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JJBS
Volume 7, Number 4, December .2014
ISSN 1995-6673
Pages 233 - 244
Jordan Journal of Biological Sciences Review
Phytochemistry, Pharmacological Properties and Industrial
Applications of Rhus coriaria L. (Sumac)
Ibrahim M. Abu-Reidah, Rana M. Jamous and Mohammed S. Ali-Shtayeh*
Biodiversity and Biotechnology Research Unit, Biodiversity and Environmental Research Center-BERC, Til, Nablus, Palestine.
Abstract
Rhus coriaria L. (Sumac), belonging to the Anacardiaceae family, is an important species and is the most used species of
the genus Rhus in the Mediterranean region since antiquity. Sumac has long been used as a flavoring spice, drink,
appetizer, and as acidulant in food recipes, in addition to its use in traditional medicine. The role of the plant in leather and
textile industry is also significant. R. coriaria is very rich in phenolics mainly and tannins as well as flavonoids; let alone
its abundance with organic acids. The leaves and fruits of R. coriaria are recognized to have defensive and beneficial
effects on a wide set of diseases, including, but not limited to, diabetes mellitus, cancer, stroke, oral-diseases,
inflammation, diarrhea, and dysentery. On the other hand, Sumac extracts were found to possess a potential antiviral,
antimicrobial, antifungal, antioxidant and hypolipidemic activities. This review updates the current phytochemical,
biological and therapeutic knowledge that so far exists on R. coriaria. It also aims at highlighting the importance of Sumac
extracts as a promising and potential source of functional ingredients and nutraceuticals with desirable bioactivities,
prompting the further use of Sumac in food preservation, pharmacology and functional food industries.
Keywords: Rhus Coriaria L. (Sumac); Anacardiaceae; Pharmacology; Phytochemistry; Antioxidant, Antimicrobial, Tannins; Organic
Acids.
* Corresponding author. e-mail: msshtayeh@yahoo.com.
1. Introduction
Rhus coriaria L. (Tanner’s Sumac or Sicilian Sumac)
(Figure 1) grows wild mainly in the Mediterranean
bordering countries, South Europe, North Africa, Iran and
Afghanistan (Nasar-Abbas and Halkman, 2004). The
plant is also originated in temperate and tropical regions
worldwide, often growing in areas of marginal
agricultural capacity. Sumac is the common name of the
Rhus genus, which comprises 91 of accepted species
names in the Anacardiaceae (The plant list 2010). The
name "Sumac" comes from "summāq" which means
"dark red" in Arabic and Syriac (Quattrocchi, 1999). Rhus
coriaria has been used in spice blends and in traditional
medicines for hundreds of years (Ali-Shtayeh et al.,
2008). The word "sumac" will be henceforth used to
indicate the spice product of R. coriaria.
Sumac has long been used as a seasoning spice, either
in pure form or in combination with other spices, as a
drink, appetizer, sauce, and also as a natural acidulant in
food recipes (Abu-Reidah et al., 2014). It is worth noting
that R. coriaria has an attractive economic importance
due to its increasing use in cosmetic and pharmaceutical
industries, coloring or preservation of foods, veterinary
practices and animal skins processing technology (Bahar
and Altug, 2009; Kizil and Turk, 2010). In the past, the
leaves, bark, roots and branches of R. coriaria were used
in dyeing as mordant natural dyes. In addition, R. coriaria
possesses high fixation, retention and fungal resistance
properties, and is useful against wood decay (Sen et al.,
2009). So far, a big deal of nutritionally and medicinally
considerable metabolites (such as phenolic acids, tannins,
anthocyanins, organic acids, proteins, essential oils, fatty
acids, fiber, and minerals) have previously been identified
from various parts of R. coriaria (Shabir, 2012).
Figure 1. Rhus coriaria L. plant and fruits; a. Sumac plant
(leaves, fruits, and flowers) b. Sumac fruits c. Sumac fruit
powder.
© 2014 Jordan Journal of Biological Sciences. All rights reserved - Volume 7, Number 4
234
Rhus coriaria has been reported to possess
antibacterial (Aliakbarlu et al., 2014; Kossah et al., 2013;
Ali-Shtayeh et al., 2013; Iauk et al., 1998), antifungal
(Onkar et al., 2011), antioxidant (Aliakbarlu et al., 2014),
anti-inflammatory (Panico et al., 2009), DNA protective
(Chakraborty et al., 2009), vascular smooth muscle cell
migration inhibition (Zargham and Zargham, 2008),
hypoglycemic (Anwer et al., 2013; Golzadeh et al., 2012),
and hypolipidemic activities (Madihi et al., 2013).
Moreover, this plant has traditionally and widely been
used in the treatment of diabetes (Mohammadi et al.,
2010), stroke and cancer (Zargaran et al., 2013), in the
digestive tract maladies such as ulcer, diarrhea, stomach
tonic, stomachache, and hemorrhoids pain (Ahmad et al.,
2013), diuresis, anorexia, measles, smallpox,
hyperglycemia, gum ailments (Abu-Reidah et al., 2014),
hypertension (Polat et al., 2013), atherosclerosis (Setorki
et al., 2012), dysentery, conjunctivitis, hematemesis,
hemoptysis, and leucorrhea, dermatitis, ophthalmia, and
liver disease, besides it was used also for throat treatment
and in addition as abortifacient. Other medicinal uses
have also been reviewed including weight loss, treatment
of skin, hair, burns, digestive system, headache and
temperature reducing (Ali-Shtayeh et al., 2013). R.
coriaria leaves have been reported to be useful in the
treatment of chronic diseases as osteoarthritis and may
form a potential application in joint disease therapy
(Panico et al., 2009). It was reported that the acute
consumption of sumac might have a protective effect on
some of the risk factors of atherosclerosis, oxidative stress
and liver enzymes, due to high fat food stress (Setorki et
al., 2012).
The present review suggests increasing the size of
research on and development efforts for obtaining
bioactive whole extracts or individual functional
components from R. coriaria, which makes the plant an
appealing species of Rhus, as well as a source of
functional food and nutraceutical ingredients.
Additionally, it may help to further establish mechanisms
of action of R. coriaria components, leading to a better
understanding of the plant extracts and components’
bioactivity. Moreover, this review attempts to focus on
the traditional use of R. coriaria based on actual research
data for its multivalent actions as health promoting dietary
additives as well as putative therapeutic agents. In the
current work, we critically review the so far known
biological activities of R. coriaria extracts in an attempt
to update the current knowledge on the plant.
2. History of Sumac use
Sumac has been used as a natural and traditional
source of medication in different dietary cultures all over
the world; the use of the plant in seasonings and flavoring
agents has been the mainstay of indigenous remedies
across the world.
Sumac is used as a spice, and has been used in cooking
for millennia. About 2,000 years ago, the Greek physician
Pedanius Dioscorides (40-90 A.D.) wrote in his
voluminous "De Materia Medica" ("Of Medical Matters")
about the healthful properties of Sumac, principally as a
diuretic and anti-flatulent (Norton, 2006).
One practice of ancient Rome continues today in
certain cuisines in which R. coriaria berries are pressed to
extract their essential oils. The oil is then mixed with
either olive oil or vinegar, depending on the type of
condiment sauce being made. Nevertheless, the medicinal
properties of R. coriaria had been noted since antiquity.
For instance, sumac was used in folk medicine for the
treatment of stroke chronic symptoms, as was described
by Avicenna (Ibn-Sina) in his well-known book, Canon of
Medicine (Zargaran et al., 2013).
Interestingly, in Iran and Palestine, sumac represents
pure ground fruit epicarps of the plant, while in Turkey
the whole fruit is ground with salt crystals (Mirhadi et al.,
2011). It is commonly used as a seasoning spice in the
Mediterranean region, especially in meat and fish dishes
(Nasar-Abbas et al., 2004). The ground sumac seeds,
mixed with olive oil, are also used in food industry in
salads and other meals (Kizil and Turk, 2010).
Today, a large mass of literature indicates that adding
sumac into food stuff or water can have beneficial effects
on human and animals (Chakraborty et al., 2009).
3. Morphological Characterization of Different Parts
of the Plant
Rhus coriaria L. is a shrub 3-4m high, the leaves
pinnate with 6-8 pairs of small oval leaflets of different
sizes, and white flowers in terminal inflorescences. The
fruits are globose, villose and reddish drupe when ripe;
with one seed, they contain tannins, essential oils, various
organic acids, anthocyanins and fixed oil. The leaves
contain gallic acid, (bi)flavonoid, sugar, wax and essential
oils (Ünver and Özcan, 2010). Generally, investigations
have focused on the tannin and flavonoid contents of R.
coriaria leaves. Physical properties, such as length (4.70
mm), weight (0.20 g), volume (19.50 mm3), geometric
diameter (3.64 mm), sphericity (0.77), and thickness (2.64
mm) of R. coriaria fruits have been estimated at 4.79 %
moisture content levels. At an identical moisture content
level porosity (68.50%), static friction (0.48-0.68), bulk
projected area (0.16 cm3), terminal velocity (3.50 m/s),
and density (304.25 kg/m3) of the fruits were also
determined (Özcan and Haciseferogullari, 2004).
4. Phytochemical Significance
In the light of the significance of sumac uses in food
seasoning, folklore medicine and industry, Rhus coriaria
has long been investigated to expose its chemical
composition. R. coriaria plant is known as an abundant
source of tannins (condensed and hydrolysable), phenolic
acids, anthocyanins, gallic acid derivatives, flavonoid
glycosides, organic acids (Abu-Reidah et al., 2014).
Parts like leaves, fruits, and seeds of R. coriaria were
reported to contain a number of phyto-constituents as
shown in Figure 2. The presence of gallotannins (mainly
hydrolysable tannins) is a characteristic property of the
Rhus genus, mostly R. coriaria species, which is an
abundant source of tannins with different isomers and
conjugations; besides, it contains other metabolites or
phytochemicals, which have been described in various
parts of the plant.
© 2014 Jordan Journal of Biological Sciences. All rights reserved - Volume 7, Number 4
235
Figure 2. Structure of some selected phytochemicals from Rhus coriaria
© 2014 Jordan Journal of Biological Sciences. All rights reserved - Volume 7, Number 4
236
Tannins are polyphenolic secondary metabolites of
plants (MW’s: 500 to 3,000), containing sufficient
hydroxyls and carboxyls’ groups (Haslam, 1989) which
form hydrogen bonds in solutions. Tannins are astringent
and bitter compounds, which can form strong complexes
with various macromolecules that bind to and can
precipitate proteins and other organic compounds
including amino acids. They play a vital role in protecting
plants from predation; and perhaps also as pesticides, as
well as in plant growth regulation (Thorington and
Ferrell, 2006). Lately, these substances have gained
attention as they may trim down the risk of chronic
diseases, by reinforcing the defenses against reactive
oxygen species (Panico et al., 2009).
The tannin compounds are widely distributed in many
plant species, where they play a role in protection from
predation, and plant growth regulation (Katie et al.,
2006).
Structurally, tannins are divided into two classes:
hydrolysable and condensed ones. Rhus coriaria has been
reported as one of the major commercial hydrolysable
tannin sources (Sarioezlue and Kivanc, 2009).
The methanol extracts from R. coriaria fruits were
reported as a rich source of natural antioxidants phenolics,
mainly tannins, which has an inhibitory function in the
migration of vascular smooth muscle cells, suggesting an
atheroprotective role for this chemical. In vitro and in vivo
studies have shown that tannins have anticarcinogenic
effects (Ram et al., 1997).
The aqueous and aqua-methanol extracts of R. coriaria
leaves and fruits were investigated using HPLC to reveal
the presence of gallotannins derivatives, namely gallic
acid (1), methyl gallate (2), digallic acid (3), tri-gallic acid
(4), and ellagic acid, together with mono- (5), di- , tri- ,
tetra- (6), penta- (7), …, deca-, undeca- and dodeca-
gallolyl glycoside derivatives as representative tannins
present in R. coriaria (Regazzoni et al., 2013). Some of
the above-mentioned galloylglucose derivatives were
reported to have the ability to reduce blood urea nitrogen
and blood pressure (Djakpo and Yao, 2010).
In fact, the galloylated-glucose derivatives were
previously studied in R. coriaria leaves using UV, paper
chromatography, and IR measurements, in addition to the
column chromatography technique which was used to
uncover the existence of flavonoid glycosides (El Sissi et
al., 1972). Flavonoid dimers (with antiviral activity) like
amenthoflavone (8), agathisflavone (9), hinokiflavone
(10), and sumaflavone (11) have also been identified in
the leaves and fruits via LC and LC-MS (Van Loo et al.,
1988; Abu-Reidah et al., 2014). Other anthocyanins were
also established: cyanidin (12), peonidin (13),
pelargonidin (14), and petunidin (15) structures and
coumarates, anthocyanins were peonidin-3-glucoside,
petunidin-3-glucoside (coumarate), delphinidin
(coumaroyl) glucosides, and cyanidin coumaroyl
glucoside. However, the presence of cyanidin-3-glucoside
(16), delphinidin-3-glucoside (17) and delphinidin (18)
has already been reported from the fruits of R. coriaria
(Mavlyanov et al., 1997).
Furthermore, some other phenolics have been isolated
from R. coriara, including gallic acid, methyl gallate,
kaempferol (19), myricetrin (20), quercetin (21), p-
benzoic acid, vanillic acid isoquercitrin, protocatechuic
acid (22), kaempferol 3-galactoside, quercetin 3-glucoside
(isoquercitrin) (23), quercetin 3-rhamnoside, myricetin 3-
rhamnoside (24), myricetin 3-glucoside (25), myricetin 3-
glucuronide, myricetin 3-rhamnoglucoside, have also
been already identified in the R. coriaria leaves and fruits
(Shabana et al., 2011; Abu-Reidah et al., 2014). The
separation of gallotannins and flavonoids was carried out
by HPLC-ESI-MS, which allowed the structure resolution
of the isobaric flavonoid glycosides.
Lately, a detailed profiling of phytochemical
compounds has been carried out by analyzing the
hydromethanolic extract of the fruits using HPLC-DAD-
ESI-MS/MS technique, where more than 200
phytochemical components have been tentatively
identified. Curiously, the occurrence of the conjugated
form of aglycone with hexose-malic moieties (24
compounds) has been very recently identified for the first
time in the Palestinian R. coriaria (Abu-Reidah et al.,
2014). In the same work, five cyanidin derivatives have
been newly detected anthocyanins in the fruit epicarps.
Moreover, the following flavonoid glycosides have been
also identified: quercetin-rhamnofuranoside (26), rutin
(27), and kaempferol 3-glucoside (Astragalin) (28).
Butein (29) is a recently identified chalconoid
derivative from R. coriaria. Notably, this compound
exhibited a significant anti-breast cancer activity (Li et
al., 2014). Another galloyl derivative compound was also
characterized in the fruits: O-galloyl arbutin (30).
Minerals are essential chemical elements for
supporting the human health, indispensably obtained from
the diet. Once minerals intake is inadequate, deficiency
symptoms may take place (McDowell, 2003). However,
minerals like potassium, calcium and magnesium were
found to be predominant in sumac. Other minerals have
also been explored, namely sulfur, cadmium, phosphor,
lead, titanium, vanadium, copper, silicon, barium,
chromium, lithium, brome, aluminum, chloride,
manganese, iron, sodium, zinc, strontium, and nitrogen
(Kizil and Turk, 2010).
On the other hand, β-caryophyllene (31) a bicyclic
sesquiterpene has been recently described to be a major
essential oil component isolated from R. coriaria (Gharaei
et al., 2013). An anti-inflammatory effect for this
terpenoid has been described elsewhere (Gertsch et al.,
2008).
Interestingly, R. coriaria fruits were found to possess
various fatty acids, including azelaic, tetradecanoic,
elaidic, stearic, eicosadienoic, arachidic, and tetracosanoic
acids, with oleic (ω 9), palmitic, and linoleic (ω 6) acids
being as major fatty acids in sumac. The polyunsaturated
fatty acid (ω 6+ ω 3) contents of the total fatty acids were
found to be between 34.84 and 37.36% (Dogan and
Akgul, 2005). The main fatty acids of sumac were found
to be: oleic (33.78-52.57%), palmitic (17.00-29.80%),
linoleic (11.60-21.90%), linolenic (0.33-1.33%) and
stearic (17 %) acids. On the other hand, linoleic (49.35-
60.60%), oleic (24.60-32.05%), palmitic (8.30-13.60%),
stearic (1.60-3.00%) and linolenic (0.46-0.74%) acids
were described to be major fatty acids of R. coriaria seeds
(Ünver and Özcan, 2010).
© 2014 Jordan Journal of Biological Sciences. All rights reserved - Volume 7, Number 4
237
It is worth noting that the major volatiles determined
from R. coriaria were aliphatic, farnesyl acetone,
aldehydes, hexahydrofarnesylacetone, and oxygenated
terpenes, among others. Terpene hydrocarbons were
reported to be the main constituents. Polyisoprenoids
from the leaves were investigated via GC–MS
(Mamatkulova et al., 2012). Α-tocopherol was found as
the predominant existing substance; besides, other minor
components, such as tocopherol mannoside,
farnesylacetate, pentadecanal, and hexadecanal, have also
been determined. D-limonene (32), a monoterpene
derivative isolated from the plant, was found to have
hypocholesterolemic effects (Golzadeh et al., 2012). A
recent study reported that cembrene (21.40 %) and β-
caryophillene (30.70 %), as main terpinoid derivatives,
are found in R. coriaria (Gharaei et al., 2013).
However, the sourness of sumac is mainly due to the
presence of organic acids, such as malic, citric and tartaric
acids (Kossah et al., 2013), while the astringent taste is
ascribed to its tannins composition. It is interesting to
know that R. coriaria fruits and seeds are incredibly rich
in antioxidants, Vitamins A and C.
5. Biological Properties
Many literature reports indicate that the addition of
sumac to the food/feed or water can impart a beneficial
effect on both human beings and animals (Capcarova et
al., 2012). Some of the recently published information
about the biological activities in literature is illustrated in
Table 1.
Table 1. Digest of reported biological activities of different used parts of Rhus coriaria L.
Pharmacological
Properties
Plant part
used
Used extract/plant
part (form)
Result/Activity
Reference
Antibacterial
activity
Fruits
Hydrodistilled extract
Demonstrated a desirable antibacterial activity
Saǧdıç, and Özcan,
2003
Fruits
Ethanol and methanol
extracts
Sumac extracts were effective against Gram positive
and Gram negative bacteria
Nasar-Abbas and
Halkman, 2004
Fruits
Ethanol 95% extract
Significant antibacterial activities against all tested
species have been shown
Nimri,et. al., 1999
Fruits
Methanol extract
A strong in vitro antioxidant activity indication of
the methanolic extract of sumac fruits
Candan, and
Sökmen, 2004
Fruits
Water extract solution
extract 0.8:10 (wt/vol)
Bacteriostatic/bactericidal effects by bacteria cycle
reduction exerted by sumac extract have
demonstrated
Gulmez, et al., 2006
Plant
Water, Methanol 80 %,
Ethanol 80 % extracts
Antibacterial activity can be exerted individually or
conjointly with other spice
Adwan, et. al., 2006
Fruits
Ethanol 80% extract
Effective antibacterial agents on both Gram-positive
and Gram-negative bacteria
Fazeli et al., 2007
Plant
Ethanol extract
R. coriaria extract can have an antimicrobial effect
on total microbial and Salmonella count in minced
meat for one week
Radmehr and
Abdolrahimzade,
2009
Leaves
Ethanol 95% extract
Showed a high antibacterial activity in comparison
with other plants
Ertürk, 2010
Plant
Ethanol 80% extract
Sumac extracts exhibited a moderate activity on
Brucella strains
Zandi, et al., 2012
Fruits
Ground and fermented
sumac
R. coriaria could decrease the formation of biofilm, a
major virulence factor in staphylococcal infections
Kırmusaoğlu, et al.,
2012
Plant
Ethanol extract
Results indicated that among other plant extracts, the
sumac one, was found to have the most potent
against: Propionibacterium acnes, S. aureus, E. coli,
P. aeruginosa
Ali-Shtayeh, et al.,
2013
Fruits
Ethanol 20% extract
A remarkable inhibitory activity was shown by
sumac extract against B. cereus. Also it strongly
inhibited the growth of H. pylori. The fruit extract
exhibited a good antioxidative capacity, justifying its
use as a natural antibacterial preservative
Kossah, et al., 2013
Plant
Water extract
Sumac water extracts showed the strongest
antibacterial activity among other 10 extracts studied.
Aliakbarlu, et al.,
2014; Aliakbarlu, et
al., 2014
Antioxidant
activity
Fruit
epicarps
Methanol extract
From results it can be noted a desirable antioxidant
activity of sumac which in turn could delay the
oxidation of palm oil
Ozcan, 2003
Plant
Ethyl acetate and 80%
methanol fractions after
initial defatting by
petroleum ether
The ethyl acetate fraction of plant materials exhibited
a noticeable antiradical activity on DPPH
Bozan, et al., 2003
Fruits
Methanol extract
Results indicate a strong in vitro antioxidant activity
of the methanolic extract of Rhus coriaria fruit based
on hydroxyl radical scavenging
Candan , 2003
© 2014 Jordan Journal of Biological Sciences. All rights reserved - Volume 7, Number 4
238
Pharmacological
Properties
Plant part
used
Used extract/plant
part (form)
Result/Activity
Reference
Fruits
Water extract
Sumac extract was more effective than BHT, and
could be added to meat products (e.g. sausage)to
enhance quality
Bozkurt , 2006
Fruits
Methanol 70% extract
Sumac extracts and fractions showed remarkable
antioxidant activity against inhibition of lipid
peroxidation and scavenging activity based on DPPH
radical assay.
Kosar, et al., 2007
Aerial
parts
Methanol 50% extract
A desirable antioxidant activity was shown
Serteser et al., 2009
Fruits
Ethanol and water
extracts
Water extracts of sumac with effective antioxidant
and radical scavenging activities as compared to
ethanol extracts.
Bursal and Köksal,
2011
Fruits
Ethanol 20% extract
Sumac fruit extract exhibited a good antioxidative
capacity also it showed a remarkable inhibitory
activity against B. cereu, besides it strongly inhibited
the growth of H. pylori.
Kossah, et al., 2013
Plant
Water extract
Sumac water extracts showed the strongest
antioxidant activity among other 10 extracts
Aliakbarlu, et al.,
2014
Antidiabetic
activity
Fruits
Methanol extract after
fractionation with ethyl
acetate and hexane
Ethyl acetate fraction of sumac fruits showed
appreciable biological activity through α-amylase
inhibition indicating significant hypoglycemic
activity.
Giancarlo, et al.,
2006
Fruits
Ethanol 96%
The Sumac extract raised markedly HDL and also
reduced LDL, increasing superoxide dismutase and
catalase activities. Also, it inhibited maltase and
sucrase activities.
Mohammadi, et al.,
2010
Fruits
Ethanolic extract
Antidiabetic activity in vivo: Alloxan-induced
diabetic wistar rats
Sharma and Arya,
2011
Seeds
Methanol extract
Antidiabetic effect of Sumac on blood glucose and
glycosylated hemoglobin levels in NIDDM rats.
Anwer et al., 2013
DNA-Protect
activity
Fruits
Sumac extract in water
solution
Sumac showed to be a potent antioxidant which may
protect humans against oxidative DNA-damage
suggesting gallic acid as main contributor for Sumac
effects
Chakraborty et al.,
2009
Lipid-lowering
and
hypocholesterolic
activity
Fruits
Methanol 80% and
100% extracts
Sumac fruit extract was of use in decrease the high
serum lipid levels, and moderate the elevated cardiac
lipid concentrations.
Shafiei, et al., 2011
Fruits
Dietary supplement
Sumac fruits, and
methanol 80% extracts
Decrease in cholesterol in the blood of rabbits
resulted after the oral administration of sumac during
90 days, showing thus a positive effect on cholesterol
and VLDL levels in adult male rabbits.
Capcarova et al.
2012
Fruits
Powder
Dietary Sumac powder
oral administration
Dietary supplementation of sumac, reduces the blood
VLDL-c, TC, and FBS concentrations in broiler
chicken
Golzadeh, et al.,
2012
Fruits
Powder
Fat diet with 2% of
Sumac powder
A protective effect of consuming sumac with food on
some risk factors of atherosclerosis and oxidative
stress (LDL-C, total cholesterol) has been
demonstrated
Madihi et al., 2013
Fruits
Dietary Sumac powder
oral administration
Sumac can be useful to decrease the negative effects
of mild heat stress on broiler chickens due to its
richness in tannins.
Alishah, et al., 2013
Antimigratory
activity
Fruits
Acetone 70% extract
Tannin extract from Sumac has an inhibitory role on
the migration of VSMC and suggesting an
atheroprotective role.
Zargham and
Zargham, 2008
Fruits
Dietary Sumac powder
oral administration
Acute consumption of Sumac might be having
protective effects on some risk factors of
atherosclerosis, and liver enzymes, due to high fat
food stress.
Setorki, 2012
Leaves
Ethanol extract
Moderate antifungal activity was found for Sumac
Ertürk, 2006
5.1. Antibacterial and Antifungal Properties
It is worth mentioning that a large number of
antibacterial activity studies have specifically focused on
sumac because of its wide-range use in the Mediterranean
area as a seasoning spice.
© 2014 Jordan Journal of Biological Sciences. All rights reserved - Volume 7, Number 4
239
Most of the antibacterial assays carried out on R.
coriaria used either ethanol or water extracts. In this
context, the water and hydro-methanol extracts from the
fruits were found to have a great activity against more
than 10 different bacteria species, among which are Gram
positive and Gram negative bacteria strains,
Staphylococcus aureus, Escherichia coli, Bacillus cereus,
Yersinia enterocolitica, Shigella dysentariae, and
Salmonella enteritidis (Nasar-Abbas and Halkman, 2004).
Among several plants tested, the aqueous extracts of
sumac had the strongest antibacterial activity against the
tested bacteria (Aliakbarlu et al., 2014). According to
Gulmez et al. (2006), the water extract of R. coriaria
fruits had an antimicrobial activity against coliform
applied on the stored poultry meat. It is worth noting that
the mature fruits of R. coriaria possess higher
antimicrobial activity in comparison to the immature
ones.
The ethanol extract of sumac was reported to be
effective in count-decreasing of the total microbial count
and salmonella in the minced meat, in which a significant
antimicrobial potential was shown for the ethanol extract
compared to controls (Radmehr and Abdolrahimzade,
2009). Furthermore, the methanol extract of sumac fruit
demonstrated an important antibacterial activity against
Bacillus pumilus, Bordetella bronchiseptica,
Staphylococcus epidermidis, and Klebsiella pneumonia,
using the agar well-diffusion method (Shabir, 2012).
The antimicrobial activity of R. coriaria extracts were
tested against six strains, including three Gram-positive
and three Gram-negative. Bacillus subtilis was found to
be the most sensitive Gram-positive with MIC of 0.5
mg/ml, while Gram-negative bacteria were affected by
higher concentrations of sumac extracts ranging 10-20
mg/ml. Among bacteria, the inhibitory effects increased
with the increase of R. coriaria fruit extracts
concentration from 0.1 to 20 mg/ml (Raodah et al., 2014).
The antibacterial activity of the plant extract against
Brucella has been also assessed, in which the mean zone
of growth inhibition for Sumac was 22.55 mm for disks
that contained 40 mg/mL, and (MIC: 3.26 mg/mL), whilst
the minimum bactericidal concentration (MBC) was 9.03
mg/mL (Motaharinia et al., 2012). The antibacterial effect
of R. coriaria on the biofilm formation of S. aureus has
been also evaluated. Significant differences between
varying concentrations of the plant extract were observed
in several strains of methicillin resistant/sensitive S.
aureus, indicating dose-related diminishes in the slime
formation noted in bacteria. Briefly, the plant extract
could reduce the formation of biofilm, a major play factor
in staphylococcal infections (Kırmusaoğlu et al., 2012).
Among the fifty Palestinian medicinal plants that were
examined to investigate their antimicrobial activities
against acne vulgaris, the ethanolic extract of R. coriaria
exhibited a strong inhibitory effect and was found to be
among the most active plant extracts against all bacterial
strains tested including, P. acnes, and Gram-negative
strains of aerobic bacteria (Ali-Shtayeh et al., 2013). It is
worth mentioning that the observed in vitro antimicrobial
potential of R. coriaria has been mainly referred to the
presence of tannins.
On the other hand, the antifungal activity results,
reported by Onkar and coworkers (2011), have indicated
that the sumac methanol extract, including other three
individual compounds (coriorianaphthyl ether, coriariaoic
acid, and coriarianthracenyl ester) thereof, were found to
be able to reduce the growth of several fungus strains.
Thus, coriariaoic acid (33) was effective against both A.
flavus and C. albicans at the lowest tested concentration
of 25 mg/ml, analogous to the standard (Fluconazole) at
higher tested concentrations against A. flavus, unlike the
case of C. albicans. Moreover, coriarianaphthyl ether has
exhibited a comparable activity at higher concentrations
of the reference drug; it was also found to be active
against all the fungal strains tested at all concentrations
used (Onkar et al., 2011). In one more study, it was
shown that the alcohol extract of R. coriaria to possess a
high antifungal activity against C. albicans and A. niger
(Ertürk, 2010).
From the results given about the antimicrobial and
antifungal activities, it can be concluded that the aqueous
and alcoholic extracts of R. coriaria possess compounds
with valuable antibacterial and antifungal activities that
can be potentially used as antimicrobial agents and in the
treatment of infectious diseases including acnes and those
caused by resistant microorganisms.
5.2. Antiviral Activity
The antiviral activity of twenty five species of various
medicinal plants in Iran was investigated, of which the
aqueous extract of R. coriaria exhibited a significant
antiviral activity against HSV-1 and adenovirus type 5 at
non-toxic concentration (Monavari et al., 2007).
Interstingly, four biflavones, viz. amentoflavone (8),
agathisflavone (9), hinokiflavone (10), and sumaflavone
(11), were isolated from the leaves and fruits of different
Rhus species. Amentoflavone (8) and agathisflavone (9)
have shown an activity against influenza A and B viruses.
Amentoflavone exhibited moderate anti-HSV-1 and anti-
HSV-2 activities with EC50 =18 and 48 μg/mL,
respectively (Lin et al., 1999). On the other hand,
hinokiflavone, amentoflavone, and agathisflavone
demonstrated significant activities against HIV-1 reverse
transcriptase, with IC50 values ranged from 65-100 μM
(Lin et al., 1997). In a previous work, hinokiflavone
isolated from Podocarpus macrophyela has shown an
antiviral activity demonstrated by its inhibitory action
noted on the Epstein-Barr virus genome expression in
Raji cells, which suggested an important antiviral potency
of this biflavone (Kozuka et al., 1989).
5.3. Antioxidant Activity
Antioxidant activity of R. coriaria fruit methanol
extract against lipid peroxidation and free radicals has
been previously reported indicating that the plant extract
may prevent the development of chronic diseases such as
atherosclerosis (Shafiei et al., 2011). On the other hand,
Aliakbarlu et al. (2013) studied the antioxidant activity of
water extract of sumac among other spices and found that
the water extracts of the plant have one of the highest
antioxidant potential among the extracts studied.
The results of antioxidant activities indicated that the
antioxidant effects are due to phenolic components,
especially, gallic acid and its derivatives (Chakraborty et
© 2014 Jordan Journal of Biological Sciences. All rights reserved - Volume 7, Number 4
240
al., 2009). Ferk and coworkers (2007) estimated the
antioxidant effect of sumac to be 50 fold more than
vitamin C and E. Besides, they reported that the daily
consumption of 0.2 mg per kg body weight gallic acid for
three days, in male rats, showed protective effects on
lymphocytes, brain, liver, colon and lung.
In a very recent study, Gabr and coworkers (2014)
extracted the active constituents of sumac like, alkaloids,
glycosides, phenol and terpenoids using GC-MS. The
antioxidant activity of R. coriaria extract and its
constituents were determined using DPPH and β-
carotene-linoleic acid scavenging activity assays.
Antioxidant activity showed a range of (72.70-87.9%)
for the plant extract compared to a lower antioxidant
activity of its active constituents. However, phenols
showed a higher range of antioxidant activity (70.1-
75.8%) compared to glycosides (65.7-67.6%), alkaloids
(53.4-58.4%) and terpenoids (50.7-51.3%), respectively
(Gabr et al., 2014).
Antiradical activities of water and ethanol extracts of
R. coriaria were studied comparatively. The study
indicated that antioxidant capacity and radical scavenging
of water extract was significantly higher than that of
ethanol extract. Also, amounts of both total phenolic and
total flavonoid contents of water extract were higher than
those of ethanol extract (Bursal and Köksal, 2011).
5.4. Antidiabetic activity
Diabetes mellitus is a metabolic disorder of the
endocrine system which is emerging as a severe problem.
It continues to increase both in numbers and in the impact
upon the quality of life, as changing lifestyles leads to
reducing physical activity and to increasing obesity. In
2010, 285 million adults worldwide were estimated to
have DM (approaching 7% of the adult population). It is
anticipated that by 2030, the number of DM patients will
exceed 438 million people, almost 8% of the adult
population (Ali-Shtayeh et al., 2012). The fruits could
improve the life of type 2 diabetic patients by exerting
mild antihyperglycemic and potent antioxidant properties.
Moreover, R. coriaria is highly recommended for the
blood lipids adjustment in diabetic patients.
The hypoglycemic efficacy of the plant extracts has
been previously investigated via hindering the α-amylase
enzyme. Ethyl acetate extract of sumac was suggested as
beneficial in the treatment and prevention of
hyperglycaemias and diabetes (IC50: 28.7 mg/mL),
suggesting a considerable blood sugar decreasing activity
of sumac extracts, whereas, the methanol extract of fruits
showed 87% inhibition activity at 50 μg/mL (Mohammadi
et al., 2010).
Another study carried out by Anwer et al. (2013)
suggested that the methanol extract of R. coriaria can
notably delay the onset of hyperinsulinemia and glucose
intolerance, and it can also improve insulin sensitivity in
rats. Above all, the gallotannin; penta-galloylglucose (7)
which was repeatedly reported in sumac plant was found
to have an antidiabetic effect, exhibited by acting as an
inhibitor of PTP1B enzyme (Baumgartner et al., 2010). In
contrast to this, it was found, by other researchers, that the
plant extracts increase the levels of blood sugar in rats
(Mirhadi et al., 2011; Pashazadeh et al., 2013). These
findings demonstrate that sumac can positively affect the
blood sugar level in diabetic patient.
5.5. Hypolipidemic Activity
Positive effects of sumac consumption on antioxidant
status and cholesterol level in rabbits have been
demonstrated in a recent study, suggesting that the plant
may have a lowering effect on blood cholesterol level in
animals and human beings (Capcarova et al., 2012;
Golzadeh et al., 2012). On the other hand, Shafiei and
coworkers (2011) showed that the sumac extract was able
to decrease high serum lipid concentrations and could
adjust the elevated cardiac lipid levels in the
hypercholesterolemic conditions.
Additionally, Valiollahi and others (2014) have shown
that the triglyceride and cholesterol level decreased
significantly in broiler chicks that consumed sumac; also,
the LDL level decreased significantly and HDL levels
increased in the same group (Valiollahi et al., 2014).
Similarly, Santiago et al., (2010) reported reduced serum
cholesterol concentrations in rats consuming d-limonene.
It was recently monitored that the acute consumption of
sumac might have a protective effect on some of the risk
factors caused by high fat food stress, such as
atherosclerosis, oxidative stress and liver enzymes
(Setorki et al., 2012). Again, a significant decrease in the
blood levels of total cholesterol, LDL-C, and fibrinogen
compared to the high-cholesterol diet group have been
described elsewhere (Madihi et al., 2013), a protective
effect demonstrated on some risk factors including
atherosclerosis and oxidative stress, followed consuming
the Sumac with food.
5.6. Scolicidal Activity
In nature, only few anthelmintics are available for
healing hydatid disease caused by the parasite
Echinococcus granulosus. Lately, Moazeni and Mohseni
(2012) have studied the scolicidal effect of the methanol
extract of sumac as anthelmintic. Thus, three
concentrations of the plant extract (10, 30 and 50 mg/mL)
were used for 10, 20 and 30 min. Whereas 16.93% rate in
the control group was for the dead protoscolices, the rate
increased to 94.13%, 97.67% and 100% after 10, 20 and
30 minutes, respectively, obtained when the protoscolices
were exposed to sumac extract at the concentration of 10
mg/mL. However, at the concentration of 50 mg/mL, one
hundred percent mortality rate was observed after 10 min
of exposure, suggesting the methanol extract to be an
effective natural scolicidal agent.
5.7. Anti-mutagenic activity
Chakraborty et al. (2009) have suggested that R.
coriaria can protect against genotoxic carcinogens, which
are degraded by specific enzymes, namely glutathione S-
transferase GST–π, and GST-α were clearly enhanced by
40%, 26%, and 52%, respectively. Actually, gallic acid, a
major constituent of the plant, is known to possess
multiple biological activities, including anticancer
function (Liu et al., 2011). However, this work indicated
an inhibitory role of invasion and migration of PC-3 cell
dose-dependently of gallic acid. Consequently, it was
postulated that the gallic acid might modulate in the
course of blocking the several signaling pathways and
© 2014 Jordan Journal of Biological Sciences. All rights reserved - Volume 7, Number 4
241
dropping the NF-κB protein level, resulting in human
prostate cancer cells inhibition.
Hinokiflavone (10) has been previously characterized
as the cytotoxic principle from R. succedanea and R.
coriaria berries; however, its significant cytotoxicity was
referred to the ether linkage between the apigenin
aglycones (Lin et al., 1989).
6. Applications of Sumac in food safety and technology
There is an increasing interest in using plant extracts
by the food industry as natural preservatives. Lipid
oxidation and microbial growth in food can be controlled
by the use of plant extracts. Water extracts of R. coriaria
possess a strong antioxidant and antibacterial activity
against food-born pathogenic bacteria, suggesting the use
of water extracts of the plant as effective and natural
preservatives in food manufacturing (Aliakbarlu et al.,
2014). Industrially, the seeds are by-products in the
production of the spice; however, they are rich in linoleic
and oleic acids that qualify the plant seeds to be
considered as a valuable raw material for the oil industry.
In this context, the mixing of R. coriaria seeds oil with
olive oil for the use in salads and cooking has already
been proposed (Ünver and Özcan, 2010).
The plant extract has shown to be more effective than
BHT (butylated hydroxytoluene) in enhancing the quality
parameters of the fermented sausage, suggesting the use
of the plant in sausage industry to enhance its total quality
(Bozkurt, 2006).
Nasar-Abbas and Halkman (2004) established that the
level of inhibitory action exerted by the R. coriaria
extract on the bacteria tested was analogous to that
commonly used in food products, the concentration at
which the plant extract exerts a desirable antibacterial
effect may be higher in foods than that studied in vitro,
but joined with other agents, it may help to control
bacterial growth in foods. The antimicrobial properties of
the plant on pathogenic bacteria in meat have also been
evaluated (Radmehr and Abdolrahimzade, 2009). From
the results, sumac exhibited significant antimicrobial
effects on the total microbial and Salmonella count in
minced meat for one week. The plant extract was found to
be effective in stabilizing peanut oil compared with BHA,
in which the antioxidant efficiency lasted for about 4
weeks. Curiously, the inhibition of autoxidation was
proportional to the concentration, suggesting that high
concentrations of sumac extract contribute mainly to the
demonstrated antioxidant activity. Also, the data can
support the application of R. coriaria as a natural
antioxidant in oily foods (Özcan, 2003).
Waste extracts of R. coriaria are considered a potential
source of natural, safe, plentiful, and also a cheap
antimicrobial resource for food, acting as a surface
decontaminant replacement by the use of the synthetic
and chemical antimicrobials in the poultry industry, since
it showed to be superior to lactic acid (antimicrobial
preservative) in terms of the quality of poultry meats
(Vatansever et al., 2008). The activity of the plant extract
might be due to the synergistic activity of slowing down
the growth rate of contaminants, originated from both
water soluble tannins and organic acids (Gulmez et al.,
2006).
However, the production of pure sumac extract
powder by using a carrier (maltodextrin) through spray
drying has been recently developed (Caliskan and Nur
Dirim, 2013). This sumac powder mix can be effectively
used in poultry and meat food production chains.
7. Conclusions
Since ancient times, R. coriaria has been used as an
important seasoning spice, in medicine, as well as in the
industry of leather. Different earlier studies suggest that
this plant possesses varied therapeutic uses, including
antioxidant, anti-inflammatory, antibacterial, antifungal,
and hypoglycemic properties. These observed biological
properties may be attributed to the presence of individual
phytochemicals, mainly phenolic compounds. R. coriaria
is thought to be very rich in these compounds.
Leaves and fruits of R. coriaria are recognized to have
defensive and beneficial effects on numerous diseases,
such as diabetes mellitus, some cancers, inflammation,
dysentery, and digestive tract system ailments. Moreover,
it possesses potential antiviral, antibacterial, antifungal,
antioxidant and hypolipidemic activities.
In this review, we have explored the recent
phytochemical and biological research available on this
well-known plant. Therefore, a comprehensive account of
its healing activity, both from a traditional and
pharmacological point of view, is presented along with
phytochemical components which are nutritionally and
medicinally significant. From the present review, it can be
concluded that the plant extracts possess compounds with
antibacterial and antifungal potential that can be used to
treat microbial infectious diseases, as well as in the food
industry. The plant extracts can be used to search for
bioactive natural products that help in the development of
new drugs and food preservatives; it is also worthy to
point out the important role of the plant in industry in
view of many recent findings and its potential for future
research.
The review also aimed at updating the current
phytochemical, biological and medicinal knowledge
available so far on R. coriaria; it also highlights the
importance of R. coriaria extracts as a promising and
potential source of functional ingredients and
nutraceuticals with desirable bioactivities, urging further
uses of sumac as a food preservative in pharmacology and
functional food industries.
Acknowledgments
The authors would like to acknowledge the fund from
the European Union under the ENPI CBC MED Program
and the collaborative international project for providing
the research grant, ref. no. I-B/1.1/288.
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