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2013 Boletn Latinoamericano y del Caribe de Plantas Medicinales y Aromticas 12 (3): 209 - 219
ISSN 0717 7917
www.blacpma.usach.cl
Revisin | Review
[Fruta de la estrella (Averrhoa carambola L.): Desde los usos tradicionales a las actividades farmacolgicas]
Sultan Ayesh Mohammed SAGHIR1, Amirin SADIKUN2, Kooi-Yeong KHAW1 & Vikneswaran MURUGAIYAH1
1
Discipline of Pharmacology, School of Pharmaceutical Sciences, Universiti Sains Malaysia, Penang, Malaysia
2
Discipline of Pharmaceutical Chemistry, School of Pharmaceutical Sciences, Universiti Sains Malaysia, Penang, Malaysia
Contactos | Contacts: Sultan Ayesh Mohammed SAGHIR - E-mail address: Sultan_a1976@yahoo.com
Abstract
Averrhoa carambola L. (Oxalidaceae), commonly known as star fruit bears a great significance in traditional medicine. Traditionally, A. carambola was used
in ailments such as arthralgia, chronic headache, boils and pyodermas, colds, cough, epistaxis, spermatorrhea, fever, food poisoning, gastroenteritis, malaria,
malarial splenomegaly, oliguria, postpartum edema, sore throat, subcalorism and traumatic injury. Pharmacological investigations on A. carambola have
demonstrated anti-inflammatory, antimicrobial, antifungal, antitumor and anti-ulcer activities. In addition, the plant possesses hypocholesterolemic,
hypoglycemic, hypotensive, nephrotoxic, neurotoxic, negative inotropic and chronotropic effects. Phytochemical investigations have shown the presence of
saponins, tannins, alkaloids and flavonoids. This review is an effort to update the pharmacological activities and clinical studies on A. carambola.
Resumen
Averrhoa carambola L. (Familia: Oxalidaceae), comnmente conocida como fruta de la estrella tiene una gran importancia en la medicina tradicional. La
Medicina Tradicional reporta el uso de A. carambola en dolencias tales como: artralgia, dolor de cabeza crnico, fornculos y piodermas, resfriados, tos,
epistaxis, espermatorrea, fiebre, intoxicacin alimentaria, gastroenteritis, malaria, paludismo, esplenomegalia malrica, oliguria, edema post-parto, dolor de
garganta , subcalorismo y lesiones traumticas. Investigaciones farmacolgicas en A. carambola han demostrado efectos anti-inflamatorios, antimicrobianos,
antitumorales, antifngicas, y actividades anti-lcera, hipocolesterolmico, hipoglucemiante, hipotensor, nefrotxicos, y efectosneurotxicos y cronotrpicos
negativos. Proyecciones preliminares fitoqumicas han demostrado la presencia de saponinas, taninos, alcaloides y flavonoides. Esta revisin constituye un
esfuerzo para actualizar las actividades farmacolgicas y estudios clnicos sobre A. carambola.
209
Saghir et al. Averrhoa carambola L.: from traditional uses to pharmacological activities
and total phenolics contents were found to be 54.45 storage, respectively. The results showed a substantial
0.43 g of gallic acid equivalent/100 g of fruit. decrease in the hepatic acetylcholinesterase activity in
Moresco et al., (2012) reported isolation of - rats treated with star fruit juice highest activity was
sitosterol from the n-hexane fraction; apigenin-6-C-- observed for the freshly prepared juice.
L-fucopyranoside and apigenin6-C-(2"-O--L-
rhamnopyranosyl)--L-fucopyranoside from the ethyl Antimicrobial and antifungal activity
acetate fraction, and a new compound apigenin6-C- Mia et al., (2007) isolated two compounds p-
(2"-O--L-rhamnopyranosyl)--D-glucopyranoside anisaldehyde and -sitosterol from the bark of A.
from the n-butanol fraction. The antioxidant potential carambola. The petroleum ether, carbon tetrachloride
of the fractions was examined using the DPPH radical and chloroform fractions of the methanol extract of A.
scavenging assay and reducing power of iron (III) to carambola when subjected to antimicrobial screening
iron (II) ions. The ethyl acetate and n-butanol fractions at 400 g/disc demonstrated mild inhibition on
showed the highest antioxidant potential to scavenge microbial growth. The average zone of inhibition
DPPH, with the IC50 values of 90.92 and 124.48 produced by the petroleum ether, carbon tetrachloride
g/mL, respectively. In the assay of reducing power, and chloroform soluble fractions were 8-12 mm, 8-12
these fractions presented 135.64 and 125.12 mg/g of mm, and 8-15 mm, respectively. The petroleum ether
ascorbic acid equivalents, respectively. The extract moderately inhibited the growth of E. coli and
antioxidant activity exhibited a significant correlation S. dysenteriae having the zone of inhibition of 12 mm
with the phenolic content (r2 = 0.997), but a poor each. On the other hand, the chloroform soluble
correlation with the flavonoids content (r2 = 0.424). fraction strongly inhibited the growth of E. coli with
The n-hexane fraction was the only fraction to show zone of inhibition 15 mm. In the case of fungi, mild
toxicity on A. salina with LC50 of 800.2 g/mL. inhibitory activity was exhibited by all extractives.
The LC50 values obtained from cytotoxicity evaluation
Anti-inflammatory activity were 0.32, 0.70, 0.06 and 3.14 g/mL for standard
Cabrini et al., (2011) examined the ethanol extract of vincristine sulfate, petroleum ether, carbon
A. carambola leaves, its hexane, ethyl acetate and tetrachloride and chloroform soluble fractions,
butanol fractions and two isolated flavonoids, respectively.
apigenin-6-C--l-fucopyranoside and apigenin-6-C-
(2-O--l-rhamnopyranosyl)--l-fucopyranoside for Antitumor activity
anti-inflammatory activity. The ethanol extract Li et al., (2012) studied the biotransformation of
reduced edema in a dose-dependent manner, resulting dihydro-epi-deoxyarteannuin B by using suspension-
in a maximum inhibition of 73 3% and an ID50 value cultured cells of A. carambola. One novel
of 0.05 (range: 0.020.13) mg/ear. Myeloperoxidase sesquiterpene, 7-hydroxy-dihydro-epideoxyarte-
activity was also inhibited by the ethanol extract, annuin B, and one known sesquiterpene, 3--hydroxy-
resulting in a maximum inhibition of 60 6% (0.6 dihydro-epideoxyarteannuin B, were obtained upon
mg/ear). The tested fractions inhibited edema the addition of dihydro-epi-deoxyarteannuin B. The
formation and myeloperoxidase activity, the ethyl study concluded that, cultured cells of A. carambola
acetate fraction was the most effective fraction, have the capacity to hydroxylate sesquiterpene
resulting in inhibition levels of 75 5 and 54 8% for compounds in a regio- and stereoselective manner.
edema formation and myeloperoxidase activity, The inhibitory effects of 7-hydroxy-dihydro-
respectively. However, the isolated compounds did not epideoxyarteannuin B and 3--hydroxy-dihydro-
show any substantial anti-inflammatory activity. epideoxyarteannuin B on proliferation of K562 and
HeLa cell lines were (59.29 0.99, 84.04 0.27
Acetylcholinesterase inhibitory activity mol/mL) and (40.63 1.45, 41.54 0.82 mol/mL) ,
Teh et al., (2010) investigated the effects of A. respectively.
carambola juice kept at different storage conditions
on the activity of acetylcholinesterase in various Anti-ulcer activity
organs of Sprague Dawley (SD) rats. Three groups (5 Goncalves et al., (2006) examined the water-alcohol
animals per group) of rats were administered with extract of leaves of A. carambola for its anti-
distilled water, and different star fruit preparations, ulcerogenic potential. The ethanolic extract at doses of
freshly prepared star fruit juice and after 3 hours 800 and 1200 mg/kg p.o., only showed significant
anti-ulcer activity in the acidified-ethanol-induced degrees); depressed the cardiac rate from 136 17 to
ulcer model in rats. However, the extract did not show 89 14 bpm, increased the QRS complex duration
any activity in the indomethacin and acute stress from 27 3.1 to 59 11 ms and increased the QT
ulcerogenic models. Thus, the study concluded interval from 229 23 to 264 19 ms. Additionally, it
ethanolic extract of A. carambola as having low anti- increased the conduction time between the right atrium
ulcer activity. and the His bundle (27 6.5%), reduced the
intraventricular pressure (86 6%) and decreased the
Negative inotropic and chronotropic effect conduction velocity of atrial impulse (17 3%).
Vasconcelos et al., (2005) examined the atrial However, the conduction time from the His bundle to
isometric force in stimulated left atria and determined the right ventricle was not altered. Atropine sulfate did
the chronotropic changes in spontaneously beating not change either the electrocardiographic parameters
right atria. A. carambola leaves extracts (1.5 mg/mL) or the intraventricular pressure effects promoted by the
abolished the contractile force in a concentration- A. carambola aqueous extract. Thus, the study
dependent manner in cardiac contractility in the suggested avoiding the use of such extracts since it can
guinea-pig atria. Among the methanolic, ethanolic, induce electrical and mechanical changes in the
aqueous, and acetic acid extracts, the aqueous extract normal heart.
was found to be the most potent (EC50 = 520 94
g/mL). The aqueous extract abolished the positive Hypotensive activity
Bowditch staircase phenomenon and reduced the Soncini et al., (2011) studied the hypotensive effect of
inotropic response to CaCl2, events that are dependent the aqueous extract of A. carambola and its
on the cellular Ca2+ inward current. In spontaneously underlying mechanisms using isolated rat aorta. In
beating atria, the aqueous extract promoted a negative vitro, the aqueous extract caused a reduction in the
chronotropic effect that was antagonized by 0.1 M Emax response to phenylephrine without a change in
isoproterenol bitartrate. The EC50 of the aqueous sensibility. Furthermore, in a depolarized Ca2+-free
extract increased from 133 58 to 650 100 g/mL medium, the aqueous extract inhibited CaCl2-induced
in the presence of this agonist. contractions and caused a concentration-dependent
Subsequently, Vasconcelos et al., (2008) rightward shift of the response curves, suggesting that
investigated the effects of the aqueous extract of A. the aqueous extract inhibited the contractile
carambola leaves on the cellular calcium influx by mechanisms involving extracellular Ca2+ influx. The
examining the left atrium of guinea pig and the study concluded the aqueous extract to be hypotensive
pituitary GH3 cells. In the atrium, the aqueous extract in nature and suggested the effects to be in part, due to
(1500 g/mL) shifted to the right the concentration- the inhibition of Ca2+, which is in agreement with its
effect curve of the positive inotropic effect produced uses in traditional medicine.
by () BAY K 8644, an L-type calcium channel
agonist. The aqueous extract increased Hypocholesterolemic activity
EC50 (concentration required to promote 50% of the Wu et al., (2009) examined the potential
maximum effect) of the inotropic effect of BAY K hypocholesterolemic activity of different insoluble
8644 from 7.8 0.38 to 115.1 0.44 nM. In GH3 cells fibers prepared from A. carambola with or without
treated with 500 g/mL of aqueous extract, the L-type micronization processing. After micronization, the
calcium inward current declined by 30%. The extract cation-exchange and water-holding capacities of the A.
did not change the voltage correspondent to the peak carambola pectic polysaccharide-rich insoluble fibres
current. It was suggested that, at least in part, the were effectively increased from 8.5 to 22.4 mL/g. The
negative inotropic effect of aqueous extract on the A. carambola microsized insoluble fibers reduced the
guinea pig atrium is due to a reduction of the L-type concentrations of serum triglyceride by and total
calcium current. cholesterol by 15.6% and 15.7%, respectively by
means of enhancing the excretion of cholesterol and
Electrophysiological effects bile acids in the feces. The study suggests a new
Vasconcelos et al., (2006) examined the effects of the approach of micronization of the fruit which may help
aqueous extract of A. carambola leaves on guinea pig to improve physiological functions of food fibers in
heart. In this study, the aqueous extract induced many fiber-rich functional food applications. The study also
kinds of atrioventricular blocks (1st, 2nd, and 3rd indicates that the particle size is an important factor in
affecting the characteristics and physiological renal function must also be warned to avoid ingestion
functions of insoluble fibers. of large amounts of the fruit or juice especially on an
empty stomach.
Hypoglycaemic activity
Ferreira et al., (2008) examined the effects of the Neurotoxic effect
hydroalcoholic extract of leaves of A. carambola L. Carolino et al., (2005) examined the effects of a
on fasting blood glucose. The hydroalcoholic extract neurotoxic fraction isolated from A. carambola on
treated animals showed significantly lower fasting GABAergic and glutamatergic transmission systems.
blood glucose (p < 0.05). In contrast, livers from The fraction was obtained by sequential
hydroalcoholic extract of these animals showed chromatography of the aqueous extract on anion
significantly higher (p < 0.05) glucose production exchange column, then on cation exchange column
from L-alanine. This effect was mediated, at least part and, finally on reversed-phase high performance liquid
of it, by an activation of the catabolism of L-alanine chromatography (HPLC). The fraction did not affect
inferred by the increased hepatic urea and L-lactate GABA/glutamate uptake or release, or on glutamate
production. Unlike L-alanine, the glucose production binding, but effected GABA binding in a
from L-glutamine, L-lactate and glycerol was not concentration-dependent manner (IC50 0.89 mM).
affected by the treatment. Likewise, the Video-electroencephalogram recordings showed that
hydroalcoholic extract treatment did not affect the cortical administration of neurotoxic fraction, induced
glucose uptake in soleus muscles, inferred by the behavioral changes in animals, including tonic-clonic
incorporation of [14C]-glucose to glycogen (glycogen seizures, evolving into status epilepticus, accompanied
synthesis) and [14C]-lactate production. Thus, the by cortical epileptiform activity. The neurotoxic
study suggests that reduction of fasting blood glucose fraction has not yet been chemically characterized but
promoted by the treatment with hydroalcoholic extract the preliminary data suggested that it contains a non
of A. carambola was not mediated by an inhibition of peptide molecule differing from oxalic acid and
hepatic gluconeogenesis and/or an increased glucose bearing a molecular weight less than 500.
uptake by muscles.
Chau et al., (2004b) investigated the PHYTOCHEMISTRY:
hypoglycaemic effects of several insoluble fiber-rich Chemical constituents isolated from A. carambola
fractions including insoluble dietary fiber, alcohol- Averrhoa carambola has been the subject of
insoluble solid and water-insoluble solid obtained phytochemical studies since late 1970s. The following
from the pomace of A. carambola , by some in vitro are the chemical constituents isolated for A.
methods. It was found that the three insoluble fiber- carambola.
rich fractions could effectively adsorb glucose, retard OH
glucose diffusion, postpone the release of glucose
from starch, and inhibit the activity of -amylase to HO OH
different extents. The hypoglycemic effects of these
insoluble fiber-rich fractions were significantly (P < OH
0.05) stronger than that of cellulose. Thus, it was HO
concluded that these fiber-rich fractions could be
O
O
incorporated as low-calorie bulk ingredients in high-
fiber foods to reduce calorie level and assist the
control of blood glucose level. OH O
Nephrotoxic effect
Neto et al., (2009) studied the effects of A. carambola
OH O
fruit on patients with renal failure, who are not yet on OH OH
dialysis and concluded that the fruit and its juice Apigenin-6-C-(2 -O- -L-rhamnopyranosyl)--L-
induces nephrotoxicity and neurotoxicity, which may fucopyranoside (Araho et al., 2005)
sometimes be fatal. Patients with chronic kidney
disease (stages 35 but not on dialysis) should be
prohibited from eating the fruit. People with normal
OH O OH
HO O
HO OH
O OH O OH
Me OH
OH Gallic acid (Guanghou and Lai, 2004)
HO
Apigenin-6-C--L-fucopyranoside (Araho et al.,
OH
2005) HO
OH
OH
HO
HO O O
O HO O
HOH2C OH OH
HO O OH O Quercetin-O--D-glucoside (Tiwari et al.,1979)
HO
OH
OH
HOHO OH
HO O OH
Apigenin- 6-C-(2-O--L-rhamnopyranosyl)--D-
glucopyranoside (Henrique et al., 2011)
O
O H OH O
HO
O
HO
OH
OCH3
Quercetin-3-O- rhamonoside (Nina et al., 2006)
P-Anisaldehyde (Mia et al., 2007)
OH
HO O+
OH
H O
H OH O OH
O
HO HO
OH
-amirin (Tadros et al., 2004)
OH
Cyanidin 3-O-- D- glucoside
(Gunasegaran, 1992)
Cl- OH
H HO O+
OH
O
HO
-sitosterol (Ranganayaki et al., 1980) OH O OH
O
HO
OH
OH
Cyanidin-3, 5-O--D-Diglucoside
(Gunasegaran, 1992)
H
OH
H HO
HO
OH
HO O -Galactosidase
OH Balasubramaniam et al., (2005) isolated -
Galactosidase (EC. 3.2.1.23) from A. carambola fruit
O OH and fractionated it using a combination of ion
exchange and gel filtration chromatography into four
OH O O isoforms, -Galactosidase I, II, III and IV. The -
O galactosidases exhibited the molecular weights 84, 77,
HO 58 and 130 kDa, respectively. -Galactosidase I, was
the most prominent isoform. The purified -
O galactosidase I was highly active in hydrolyzing (1
HO 4) -linked spruce and a mixture of (1 3)- and (1
HO OH OH 6) -linked gum arabic galactans. The -
Rutin (Tiwari et al., 1979) galactosidase I also exhibited the capacity to solubilize
and depolymerize structurally intact pectins as well as
to modify alkaline-soluble hemicelluloses, indicating
in part changes that occur during ripening.
HO
OH Pharmacognostic and phytochemical analysis
O Thomas et al., (2008) conducted preliminary
O pharmacognostic and phytochemical analysis and
showed the presence of saponins, tannins, alkaloids
HO and flavonoids. Furthermore, the study revealed that
OH the water-soluble and alcohol soluble extractive values
decreased gradually with ripening of fruit.
Vitamin C (Guanghou and Lai, 2004)
Analysis of oxalic acid
Wilson et al., (1982) quantified oxalic acid in 15
C13-aroma compounds Florida-grown A. carambola cultivars using simple
Herderich et al., (1992) reported identifications of and rapid high-performance liquid chromatographic
glycosidically bound constituents from star fruit (A. (HPLC) method. Oxalic acid levels were found to vary
carambola L.) using HRGC and HRGC-MS among the cultivars examined from 0.08 to 0.73 g per
techniques. The constituents were obtained from the 100/g of fruit.
extracts by Amberlite XAD-2 adsorption followed by
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