Pharmacological Aspects of Terminalia belerica

Abstract

Terminalia belerica Roxb. is member of family combretaceace, growing widely
throughout the Indian subcontinent, Bangladesh, Nepal, Sri-Lanka and South East
Asia. It is used in several traditional medicines to cure various diseases. Glucoside,
tannins, gallic acid, ellagicacid, ethylgalate, gallylglucose, chebulanic acid are mainly
believed to be responsible for its wide therapeutic actions. It is known to possess
medicinal activities such as analgesic, antioxidant, hepatoprotective, antibacterial,
anticancer and immune-modulatory activities. In this chapter information concerning
pharmacological attributes of T. belerica has been summarized.

Full text

52Mol. Biol. and Pharm. of Beneficial Plants ISBN 978-93-85995-56-9
Pharmacological Aspects..................Terminalia belerica Gupta et al, 2017
4
Pharmacological Aspects of
Terminalia belerica
Ashutosh Gupta, Ramesh Kumar,
*Shashank Kumar and Abhay K. Pandey
Department of Biochemistry, University of Allahabad, Allahabad-211002, India
*Centre for Biochemistry and Microbial Sciences, Central University of Punjab,
Bathinda-151001, Punjab, India
ABSTRACT
Terminalia belerica Roxb. is member of family combretaceace, growing widely
throughout the Indian subcontinent, Bangladesh, Nepal, Sri-Lanka and South East
Asia. It is used in several traditional medicines to cure various diseases. Glucoside,
tannins, gallic acid, ellagicacid, ethylgalate, gallylglucose, chebulanic acid are mainly
believed to be responsible for its wide therapeutic actions. It is known to possess
medicinal activities such as analgesic, antioxidant, hepatoprotective, antibacterial,
anticancer and immune-modulatory activities. In this chapter information concerning
pharmacological attributes of T. belerica has been summarized.
Key words: Terminalia belerica, Phytoconstituent, Pharmacology, Traditional system
of medicine.
INTRODUCTION
Plants produce wide range of bioactive compounds and constitute a
rich source of medicines. The ancient Ayurvedic, Unani and Siddha systems
of medicine is based on the healing ability of plants. In different regions of
the world, plant derived medicinal systems remain important in the treatment
of various diseases. Ayurvedic remedy is quite commonly practiced in India
with an estimated 85 % of Indians still using crude plant preparations for the
treatment of a wide variety of diseases and ailments (Kamboj, 2000). Many
of the prescription drugs currently promoted for a wide variety of ailments
Book: Molecular Biology and Pharmacognosy of Beneficial Plants
ISBN: 978-93-85995-56-9
Editors: Prof. Abbas Ali Mahdi, Murtaza Abid,
Dr. M.M. Abid Ali Khan, Dr. M.I. Ansari and
Dr. Raaz K. Maheshwari
Publisher: Lenin Media Private Limited, Delhi, India
©All rights reserved
Year of Publication 2017
4

53Mol. Biol. and Pharm. of Beneficial Plants ISBN 978-93-85995-56-9
Pharmacological Aspects..................Terminalia belerica Gupta et al, 2017
were originally isolated from plants and/or are semi-synthetic analogues of
plant derived chemicals. It has been estimated that approximately 25 % of all
prescription drugs currently in use are of plant origin (Walsh, 2003; Newman
and Cragg, 2007). Furthermore, approximately 75% of new anticancer drugs
used between 1981 and 2006 were derived from plant compounds (Newman
and Cragg, 2007).
Terminalia belerica Roxb. (Family Combretaceae) is a large deciduous tree
with broadly elliptic leaves clustered at the ends of branches (Meena et al.,
2010). It is wildly distributed throughout the world especially Indian
subcontinent, Srilanka, Pakistan, Nepal and South East Asia. T. belerica is
used in traditional medicine due to the wide spectrum of pharmacological
activities associated with the biologically active secondary metabolites present
in this plant. Variety of phytochemicals are isolated from various parts of
the plant which include alkaloid, coumarin, flavones, steroids, lignans, tannins,
glycosides, terpenoid, saponin etc.(Abraham et al., 2014).
PLANT DESCRIPTION
Family Name: Combretaceae
Kingdom: Plantae
Division: Magnoliophyta
Class: Magnoliopsida
Order: Myrtales
Family: Combretaceae
Genus: Terminalia
Species: belerica

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Pharmacological Aspects..................Terminalia belerica Gupta et al, 2017
T. belerica is also referred to as Beleric Myrobalan in English, Bibhitaki in
Sanskrit, and locally known as Bahera in India. It has been used for centuries
in the Ayurveda, a holistic system of medicine originating from India. It is a
large (10-20 meter) deciduous tree with characteristic thick brownish gray
bark and is found throughout the Indian forests and plains. The stems are
straight, frequently buttressed when large. Leaves are alternate, broadly elliptic,
clustered towards at the ends of branches when young but glabrous on
maturity and the nerves are prominent on both surfaces. Flowers are greenish-
yellow, borne in axillary, spender spikes longer than the petioles and having
offensive odor. Fruit a drupe about 2.5 cm long, globose or narrowed at the
base, silky-brownish-velvety. (Karthikeyan et al., 2012; Das et al., 2012)
Phytoconstituents
Its principle phytoconstituents are beta-sitosterol, gallic acid, ellagic acid,
ethyl gallate, galloyl glucose, chebulagic acid. Four lignans including
termilignan, thannilignan, hydroxy-3', 4'-(methylenedioxy) flavan, and
anolignan-B have been found (Singh, 2006). Fruit contains terpenoids (belleric
acid and chebulagic acid), saponin (bellericoside and bellericanin) (Meena et
al., 2010; Sharma, 2012) and tannins (23.60%-37.36%), which are composed of
chebulinic acid, chebulagic acid, 1, 3, 6-trigalloylglucose and 1,2,3,4, 6-
pentagalloylglucose, corilagin, andglucogallin etc. (Saxena, et al., 2013;
Gangadhar et al., 2011). Seed contains alkaloids, coumarin, flavone, glycosides
(D-glucose, fructose, sucrose, galactose and mannose) (Parle et al., 2014).
Bark contains beta-sitosterol, tannins, ellagic acid, gallic acid and catechol.
Traditional Uses
T. belerica fruits exhibit medicinal activity. These are used as laxative,
astringent, anthelmintic and antipyretic. Fruits are useful in treatment of hepatitis,
bronchitis, asthma, dyspepsia, piles, diarrhoea, coughs, hoarseness of voice, eye
diseases, scorpion-sting and also used as a hair tonic (Singh et al., 2011; Rastogi
and Mehrotra, 2004). Decoction of the green fruit is used for cough. Pulp of the
fruit is useful in dysenteric-diarrhoea, dropsy, piles and leprosy. Half ripe fruit
is used as purgative. Kernel of the fruit is narcotic. Inhabitants of Khagrachari
in Bangladesh use fruits in menstrual disorder. Seed oil is used in rheumatism.
Gum of the bark is demulcent and purgative. The triterpenoid present in the
fruits possess significant antimicrobial activity. Kernel oil has purgative action
and its prolonged use is well tolerated in mice (Ghani, 2003).
PHARMACOLOGICAL ACTIVITIES
Antioxidant activity
Oxidative stress arises from an imbalance in the formation and
metabolisms of reactive oxygen species (ROS). It is associated with many

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pathophysiological conditions in humans. Antioxidants are molecules that
inhibit or reduce free radical reactions and finally prevent cellular damage
(Young and Woodside, 2001). Antioxidant supplements help in reducing the
oxidative damage at cellular level. Depending on phytochemical constitution,
antioxidant defense mechanisms vary. Both forms of antioxidants (enzymatic
and non-enzymatic) are present in the intracellular and extracellular
environments. T. belerica has been reported to possess potent antioxidant
action (Fahmy et al., 2015).
A comparative study on radical scavenging activity of ethanolic and
aqueous extract of T. belerica fruit suggested that aqueous extract has
comparatively better scavenging action against superoxide anion, nitric oxide
and ABTS radicals. Aqueous extract also exhibited effective reducing power
and FRAP values, but the total antioxidant capacity values of aqueous extract
are lower than ethanolic extract (Pfundstein et al., 2010). In other study,
acetone and other fractions of T. belerica also showed radical scavenging
action in DPPH free-radical scavenging and â-carotene bleaching assay along
with reducing power capacity. These activities were correlated closely with
their phenolic content. Ethyl acetate (EA) fraction was found more effective
than crude acetone extract in all antioxidant assays, except chelating power
which was highest in water fraction. The antioxidant potential was compared
with known antioxidant butylated hydroxyl toluene (BHT) and correlated
with total phenolic and flavonoid content in crude extract and fraction (Guleria
et al., 2010). An HPTLC analysis of the EA fraction further showed that it
contains gallic acid, ferulic acid and ascorbic acid as major compounds. The
results suggested that the principal antioxidant molecules in crude extract/
fractions of T. belerica fruit are non-flavonoid polyphenolic compounds
(Nampoothiri et al., 2011).
Hepatoprotective activity
The liver is a vital organ of vertebrates and some other animals (Abdel
et al., 2010). It has a wide range of functions, including detoxification of
various metabolites, protein synthesis, and the production of bile necessary
for digestion. Hepatotoxicity refers to inability of liver to detoxify the toxic
compounds. One of the most sensitive and dramatic indicators of hepatocyte
injury is the release of intracellular enzymes, such as transaminases and serum
alkaline phosphatase in the circulation during hepatic abnormalities. The
elevated activities of these enzymes are indicative of cellular leakage and
loss of the functional integrity of the cell membrane in liver (Rajesh and
Latha, 2004). The hepatoprotective activity of T. belerica fruit extract and its
bioactive compounds have been revealed against CCl4 induced liver injury
in rats. The toxicity of CCl4 depends upon the cleavage of C-Cl bond to

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generate a trichloromethyldioxy free radical (CCl3O2). This cleavage occurs
in the endoplasmic reticulum and is mediated by the cytochrome P-450, a
mixed function oxidase system. The product of the cleavage binds irreversibly
to hepatic proteins and lipids (Pingale, 2011). Different dose of plant extract
(200-800 mg/kg body weight) and gallic acid (50-200 mg/kg body weight)
showed dose dependent recovery of biochemical parameters (SGOPT, SGPT,
lipid peroxidation and glutathione) (Shukla et al., 2006). Ethyl acetate extract
significantly improved hepatic necrosis, which coincided with simultaneous
reduced expression of oxidative stress biomarkers, 4-hydroxynonenal (4-
HNE) and 3-nitrotyrosine (3-NT), and restored P450 2E1 (CYP2E1) expression
(Rashed et al., 2014). Furthermore methanolic extract provides protection
against iron induced liver injury. Additional iron deposition in the liver
catalyses the production of ROS which in turn initiate oxidative damage of
protein and nucleic acids leading to several diseases. Methanolic extract of
T. belerica fruit has both reducing power as well as iron chelating activity
and thereby reduces the toxic level of iron in iron overload mice and
hence protects liver from oxidative stress and fibrosis. Its administration
significantly lowered serum enzyme and serum ferritin levels, which act as a
indicators of severe iron overload (Hazra et al., 2012)
Antimicrobial activity
Infectious diseases have become the major concern for public health
issues because of the emergence of drug resistant strains with less
susceptibility to antibiotics. T. belerica has shown potent action against
infectious agents in vitro. Fruit extract contains phenol, tannins, alkaloid
and flavonoids. Alkaloid could be responsible for inhibiting the microorganism
by impairing the enzymes involved in energy production, interfering with
the integrity of cell membrane and structural component synthesis. Tannins
in the fruit extract of T. belerica could be implicated in preventing the
development of microorganisms by precipitating the microbial protein and
making nutritional proteins unavailable for them (Hung and Chung, 2003).
Tannins have been found to form irreversible complexes with proline rich
proteins resulting in the inhibition of cell protein synthesis (Hagerman and
Butler, 1981). Coagulase is major virulence factor of S. aureus which converts
the host plasma fibrinogen to fibrin, forming blood clots. T. belerica extract
inhibit the activity of this enzyme when S. aureus grown in the presence of T.
belerica extract. The lower MIC values of crude and methanol extracts against
S. aureus suggested the efficacy of T. belerica phytoconstituents (Elizabeth,
2005). T. belerica aqueous fruit extract has shown activity against numerous
pathogenic bacteria viz., Escherichia coli, Pseudomonas aeruginosa, Klebsiella
pneumonia, Shigella flexneri, and Salmonella typhi (Devi et al., 2014). In a study
conducted by Saraphanchotiwitthaya et al. (2008), stem and leaf extracts of

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T. belerica also showed antibacterial activity against many Gram positive and
Gram negative bacteria including Corynebacterium rubrum, Staphylococcus
epidermidis, K. pneumonie, E. coli and S. typhimurium. None of these studies
identified the antibacterial components. However, studies have demonstrated
that antibacterial activity was associated with the polar extracts (Aneja and
Joshi, 2009; Aneja et al., 2012).
Antidiabetic activity
Diabetes refers to a group of metabolic disorders that result in increased
blood glucose level, either because the pancreas does not produce enough
functional insulin (type 1 diabetes), or because cells do not respond to the
insulin which is produced (type 2 diabetes) (Jacqueline et al., 1997). Excessive
amount of glucose reaching mitochondria lead to an overdrive of the electron
transport chain, resulting in overproduction of superoxide anions normally
scavenged by mitochondrial SOD enzyme. When the later fails, oxidative
stress develops and it was proposed that this mechanism is responsible for
the activation of all major diabetic complications involving glycation, and
sorbitol pathways etc. (Nishikawa et al., 2000). T. belerica also shows
antidiabetic activity. Administration of different doses of hexane, ethyl
acetate and methanolic fruit extracts of T. belerica for two months in
Streptozotocin induced diabetic rats expressively improved the plasma insulin,
C-peptide, glucose tolerance levels, body weight andserum total protein.
Moreover plant extract also reduced the cholesterol, urea, uric acid and
creatinine levels in serum in diabetic rats (Latha and Daisy, 2010). It has
been reported thatcontinuous administration of 75% T. belerica methanolic
extract blocks hyperglycaemia in diabetic rats via its antioxidant activity
(Sabu and Kuttan, 2009). Remarkable decreases in free radicals, and increased
glutathione, superoxide dismutase, catalase, glutathione peroxidase and
glutathione reductase activities, were observed in diabetic rats following T.
belerica extract treatment. T. belerica fruit aqueous extract stimulated insulin
secretion from a pancreatic â-cell line to a similar extent to glibenclamide
(Kasabri et al., 2010). The aqueous extract also showed insulin derivative
activity, improving glucose uptake into 3T3-L1 adipocytes and declining
starch absorption and protein glycation.
Angiogenic activity
Angiogenesis represents an excellent therapeutic target for the treatment
of cardiovascular diseases. It is a potent physiological process that underlies
the natural manner in which our bodies respond to a decrease of blood
supply to vital organs, namely the production of new collateral vessels to
overcome the ischemic state. T. belerica leaf ethanolic extract has shown
angiogenic activity in mice using in vivo sponge implantation assay. Gelatin

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sponge with or without ethanolic extract of T. belerica leaf was
subcutaneously injected into Swiss albino mice and 14 days later, the implanted
sponges in mice was excised and histologically examined. Gelatin sponges
alone were pale in their color indicating no or less blood vessel formation
while sponges mixed with leaf ethanolic extract appeared dark-red in color.
The stained section showed that sponge containing ethanolic extract had
produced more vessels in gels than sponges alone. The new vessels were
abundantly filled with intact RBCs, which indicated the formation of a
functional vasculature inside the sponges, and blood circulation in newly
formed vessels by angiogenesis, induced by ethanolic extract of T. belerica
leaf. The extract also caused marked enhancement in hemoglobin content.
These results revealed profound angiogenic potential in T. belerica ethanolic
leaf extract (Prabhu et al., 2012).
Antithrombotic and thrombolytic activity
Atherothrombotic diseases such as myocardial or cerebral infarctions
are serious consequences of the thrombus formed in blood vessels. A
blood clot (thrombus) formed in the circulatory system due to failure
of haemostasis causes vascular blockage. Thrombolytic agents are used to
dissolve the previously formed clots in the blood vessels. (Prasad et al., 2007).
There are reports suggesting thrombolytic and antithrombotic activity in T.
belerica fruits possess. However in vivo clot dissolving properties and active
component of T. belerica for clot lysis are yet to be discovered. Ansari and
coworkers (2012) used an in vitro model to check the clot lysis and
antithrombotic effect of alcoholic and aqueous extracts of T. belerica fruits.
They used streptokinase as a positive control. The study revealed that extracts
delayed the clot formation in dose dependent manner. Maximum delay (>90
min) in clot formation was observed at an extract concentration of 0.20 mg/
dl which is comparable to the activity shown by streptokinase. However for
thrombolytic activity, the clot dissolution time was reported to be about 60
min at 1.0 mg/dl concentration of both the extracts.
Wound healing activity
Wound healing is a complex phenomenon which includes a number
of processes such as migration and proliferation of both epithelial and
connective tissues, formation of extracellular matrix proteins, alteration of
connective tissue, parenchymal components, collagen synthesis and acquisition
of wound strength. Saha et al. (2011) have reported the wound healing
potential of T. belerica extract in rabbit model. Extract paste (500mg/animal)
was applied to skin incision from the dorsal area just behind the shoulders
of rabbit. Significant increase in the levels of hydroxyproline, DNA and uronic
acid contents and improvement on maturation, wound contraction and

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epithelialization was observed between 4 to 12 days. The study suggested
that the herbal paste prepared from T. chebula and T. belerica enhanced
fibroblast function, improved production of glycosaminoglycan and
deposition of collagen which is required for wound healing and may be
useful as an adjuvant in wound healing process.
Anticancer activity
Proto-oncogenes and tumour suppressor genes are responsible for
encoding proteins that regulate cell division/cell cycle, as well as for the
repair of damaged DNA and programmed cell death by apoptosis. Mutations
within these genes have been implicated in the onset of cancer (Hanahan
and Weinberg, 2000). These cells fail to recognize signals that restrict cell
division, resulting in uncontrolled cell growth. In tumour genesis, multiple
genes may be altered and transmitted to daughter cells, which subsequently
escape normal growth restraints and form a tumour that may be benign or
malignant. T. belerica extracts have shown growth inhibitory activity,
with a certain degree of selectivity against the lung (A549) and liver
(HepG2) cancer cell lines. Combination of T. belerica with cisplatin or
doxorubicin also demonstrated synergistic effects in inhibiting growth of
A549 and HepG2 cells (Pinmai et al., 2008). Further study by Laila and Amal
(2014) have shown higher cytotoxic response of 70% methanolic extract
(IC50=19.35 ìg/ml) against the HepG-2 cell line followed by ethyl acetate
(IC50=24.5 ìg/ml) and butanol fractions (IC50=28.6 ìg/ml). Other workers have
also reported cytotoxicity of extracts against nine human cancer cell lines,
including cancers of colon (HCT-16 and Colo-205), lung (A549), breast (T47D
and MCF-7), prostate (PC-3), and leukemia (THP-1, HL-60 and K562) by
using SRB and MTT assays. The study revealed that the T. belerica extract
inhibited the cell proliferation of above mentioned cancer cell lines in a
concentration dependent manner. DNA content analysis by flow cytometry
indicated that the extract was responsible for blocking G0/G1 phase of the
cell cycle and thereby inhibited cell viability of leukemia (HL-60 and K562)
cells (Kawthar et al., 2015). These findings suggested that T. belerica extracts
have potent anticancer activity.
Antispasmodic and bronchodilatory activity
T. belerica fruit crude extract promotes relaxation of spontaneous
contractions in isolated rabbit jejunum. It also reverses the carbachol and K+-
induced contractions in a pattern similar to that of dicyclomine. Crude extract
shifts the Ca2+ concentration-response curves to right, like nifedipine and
dicyclomine. In vivo study in rodents revealed that crude extract of T. belerica
also possessed protective effect against castor oil-induced diarrhea and
carbachol-mediated bronchoconstriction. In guinea-pig trachea, crude extract

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relaxed the carbachol-induced contractions, shifted carbachol-curves to right
and inhibited the contractions of K+. Anticholinergic effect was distributed
both in organic and aqueous extracts, while calcium channel blocking was
present in the aqueous extract (Gilani et al., 2008).
Immunomodulatory activity
A chemical agent that modifies the immune response or the functioning
of the immune system is referred as immunomodulator. It is well known
that macrophages play a significant role in the defense mechanism against
host infection and killing tumor cells. T. belerica fruit extracts possess
immunomodulatory activity which is proved by phagocytic and lymphocyte
proliferation activity of fruit methanolic extract on the mouse. Methanolic
extract has been reported to stimulate the production of superoxide anions
and acid phosphatase and hence promotes macrophage phagocytosis. In
lymphocyte proliferation assay, the extract with phytohemagglutinin exhibited
maximal activation. With concanavalin A, lipopolysaccharide and pokeweed
mitogen, similar activation of lymphocyte proliferation was observed.
However, at low concentrations, T. belerica extract with concanavalin A and
pokeweed mitogen caused suppressant activity (Saraphanchotiwitthaya et
al., 2008). Acetone extract of T. belerica has been shown to enhance the B- and
T-cells proliferation along with increased IL-10 secretion whereas it reduced
the production of IFN-ã and IL-2 (Saraphanchotiwitthaya and Ingkaninan,
2014).
Antihypertensive activity
The aqueous-methanolic extract of T. belerica fruit caused a dose-dependent
reduction in the arterial blood pressure of rats. The extract was tested in
two different types of vascular tissues. In isolated guinea-pig atria, extract
inhibited the force and rate of atrial contractions. Whereas, in rabbit thoracic
aorta, crude extract relaxed the phenylephrine and K+ induced contractions
as well as suppressed the phenylephrine control peaks in the Ca2+ free
medium, similar to that caused by verapamil (Khan and Gilani, 2008).
CONCLUSION
This chapter has summarized the therapeutic potential of T. belerica. The
vast study done on the plant proved that it has important phytoconstituents
like, bellericanin, ellagic acid, gallic acid, termilignan, thannilignan, flavone
and anolignan B, tannins, ellargic acid, ethyl gallate, galloyl glucose and
chebulaginic acid, phenyllemblin, â- sitosterol. T. belerica has pharmacological
attributes such as antioxidant, anticancer, antidiabetic, wound healing,
antibacterial, anti-inflammatory and hepatoprotective potential. Presence of
various phytochemicals finds correlation with the medicinal activities.

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Characterization of bioactive compounds is needed to fulfil the gap in
understanding the pharmacological implications of disease management.
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Corresponding author: Dr. Abhay K. Pandey, Department of Biochemistry,
University of Allahabad, Allahabad-211002, India
Email: akpandey23@rediffmail.com