Plant Foods Hum Nutr (2007) 62:165–175
DOI 10.1007/s11130-007-0058-4
ORIGINAL PAPER
Biological Activities of Extracts from Sumac (Rhus spp.):
A Review
Sierra Rayne & G. Mazza
Published online: 2 October 2007
# Springer Science + Business Media, LLC 2007
Abstract Sumac is the common name for a genus (Rhus)
that contains over 250 individual species of flowering
plants in the family Anacardiaceae. These plants are found
in temperate and tropical regions worldwide, often grow in
areas of marginal agricultural capacity, and have a long
history of use by indigenous people for medicinal and other
uses. The research efforts on sumac extracts to date indicate
a promising potential for this plant family to provide
renewable bioproducts with the following reported desirable bioactivities: antifibrogenic, antifungal, antiinflammatory, antimalarial, antimicrobial, antimutagenic, antioxidant,
antithrombin, antitumorigenic, antiviral, cytotoxic, hypoglycaemic, and leukopenic. As well, the bioactive components can be extracted from the plant material using
environmentally benign solvents that allow for both food
and industrial end-uses. The favorable worldwide distribution of sumac also suggests that desirable bioproducts may
be obtained at the source, with minimal transportation
requirements from the source through processing to the end
consumer. However, previous work has focussed in just a
few members of this large plant family. In addition, not all
of the species studied to date have been fully characterized
for potential bioactive components and bioactivities. Thus,
there remains a significant research gap spanning the range
from lead chemical discovery through process development
and optimization in order to better understand the full
potential of the Rhus genus as part of global green
technology based on bioproducts and bioprocesses research
programs.
S. Rayne : G. Mazza (*)
Pacific Agri-Food Research Centre,
Agriculture and Agri-Food Canada,
4200 Highway 97,
Summerland, British Columbia V0H 1Z0, Canada
e-mail: MazzaG@agr.gc.ca
Keywords Biological activities . Extracts . Rhus spp. .
Sumac . Bioproducts . Antiinflammatory . Antioxidant .
Antimicrobial . Nutraceuticals
Introduction
A central tenet of green chemistry is the ability to obtain a
commercially viable product with desirable properties from
a widely available renewable feedstock using environmentally benign processes [1–3]. In particular, there is
significant interest in obtaining extracts with particular
biological activities from plants using green technologies
[4–7]. However, there is a tension in the use of agriculturally optimum land worldwide for producing biologically
sourced industrial- and health-based chemicals, versus the
production of food products for human consumption [8, 9].
Thus, efforts are underway to identify and investigate
potential industrially valuable crops rich in bioactive
components that can grow in marginal lands with little or
no fertilizer or irrigation inputs [9, 10].
Sumac is the common name for a genus (Rhus) that
contains over 250 individual species of flowering plants in
the family Anacardiaceae [11]. This genus is found in
temperate and tropical regions worldwide, with representative members by geographic location given in Table 1. In
general, sumac can grow in non-agriculturally viable
regions, and various species have been used by indigenous
cultures for medicinal and other purposes, suggesting
potential for commercializing the bioactivity of these plants
without competing for food production land uses [12]. For
example, R. glabra (smooth sumac) is traditionally used by
native peoples of North America in the treatment of bacterial
diseases such as syphilis, gonorrhea, dysentery, and gangrene [13]. R. coriaria (tanner’s sumac), which grows wild
in the region from the Canary Islands through the Mediterranean region to Iran and Afghanistan, is commonly used as
166
Plant Foods Hum Nutr (2007) 62:165–175
Table 1 Summary of the geographic distribution of representative
members of the sumac genus (Rhus spp.)
Location
Representative members
Asia
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
Australia
Mediterranean
Mexico and Central America
Pacific Ocean
Africa
chinensis (Chinese Sumac)
hypoleuca
javanica
punjabensis (Punjab Sumac)
verniciflua
taitensis
coriaria (Tanner's Sumac)
pentaphylla
tripartite
muelleri (Müller's Sumac)
sandwicensis
acocksii
albomarginata
angustifolia
batophylla
baurii
bolusii
burchellii
carnosula
chirindensis
ciliate
crenata
cuneifolia
dentate
discolor
dissecta
divaricata
dracomontana
dregeana
dura
engleri
erosa
fastigiata.
gerrardii
glauca
gracillima
grandidens
gueinzii
harveyi
horrida
incise
kirkii
keetii
krebsiana
laevigata
lancea
leptodictya
longispina
lucens
lucida
macowanii
magalismontana
maricoana
marlothii
microcarpa
Table 1 (continued)
Location
North America
Representative members
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
R.
montana
natalensis
nebulosa
pallens
pendulina
pentheri
pondoensis
populifolia
problematodes
pterota
pygmaea
pyroides
quartiniana
refracta
rehmanniana
rigida
rimosa
rogersii
rosmarinifolia
rudatisii
scytophylla
sekhukhuniensis
stenophylla
tenuinervis
tomentosa
transvaalensis
tridactyla
tumulicola
undulate
volkii
wilmsii
zeyheri
aromatica (Fragrant Sumac)
choriophylla (Mearns Sumac)
copallina (Winged Sumac)
glabra (Smooth Sumac)
integrifolia (Lemonade Sumac)
lanceolata (Prairie Sumac)
laurina (Laurel Sumac)
michauxii (Michaux's Sumac)
microphylla (Desert Sumac)
ovata (Sugar Sumac)
trilobata (Skunkbush Sumac)
typhina (Staghorn Sumac)
toxicodendron
vernix
virens (Evergreen Sumac)
Adapted from ref. [11]
a spice by grinding the dried fruits with salt, and is also
widely used as a medicinal herb in the Mediterranean and
Middle East, particularly for wound healing [14].
Over the past few decades, a number of publications
have reported on the biological activities of extracts from
sumac. However, no comprehensive review has been
Plant Foods Hum Nutr (2007) 62:165–175
performed to summarize the state-of-the-art, especially in
light of the recent focus on the use of bioproducts in a
sustainable world economy. Thus, in the current work, we
critically review the known biological activity of extracts
from sumac species, and suggest future research avenues
that warrant exploration. In addition, we found that the
research to date has focussed on only a few members of this
large plant family. Because of this, the review is timely in
helping to suggest increasing our breadth of research and
development efforts for obtaining bioactive extracts from
sumac using green technologies, by building on the
promising findings from the selected members of the Rhus
genus investigated to date. If there are generalizable
bioactive properties within the genus to be discovered, the
favorable worldwide distribution of sumac suggests that
desirable bioproducts may be obtained at the source, with
minimal transportation requirements from the source
through processing to the end consumer. This makes sumac
an appealing genus on which to possibly focus substantial
green chemistry research efforts, as its ability to grow on
marginal land, produce potentially useful bioactive products, be and ubiquitous in nature warrant its consideration
as a potential signature species for bioproducts and
bioprocesses research programs.
Bioactivity of Sumac Extracts
Sumac extracts have been shown to exhibit a wide range of
biological activities, which are summarized in Table 2 and
discussed in more detail below.
Antimicrobial, Antifungal, and/or Antiviral Activity
Sumac extracts are most notable for their antimicrobial
activities, although some limited information is available on
their antifungal and antiviral activities. As part of a
screening of 100 medicinal plants in British Columbia
(Canada), crude methanolic extracts of R. glabra branches
exhibited both the widest zones of inhibition in a disc assay,
and the broadest spectrum of inhibition (active against all of
the following species of bacteria tested: Bacillus subtilis,
Enterobacter aerogenes, Escherichia coli DC2, Klebsiella
pneumoniae, Mycobacter phlei, Pseudomonas aeruginosa
H187, Serratia marcescens, Staphylococcus aureus methS,
Staphylococcus aureus methR P00017, and Salmonella
typhimurium TA98) [15]. To obtain the crude extracts, the
plant material was air dried and ground in a Wiley mill with
a 2 mm mesh, followed by extraction with methanol and
filtration through cheesecloth, cotton wool, and a paper
filter. Similarly, in a follow-up study, the same methanolic
extracts from R. glabra branches inhibited the following
nine fungal strains tested: Aspergillus flavus, A. fumigatus,
167
Candida albicans, Fusarium tricuictum, Microsporum
cookerii, M. gypseum, Saccharomyces cerevisiae, Trichoderma viridae, and Trichophyton mentagrophytes [16].
While the R. glabra extract had the strongest antibiotic
activity among the 100 plants surveyed, it was only
moderately inhibitory of the fungi although it exhibited a
broad spectrum of activity.
To better understand the compounds likely responsible
for the observed antimicrobial activity of R. glabra, ground
dried branches were exhaustively extracted with methanol
and fractionated with hexane, chloroform, chloroform/
methanol (3:2 v/v) and water [17]. All fractions were tested
against Gram positive and Gram negative bacteria, with the
most active fraction being chloroform/methanol (3:2 v/v).
Subsequent column chromatography allowed the isolation
and purification of the following three compounds, which
were found to be the only active constituents against the
bacteria: methyl gallate (1; minimum inhibitory concentration (MIC) of 13 μg/ml), 4-methoxy-3,5-dihydroxybenzoic
acid (2; MIC of 25 μg/ml), and gallic acid (3; MIC of
>1,000 μg/ml) (Fig. 1).
The majority of the antimicrobial studies on sumac have
focussed on R. coriaria, and specifically, on the fruits
because of their widespread use in the Mediterranean and
Middle East as a dried spice. All of the studies have used
either ethanol or water based extracts. Fruits of R. coriaria
extracted with 95% (v/v) ethanol exhibited a broad range of
antimicrobial activity by inhibiting the growth of all of the
following Gram positive and Gram negative species tested:
Bacillus cereus, Escherichia coli strains B, 01111, 2759,
and 25922, Klebsiella pneumoniae, Proteus vulgaris,
Pseudomonas aeruginosa, Shigella dysentariae, Staphylococcus aureus, S. epidermidis, Streptococcus pyogenes,
Enterococcus faecalis, and Yersinia enterocolitica [18]. The
observed antimicrobial activity was ascribed to the tannins
in the ethanolic extracts, with MICs in the range of 10 to
26 mg/ml depending on the bacterial species.
Subsequent work also investigated the inhibitory effect of
97% (v/v) ethanol extracts from ripened and unripened
R. coriaria fruits against six Gram positive (Bacillus cereus,
B. megaterium, B. subtilus, B. thuringiensis, Listeria monocytogenes, and Staphylococcus aureus) and six Gram negative
(Citrobacter freundii, Escherichia coli strains Type I and
O157:H7, Hafnia alvei, Proteus vulgaris, and Salmonella
enteritidis) bacteria [19]. The extract was found to be
effective against all tested bacteria, with the Gram positives
more sensitive. Bacillus spp. was the most sensitive, with MICs
at about 500 μg/ml, followed by S. aureus (1,000 μg/ml),
and L. monocytogenes (1,500 μg/ml). Among the Gram
negative bacteria, S. enteritidis and E. coli type I were the
most resistant (MICs up to 3,000 μg/ml), followed by E. coli
O157:H7 (2,500 μg/ml), H. alvei (2,000 μg/mL), P. vulgaris
(1,500 μg/ml), and C. freundii (1,000 μg/ml). Ripened fruits
168
Plant Foods Hum Nutr (2007) 62:165–175
Table 2 Summary of reported biological activities of compounds and fractions extracted from sumac
Biological
activity
Species
Plant part
Antifibrogenic
Antifungal
Antiinflammatory
Antimalarial
R.
R.
R.
R.
Bark
Branches
Roots
Leaves
Antimicrobial
R. retinorrhoea
R. glabra
verniciflua
glabra
undulate
retinorrhoea
R. coriaria
Antimutagenic
R. verniciflua
Antioxidant
R. verniciflua
R. succedanea
R. coriaria
Antithrombin
Antitumorigenic
R. hirta
R. verniciflua
R. verniciflua
Antiviral
R. succedanea
Cytotoxic
R. verniciflua
Hypoglycaemic
Leukopenic
R. coriaria
R. vernificera
Compound(s) and/or extract type
Butein
Methanol extract
Apigenin dimethyl ether
7-O-methylnaringenin, eriodictyol, 7,3’-O-dimethylquercetin, 7-Omethylapigenin,
7-O-methylluteolin, and (2S,2”S)-7,7”-di-O-methyltetrahydroamentoflavone
Leaves
7-O-methylnaringenin
Branches
(a) Methyl gallate, 4-methoxy-3,5-dihydroxybenzoic acid, and gallic acid
(b) Methanol extract
Seed
Ethanol and methanol extracts
Fruits
(a) Water extract
(b) Ethanol/water (19:1 v/v)
(c) Hydrodistillation extract
(d) Water-soluble fraction of methanol extract partitioned against chloroform
(e) Ethanol/water (4:1 v/v)
Heartwood Garbanzol, sulfuretin, fisetin, fustin, and mollisacasidin
Branches
Protocatechuic acid, fustin, fisetin, sulfuretin, and butein
Branches
(a) Ethanol extract fractionated on Sephadex G-150 (activity ascribed to
laccase, benzenediol/oxygen oxidoreductase)
(b) Fustin, quercitin, butein, and sulfuretin
(c) Crude Ethanol extract further fractionated using prep-LC with acetonitrile/
water gradient
Bark
Ethanol/water (3:1 v/v) extract
Sap
10’(Z),13’(E),15’(E)-heptadecatrienylhydroquinone, 10’(Z),13’(E)heptadecadienylhydroquinone, and 10’(Z)-heptadecenylhydroquinone
Fruits
(a) Methanol extract
(b) Water extract
(c) Water-soluble fraction of methanol extract partitioned against chloroform
Leaves
Methanol extract
Whole
Ethyl acetate and methanol fractions after initial defatting (petroleum ether),
plant
extraction with aqueous/methanol (1:4 v/v), and partitioning (n-hexane/ethyl
acetate)
Fruits
Methanol extract
Stems
6-Pentadecylsalicylic acid
Branches
(a) Ethanol extract fractionated on Sephadex G-150 (activity ascribed to
laccase, benzenediol/oxygen oxidoreductase)
(b) Protocatechuic acid, fustin, fisetin, sulfuretin, and butein
Fruits
Robustaflavone, amentoflavone, agathisflavone, volkensiflavone,
succedaneaflavone, and rhusflavanone
Branches
Ethanol extract fractionated on Sephadex G-150 (activity ascribed to laccase,
benzenediol/oxygen oxidoreductase)
Fruits
Methanol extract further fractionated with ethyl acetate and hexane
Sap
Polysaccharide extracts
were also found to have a significant higher antimicrobial
activity compared to unripened fruits.
Most recently, additional work using dried R. coriaria
seed, found an antibacterial effect of a combined ethanol/
methanol extract against Pseudomonas aeruginosa [20]. As
well, hydroalcoholic extracts of R. coriaria fruits prepared
by a cool percolation method using 80% (v/v) ethanol were
tested against representative Gram positive and negative
Reference(s)
[49]
[16]
[50]
[26]
[26]
(a) [17]
(b) [15]
[19]
(a) [22, 23]
(b) [18, 19]
(c) [24]
(d) [44]
(e) [21]
[52]
[53]
(a) [37]
(b) [30]
(c) [29]
[38]
[47]
(a) [40]
(b) [45]
(c) [43]
[41]
[42]
[46]
[48]
(a) [37]
(b) [58]
[25]
[37]
[51]
[55, 56]
bacteria such as Staphylococcus aureus, Bacillus cereus,
Escherichia coli, Salmonella typhi, Proteus vulgaris, and
Shigella flexneri [21]. The sumac extract exhibited antibacterial activity against all the species tested, with MICs
ranging from 0.05 mg/ml (B. cereus) to 0.20 mg/ml (E. coli
and S. flexneri) on a weight/volume percentage.
Water extracts of R. coriaria fruits, like the ethanolic
extracts, also display antimicrobial activity. Water extracts
Plant Foods Hum Nutr (2007) 62:165–175
O
O
OCH3
HO
OH
HO
OH
169
O
OH
HO
OCH3
OH
OH
Abbas et al. [22] found that water extracts from R. coriaria
fruits had the greatest effectiveness against Gram positive
bacteria, with Gram negative strains being more resistant,
and a four to five log cycle reduction in Bacillus spp. after
1 h exposure to a 1.0% (w/v) sumac extract. Other microbial
species tested had a two to three log cycle reduction after the
1 h exposure period.
Similarly, Gulmez et al. [23] reported that a water extract
(45 °C for 12 h) from R. coriaria fruits exhibited antimicrobial activity at a concentration of 8% (w/v)—particularly
towards coliforms (total and fecal)—on poultry meat during
storage. In contrast to the conventional alcoholic and
aqueous extracts from sumac, which appear to have
substantial antimicrobial activity, a hydrodistillation extract
of dried R. coriaria fruits was found to be ineffective as an
antimicrobial agent [24].
To the best of our knowledge, only one study has
examined the broad spectrum antiviral properties of sumac
extracts, and the work focussed on biflavonoids isolated
from the seed kernels of R. succedanea [25]. Six biflavonoids [robustaflavone (4), amentoflavone (5), agathisflavone (6), volkensiflavone (7), succedaneaflavanone (8), and
rhusflavanone (9)] were isolated from R. succedanea seeds
and tested for inhibitory activities against a number of
viruses including respiratory viruses (influenza A, influenza
B, respiratory syncytial, parainfluenza type 3, adenovirus
type 5, and measles) and herpes viruses (HSV-1, HSV-2,
HCM, and VZV) (Fig. 2). The results indicated that 4
exhibited strong inhibitory effects against influenza A and
OH
OH
1
2
3
Fig. 1 Compounds exhibiting antimicrobial activity in sumac extracts
(1 h at 25 °C following by 2 min of boiling) of dried R.
coriaria fruits at 0.1 to 5% (w/v) exhibited antimicrobial
activity against the following bacteria: Bacillus cereus, B.
megaterium, B. subtilis, B. thuringiensis, Listeria monocytogenes, S. aureus, C. freundii, E. coli (Type I and O157:
H7), H. alvei, P. vulgaris, and S. enteritidis [22]. Both
ripened and unripened fruits displayed similar antibacterial
effectiveness (in contrast to ethanolic extracts obtained by
the same research group, where ripened fruits had a
significant higher antimicrobial activity compared to unripened fruits [19]), but differences in antimicrobial activity
were found between the various bacteria. The Bacillus
group was, in general, found to be more sensitive among
Gram positive bacteria with B. subtilis being the most
sensitive [MICs from 0.25–0.32% (w/v)]. L. monocytogenes
was the most resistant among Gram positive strains with a
MIC of 0.67% (w/v). P. vulgaris was the most sensitive
Gram negative strain [MIC of 0.63% (w/v)], with S. enteritidis
and E. coli having the highest resistance. Overall, Nasar-
OH
OH
OH
HO
HO
O
OH
O
O
OH
HO
O
HO
O
HO
O
OH
OH
OH
O
OH
OH
5
OH
OH
O
O
OH
HO
OH
O
O
O
O
OH
H
HO
6
OH
4
OH
O
O
O
HO
OH
O
HO
OH
O
O
O
HO
7
OH
OH
8
O
O
OH
HO
O
OH
OH
OH
O
9
Fig. 2 Compounds exhibiting antiviral activity in sumac extracts
170
influenza B viruses with EC50 values of 2.0 and 0.1 μg/ml,
respectively. 5 and 6 also demonstrated significant activity
against influenza A and B viruses. 4 and 5 showed
moderate anti-HSV-1 and anti-HSV-2 activities with EC50
values of 18 μg/ml (HSV-1) and 48 μg/ml (HSV-2), and
8.5 μg/ml (HSV-1) and 8.6 μg/ml (HSV-2), respectively. 9
demonstrated inhibitory activities against influenza B,
measles, and HSV-2 viruses, while 8 exhibited inhibitory
activities against influenza B virus and VZV. It is also of
note that 5 has been reported in R. retinorrhoea leaves [26]
and 6 in R. semialata leaves [27], suggesting that other
Rhus species may contain antiviral constituents.
The literature strongly suggests the potential for useful
antimicrobial, antifungal, and antiviral agents to be
obtained from sumac extracts, but the work to date has
been too focussed on one primary species and plant part
(fruits of R. coriaria) given its regional use as a spice. This
focus is understandable, but (as with the other bioactive
properties discussed below) future efforts should survey the
worldwide sumac species to determine if these properties
are generalizable across the Rhus genus. In addition, since
the bioactivities appear to be ascribed to polar compounds
extractable with protic solvents, additional studies are
required on whether these properties occur in extracts from
other plant parts (e.g., stems/branches, roots, and leaves),
and that the optimum extraction and storage conditions are
to obtain the highest quality yields of desired functionality.
The use of other green solvent systems, particularly suband super-critical fluids (e.g., CO2, water), also warrants
investigation.
Plant Foods Hum Nutr (2007) 62:165–175
cytes. Results from deoxyribose, DNA nicking, and
glucose/glucose oxidase enzyme assays indicated that the
extract contained a strong scavenging activity of oxygen
free radicals, particularly hydroxyl radicals, but also
exhibited cytotoxicity at higher concentrations towards the
thymocytes.
In further studies on the same extract, the crude ethanol
extract was separated using column chromatography into
three water-eluted fractions and three organic solvent
fractions [30% ethanol in water (v/v), absolute ethanol,
and 5% acetic acid in water (v/v)] to better understand the
source of the observed bioactivity in the R. verniciflua
wood [30]. The water eluted fractions were the most
protective against reactive oxygen species generated by
iron and enzymes. As well, one of the water eluted fractions
[shown to contain the flavonoids fustin (10), quercitin (11),
butein (12), and sulfuretin (13)] protected against thymocyte
apoptosis mediated by hydroxyl radicals, and these compounds were attributed to the antioxidant activity (Fig. 3). 10
and 13 have also been reported in the wood of R. copallina
[31], R. glabra [31–33], and R. typhina [31], suggesting that
these species may also yield extracts with antioxidant
behaviour. 11 has also been found in the leaves of R. coriaria
[34] and R. typhina [35, 36].
Kitts and Lim investigated the antioxidant, cytotoxic,
and antitumorigenic activities of a fractionated ethanol
extract derived from branches of R. verniciflua, and gel
electrophoresis results suggested that the active component
of a Sephadex G-150 fractionated extract was a copper
containing protein, possibly a plant laccase (benzenediol/
oxygen oxidoreductase EC 1.10.3.2) [37]. Antioxidant
Antioxidant Activity
Developing new, safe, and naturally derived antioxidants
for food and health applications is a major goal in
sustainable bioproducts. Synthetic antioxidants such as
butylated hydroxyanisole (BHA) and butylated hydroxytoluene (BHT) are widely used in spite of concerns regarding
their toxicology and a sustainable supply [28]. Most of the
research performed on sumac extracts has examined
antioxidant activity, and there appears to be potential for
commercial development of the products from a number of
species. However, as with other areas of bioactivity, the
work to date has been focussed on a limited number of
species (R. verniciflua and R. succedanea in Asia, R. coriaria
in the Mediterranean/Middle East, and R. hirta in northeastern North America). More breadth in worldwide species
is required to better understand the potential of sumac as a
commercial source of natural antioxidants.
Crude ethanol extracts from R. verniciflua wood have
exhibited strong antioxidant activity using cultured neuronal cells [29]. The unfractionated ethanol extract showed
both antioxidant and cytotoxic effects on mouse thymo-
OH
OH
OH
HO
O
OH
HO
O
OH
O
10
HO
OH
OH
OH
OH
HO
OH
O
11
HO
OH
O
O
O
12
13
OH
R R=10'(Z),13'(E),15'(E)-heptadecatrienyl (14)
R=10'(Z),13'(E)-heptadecatrienyl (15)
R=10'(Z)-heptadecenyl (16)
OH
Fig. 3 Compounds exhibiting antioxidant activity in sumac extracts
Plant Foods Hum Nutr (2007) 62:165–175
activity of the extract was observed in both aqueous and
lipid in vitro oxidation reactions using DPPH, Fenton
reaction deoxyribose, and lipid emulsion test systems, and
cultured mouse brain neurons were protected against
glucose oxidase induced hydroxyl radical in the presence
of 4.9 μM (58% protection) and 22.7 μM (95% protection)
fractionated R. verniciflua extract. In addition, 2.5 μM
fractionated extract led to 70% tumor cell death after 24 h
incubation in the HeLa and CT-26 cell lines.
In terms of direct practical industrial antioxidative application, the only study using R. verniciflua wood involved a
75% ethanol (v/v) extract obtained at 80 °C for 3 h and
evaluated in frying oil of Yukwa base (rice snack) [38].
Additions of 400 and 1,000 mg/l of sumac extract to the
frying oil indicated a superior antioxidative action compared
to BHA and α-tocopherol. Other work at stabilizing food
products with sumac extracts includes the use of a methanol
extract from R. coriaria fruits tested in sunflower oil stored
at 70 °C by measuring peroxide values after regular intervals
[39]. Along with rosemary and Turkish sage, sumac extracts
were found to be most effective in stabilizing sunflower oil,
followed by wild thyme and black thyme.
Antioxidant properties for stabilizing peanut oil were
also reported on the methanol extracts of R. coriaria fruits
and leaves [40, 41]. Fruit extract addition to peanut oil from
1 to 5% (w/v) generally inhibited the formation of
hydroperoxide during the initial 7 days after addition [40],
but at 28 days of storage, the sumac extract had
substantially lower antioxidant potential compared to
BHA controls. Similar results were observed with leaf
extracts [41], whereby the addition to peanut oil at 4% (w/v)
had a limited effect relative to the BHT controls.
Other work has examined the antioxidant and free radical
scavenging activities of R. coriaria fruit extracts obtained by
extraction with 80% methanol (v/v), and further fractionated
using n-hexane, ethyl acetate, and water [42]. The ethyl
acetate fraction exhibited greater antioxidant activity than the
corresponding BHA and BHT controls as measured using the
DPPH assay, but tests using the linoleic acid peroxidation
assay indicated lower activity than the synthetic controls.
Candan’s group has also examined the antioxidative ability
of chloroform partitioned methanol extracts from R. coriaria
fruits for lipid peroxidation, free radical scavenging, superoxide radical scavenging, and xanthine oxidase activity [43,
44]. The IC50 value for lipid peroxidation was estimated at
1,200 μg/ml in the Fe2-ascorbate system, while those for
superoxide scavenging ability in the xanthine–xanthine
oxidase method and hydroxyl radical scavenging activity in
the deoxyribose decomposition method with 283 and
3,850 μg/ml, respectively [43]. As well, the fractionated
extract was an uncompetitive inhibitor of xanthine oxidase
and scavenger of superoxide radical in vitro with IC50 values
of 173 and 232 μg/ml, respectively [44].
171
In the only aqueous extraction study regarding the antioxidative behaviour of R. coriaria fruits, a water extract (25 °C
for 24 h) was more effective than BHT in preserving sausage,
decreasing formation of putrescine, histamine, tyramine, and
thiobarbituric acid reactive substances during storage [45].
Other than R. verniciflua and R. coriaria, only two other
sumac species (R. hirta and R. succedanea) have been
investigated for their extracts’ antioxidant activities. A
methanolic extract from the fruits of R. hirta performed
similarly to green teas for scavenging superoxides produced
by a NBT/xanthine oxidase (XO) assay, and greater than
green tea and ascorbic acid for peroxyl radical scavenging
using a DCF/AAPH assay [46]. Of the 35 native plant
species from the boreal forest region of northeastern North
America that were tested based on their historical use by
indigenous peoples for treating diabetes and its complications, R. hirta exhibited the lowest IC50 (3.7 μg/ml) in the
DPPH assay, and the highest percent inhibition in the NBT/
XO (44.5%) and DCF/AAPH (31.5%) assays.
An antioxidant directed HPLC fractionation of the 80%
ethanol (v/v) extract from the sap of R. succedanea was
used to isolate three heptadecenyl compounds (14, 15, and
16; see Fig. 3 for structures) with antioxidative and
cytotoxic activities against five cancer lines [cervix epitheliod carcinoma (HeLa), hepatoma cell line (Huh7),
colorectal cancer cell line (HCT116), colon adenocarcinoma (LoVo), and rat C6 glioma cells] with IC50 concentrations ranging from 0.9 to 6.4 μg/ml [47].
With a number of studies indicating that sumac extracts
display considerable antioxidant behaviour, and with a few
applied examples, we argue that this genus may offer
promise for a natural source of commercial antioxidants.
However, more species breadth is required in delineating
the possible generality of obtaining viable natural antioxidants from sumac, as well as studies that consider the
agronomic growth potential, optimized extraction and
processing methods, and corresponding economic aspects
at the feasibility level.
Anticlotting Activity
Limited work has been done on the antithrombin activity of sumac extracts, with only a single report of 6pentadecylsalicylic acid (17) being isolated from air-dried
stems of R. semialata after methanol extraction and
subsequent column chromatographic purification [48].
The compound showed antithrombin activity at 50 μg/ml
using the amidolytic method, and prolonged clotting time in
a dose-dependent manner in the clotting assay of thrombin–
fibrinogen interaction. As with other areas of potentially
bioactive agents from sumac, significantly most breadth in
research efforts worldwide is required to determine not only
the feasibility of obtaining commercially viable products
172
Plant Foods Hum Nutr (2007) 62:165–175
from the plants, but also in whether all members of the
genus display similar bioactive possibilities.
O
OH
HO
C15H31
17
Antifibrogenic, Antiinflammatory, Hypoglycemic,
and/or Leukopenic Activities
Antifibrogenic activity of R. verniciflua was assigned to 12
[49], which was isolated from the bark by drying and
pulverizing, extracting with hot methanol for 3 hours,
subsequently dissolving the methanol extract in water/
methanol (3:2 v/v), and partitioning with n-hexane followed
by dichloromethane. The dichloromethane extract was
separated by Sephadex LH-20 column chromatography
(dichloromethane:methanol, 20:1 v/v) to yield five fractions, the fourth was further chromatographed to give pure
12 in 0.035 w/w% yield. Testing of the isolated 12 on liver
fibrosis in rats indicated that the compound had antifibrotic
effects, and dose levels of 10 to 25 mg kg−1 day−1 showed a
significant reduction of hydroxyproline and malondialdehyde levels in rats. The expression of α1(I)collagen and
tissue inhibitor of metalloproteinase-1 (TIMP-1) mRNAs in
liver was reduced in a dose-dependent manner in rats given
12 compared with corresponding carbon tetrachloride
controls. Thus, 12 appears to act as an antifibrogenic agent
by inhibition of collagen accumulation and lipid peroxidation, and by down regulation of the expression of both α1
(I)collagen and TIMP-1 mRNA.
From the roots of R. undulata, apigenin dimethyl ether
(18) was isolated and found that, at a dose of 75 mg/kg, this
compound exhibited 81% inhibition of the phlogistic
response (carrageenan induced edema) in a rat [50].
biological activity in the ethyl acetate extract was attributed
to the presence of flavonoids as tentatively identified by
thin-layer chromatography, while dominantly terpenoids
were found in the n-hexane fraction.
The exudate that can be obtained from the stem bark of lac
tree (R. vernicifera) has been used mainly as a material for
traditional paint and lacquer in East Asian countries [52].
The lacquer polysaccharide is an acidic heteropolysaccharide
with a 1,3-β-linked D-galactopyranosidic main chain having
complex branches with 4-O-methyl-β-glucoronic acid in the
terminal [53, 54]. Studies on isolated Chinese laquer
polysaccharide from R. vernicifera have found significant
bioactivity against leukopenia [55, 56]. In addition to the
material properties of this product, further work is required to
better understand its range of potential bioactivities.
Antimalarial Activity
Work with dried and ground leaves of R. retinorrhoea from
Saudi Arabia, which were extracted using dichloromethane,
suggests that a modest antimalarial activity can be obtained
[26]. Partitioning of the dichloromethane extract between
hexane and acetonitrile, followed by silica gel column
chromatography (benzene/ethyl acetate) yielded the following five flavonoids, 7-O-methylnaringenin (19), eriodictyol
(20), 7,3′-O-dimethylquercetin (21), 7-O-methylapigenin
(22), 7-O-methylluteolin (23), and the biflavone (2S,2″S)7,7″-di-O-methyltetrahydroamentoflavone (24) (Fig. 4).
OH
H3CO
OH
OH
O
HO
OH
O
O
19
OCH3
OH
O
OH
20
H3CO
O
H3CO
OCH3
H3CO
O
OH
O
OH
O
OH
OH
21
OH
O
OH
22
OH
O
H3CO
O
18
Methanol extracts of R. coriaria fruits were recently
studied for potential hypoglycemic activity [51]. The crude
extracts were further fractionated by ethyl acetate and nhexane, and the ethyl acetate extracts exhibited significant
hypoglycemic activity through α-amylase inhibition (87%
inhibition at 50 μg/ml), with lower activity from the nhexane fraction (77% inhibition at 250 μg/ml). The higher
OH
OH
OH
O
O
23
H3CO
O
O
H3CO
OH
OH
OH
O
24
Fig. 4 Compounds exhibiting antimalarial activity in sumac extracts
Plant Foods Hum Nutr (2007) 62:165–175
173
The biflavone 24 exhibited moderate antimalarial activity
with an IC50 of 0.98 μg/ml against Plasmodium falciparum
(W2 clone) and weak activity against P. falciparum (D6)
with an IC50 of 2.8 μg/ml, but was not cytotoxic. 19
showed weak antimicrobial activity against Candida albicans, C. krusei, Staphylococcus aureus, Mycobacterium
smegmatis, M. intracellulare, and M. xenopi. Given the
global interest in environmentally and economically sustainable antimalarial treatments, further work is needed on
ascertaining whether this desirable bioactivity can be
obtained from the numerous sumac species indigenous to
malarial regions of sub-Saharan Africa (see Table 1).
and apoptosis-inducing effects in mouse tumorigenic
hepatic cells. Additional work on a chloroform-methanol
fraction from a crude acetone extract of R. verniciflua
wood suggested that these flavonoids may also be
responsible for inhibiting the growth of human lymphoma
cells [58].
O
OH
OH
27
Antimutagenic, Cytotoxic, and/or Antitumorigenic
Activities
Park et al. examined the heartwood of R. verniciflua, and
following an initial methanol extraction, the following four
flavonoids were separated by ethyl acetate fractionation and
column chromatography: 10, 13, fisetin (25), and garbanzol
(26) [52]. The crude methanolic extract was applied to rats,
and prevented the activation of hepatic microsomal cytochrome P450 enzymes and inhibition of hepatic glutathione
S-transferase, leading to further isolation efforts to identify
the specific compounds responsible for the observed
bioactivity. When the individual flavonoids were subjected
to the Ames test, it was observed that 13 might effectively
prevent the metabolic activation, or scavenge the electrophilic intermediates, capable of causing mutation. In
contrast, 10 showed a dose-independent antimutagenic
activity with mutagenic and antimutagenic behaviour.
However, a 1:1 (w/w) mixture of 10 and 13 exhibited
dose-dependent antimutagenicity, indicating that 13
inhibited the mutagenicity of 10.
OH
OH
OH
HO
HO
O
O
OH
OH
O
O
25
26
OH
Compounds 10, 13, and 25 have also been reported in the
wood of R. copallina [31], R. glabra [31–33], and R.
typhina [31], suggesting that these species may also yield
extracts with antitumorigenic behaviour.
Similarly, Son et al. prepared a flavonoid containing
chloroform-methanol fraction from a crude acetone extract
of R. verniciflua wood that contained the following
compounds: 10, 12, 13, 25, and protocatechuic acid (27)
[57]. The fraction exhibited selective growth inhibition
Conclusions
The research efforts on sumac extracts indicate a promising
potential for the plant family to provide renewable bioproducts with the following desirable bioactivities: antifibrogenic, antifungal, antiinflammatory, antimalarial,
antimicrobial, antimutagenic, antioxidant, antithrombin,
antitumorigenic, antiviral, cytotoxic, hypoglycaemic, and
leukopenic. As well, the bioactive components can be
extracted from the plant material using environmentally
benign solvents (e.g., ethanol, water) that allow for both
food and industrial end-uses. Furthermore, a substantial
opportunity exists to investigative the use of other green
solvents (e.g., sub- and super-critical liquids, ionic liquids)
for obtaining bioactive compounds and other phytochemicals from sumac, and in processing the residue for
complete biomass conversion.
However, as this overview demonstrates, the previous
work has focussed on only a few members (eight) of this
large plant family (ca. 250 species). In addition, not all of
the species studied to date have been fully characterized for
potential bioactivities. Thus, there remains a significant
research gap spanning the range from chemical discovery
through process development and optimization in order to
better understand the full bioactive potential of the Rhus
genus as part of global green technology based on
bioproduct and bioprocess research programs.
Acknowledgements We thank the Natural Sciences and Engineering
Research Council (NSERC) of Canada for financial support.
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