
2.30 mg/ml [18].
Another study showed that extracts of Mahonia
bealei, whether tanninized or de-tanninized, did
not show any activity against clinically important
multidrug resistant pathogenic strains of
Acinetobacter baumannii 31P, 125 and 152P
[29]. However, a US patent document showed a
preparation method for the extract of Mahonia
bealei that exerted biostatic effects on
Escherichia coli, Staphylococcus aureus and
Enterococcus faecalis. Inhibitory effect was not
reported on Klebsiella pneumonia, Pseudomonas
aeruginosa and Enterobacter cloacae. An
important feature of this invention is the simple
method of extract preparation using the stem and

Kakar et al
Trop J Pharm Res, October 2019; 18(10):2223
leaves of Mahonia bealei as raw materials, with
water, ethanol or water-containing alcohol as
solvent. This patent emphasizes the antibacterial
activity of M. bealei [30]. It has been reported that
alkaloid extract of the roots of M. bealei (Fort.)
Carr. inhibited the proliferation of Avian influenza
virus (AI) in embryos at a dose of 0.25mg/ml, and
showed no adverse side effects on the
experimental embryos, even at doses up to 20
mg/ml [31].
Antitumor properties
A study has reported that water extract of leaves
of M. bealei inhibited the proliferation of human
colon cancer (HT-29) cells [10]. Molecular and
chromatographic evidence indicated that the
proportion of apoptotic cells increased while the
expression of survivin gene was downregulated
[10]. The survivin gene is an important member
of an apoptotic family of inhibitors which
presence results in the prevention of apoptotic
cell death while it promotes proliferation of cells.
Studies have revealed that survivin gene
expression is upregulated in tumors, while its
expression is normally downregulated in normal
cells [32]. After evaluation of antitumor property
in [10], the compound responsible for the
antitumor effect was identified through sequential
partitioning of the aqueous extract of M. bealei
leaves using ethyl acetate, n-butanol and
dichloromethane. Cytotoxicity of each fraction
was assessed against HT-29 cells and it was
revealed that the dichloromethane fraction was
active against HT-29 cell lines. Further studies
showed that the anticancer effect was due to the
presence of berberine, which had IC50 of 36.54
µM for HT-29 cells [10]. In another investigation,
palmatine, an alkaloid obtained from M. bealei
was shown to exhibit anti-proliferative properties
as well as cytokine-lowering effects in vitro and in
vivo [33]. Previous research had shown that an
important risk factor for tumor development
(including colorectal cancer) was chronic
inflammation, while inhibition of inflammatory
pathway was effective in preventing the
development of colon cancer [34, 35]. In vitro
studies to check levels of production of LPS-
induced inflammatory cytokines showed higher
cytokine levels in HT-29 cell lines than in SW-
480 cell lines, while the administration of
palmatine resulted in significant reduction of IL8
cytokine levels in HT-29 cell lines. Results of in
vivo studies showed that oral administration of
palmatine at doses of 10 or 20 mg/kg/day in
APCmin/+ resulted in significant reduction of tumor
numbers in colon and small intestine. Therefore,
orally-administered palmatine may have
significant therapeutic potential for colorectal
cancer [33]. Since palmatine obtained from
Mahonia bealei and orally administered M. bealei
were used in the above study, it was concluded
that M. bealei possesses antitumor properties
[33].
Antioxidant effects
Studies have shown that free radicals are major
causes of oxidative damage to biological
molecules as a result of which diseases like
cancer, coronary heart disease and dementia
develop. Free radicals are also considered major
factors in the aging process [35]. A study of the
water extract of leaves of Mahonia bealei (Fort)
Carr. showed that it exhibited antioxidant
properties. The stable free radical 2, 2-diphenyl-
1-picrylhydrazyl (DPPH) is used for the
evaluation of reducing substances in biological
systems as well as foods [36]. Experimental
evidence revealed that leaf extract of Mahonia
bealei exhibited DPPH free radical scavenging
effect in concentration-dependent manner, with a
concentration of 100µg/ml producing the highest
(73.67 %) scavenging effect [10]. The superoxide
radical brings about oxidative damage to cells
[37]. The aqueous leaf extract of M. bealei
scavenged superoxide anions in a concentration-
dependent manner, and significantly reduced
oxidative modification of proteins [10]. Proteins
are one of the major targets of oxidative damage
by free radicals [38]. In another study, it was
shown that ethanol extract of M. bealei exhibited
anti-radical effects against DPPH, with IC50 value
of 80.0 µg/ml, and against ABTS+ with IC50 value
of 26.2 µg/ml [39].
Anti-gastrin effect
Gastric ulcer is an important and common
pathological condition that causes loss of weight,
loss of appetite, vomiting, heartburn and other
clinical manifestations [40]. In the clinical
treatment of gastric ulcer, the inhibition of gastric
acid secretion is very important because gastric
acid has been identified as the key pathogenic
factor of the disease [41]. Historically, the
introduction of H2 receptor antagonists and
proton pump inhibitors that target gastric H+/K+-
ATPase resulted in a major breakthrough with
respect to the treatment of gastroesophageal
reflux diseases and peptic ulcer [42,43]. Studies
show that gastric H+/K+-ATPase is responsible
for the acidification of stomach. It is a proton
pump which stimulates gastric acid production.
The inhibition of this pump is useful in clinical
treatment of reflux disease, peptic ulcer and
dyspepsia [42].
Previous studies showed that other medicinal
plants in TCM such as Dregea sinensis Hemsl.

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Trop J Pharm Res, October 2019; 18(10):2224
(Daibaiji) and Dracaena cochinchinensis (Lour.)
(also called dragon’s blood) exerted gastro-
protective effects in vivo [44,45]. A study has
shown that total alkaloids from the stem of M.
bealei, when applied on experimental rats
lowered the content of gastrin by inhibiting H+/K+-
ATPase activity, resulting in reduction of gastric
acidity. A 57 % protective effect of total alkaloids
from M. bealei was observed on pyloric ligation-
induced gastric ulcer in rats in vivo, relative to 63
% protection by the positive control omeprazole
[13].
Anti-inflammatory effects
Inflammation is an important response that is
ubiquitously produced as a defense mechanism
against pathogens in all organisms.
Macrophages are major immune cells that play a
key role in the onset of inflammation [46]. The
results obtained from in in vivo and in vitro
experiments have indicated that the leaves of M.
bealei (Fort.) Carr. possess anti-inflammatory
properties [47]. A key factor in initiating
inflammatory response is the production of NO
free radical which acts as a major factor that
triggers inflammatory responses [48]. Along with
in vitro study on cell lines, an in vivo study was
also conducted using lipopolysaccharide-induced
acute lung injury (ALI) in the mouse model. This
model was used because inflammatory response
is triggered in lung injury, and TNF-α and IL-6
are important indicators of early onset of
inflammatory response [49].
Using mouse model, it has been revealed that
the levels of inflammatory mediators are reduced
by treatment with the dichloromethane fraction of
leaves of Mahonia bealei (Fort). Carr. [47]. A
study showed that a triterpene obtained from the
leaves of Mahonia bealei reduced the production
of cytokines, downregulated MAPK pathway, and
inhibited activation of NF-kB [50].
A summary and comparison of traditional
medicinal uses of different parts of M. bealei, and
scientific evidence reported based on research
conducted by different scientists are shown in
Table 1.
A summary of classes of useful compounds
obtained from different parts of Mahonia bealei,
their traditional medicinal uses, and scientific
evidence obtained to date are presented in
Figure 9.
CONCLUDING REMARKS
Mahonia bealei has been traditionally used for
medicinal purposes throughout the ancient times.
With the advancement of scientific research,
scientific evidence is being explored to establish
the bases for the uses of the plant. Although
several compounds from the roots, stem and
leaves of Mahonia bealei have been extracted
and used in different studies, a lot still needs to
be done. A comparison of traditional uses of
different parts of Mahonia bealei with scientific
evidence reported to date shows that many uses
of the have not yet been scientifically
investigated. Therefore, future research require
more studies on different parts of this plant. A
comparison of the properties of different solvent
extracts of different parts of the plant is also
required. More importantly, studies of possible
synergistic effects of different extracts may lead
to discovery of new therapeutic uses of this plant.
Table 1: Summary of traditional uses of Mahonia bealei and reported activities
S/no.
Part of plant
used
Traditional uses
Reference
Scientific study
Source
Reference
1 Roots, stem and
leaves Diarrhea Pharmacopeia
[7] No Reported - -
2 Roots, stem and
leaves Dysentery Pharmacopeia
[7]
Not Reported - -
3 Roots, stem and
leaves
Clearing heat
Pharmacopeia
[7]
Antiinflammatory
Activity Leaves [47,49]
4 Leaves and fruit Detoxification Chinese
Pharmacopoeia
[9]
Antioxidant
Activity Leaves [10,39]
5 Dried stem Icteric hepatitis
conjunctivitis Pharmacopeia
[7]
Not Reported - -
6 Dried stem Ulcers Pharmacopeia
[7]
Anti-gastrin
Activity Stem [13]
7 Dried stem Carbuncles Pharmacopeia
[7]
Not Reported - -
8 Dried stem Toothache Pharmacopeia
[7]
Not Reported - -
9 Dried stem Stomach fire Pharmacopeia
[7]
Anti-gastrin
Activity Stem [13]

Kakar et al
Trop J Pharm Res, October 2019; 18(10):2225
10 Roots Antipyretic [27, 28] Antimicrobial
Activity Stem and
Leaves [18,29-31]
Figure 9: A scheme showing classes of useful
compounds obtained from different parts of Mahonia
bealei, their traditional medicinal uses, and scientific
evidence obtained to date
DECLARATIONS
Conflict of interest
No conflict of interest is associated with this
work.
Contribution of authors
We declare that this work was done by the
authors named in this article, and all liabilities
pertaining to claims relating to the content of this
article will be borne by the authors. Mohibullah
Kakar generated the idea, searched and
compiled the data. Muhammad Saeed and Ke
Lou helped in the compilation and searching of
data. Imran Suheryani and Wu Shuang helped in
the arrangement and writing of the review. Yulin
Deng and Rongji Dai provided all the funding and
guidelines for the manuscript.
Open Access
This is an Open Access article that uses a fund-
ing model which does not charge readers or their
institutions for access and distributed under the
terms of the Creative Commons Attribution
License (http://creativecommons.org/licenses/by/
4.0) and the Budapest Open Access Initiative
(http://www.budapestopenaccessinitiative.org/rea
d), which permit unrestricted use, distribution,
and reproduction in any medium, provided the
original work is properly credited.
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