Food Control 30 (2013) 714e720

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Food Control
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Antioxidant and antibacterial activities of flavonoids and curcuminoids from

Zingiber spectabile Griff.
Yasodha Sivasothy a, Shaida Fariza Sulaiman b, Kheng Leong Ooi b, Halijah Ibrahim c, Khalijah Awang a, *
a
Department of Chemistry, Faculty of Science, University Malaya, 50603 Kuala Lumpur, Malaysia
b
School of Biological Sciences, Universiti Sains Malaysia, 11800 Minden, Penang, Malaysia
c
Institute of Biological Sciences, Faculty of Science, University Malaya, 50603 Kuala Lumpur, Malaysia

a r t i c l e i n f o a b s t r a c t

Article history: The antioxidant potential of spectaflavoside A (1) along with kaempferol and its four acetylrhamnosides
Received 20 June 2012 (2e6), demethoxycurcumin (7) and curcumin (8), isolated from the rhizomes of Zingiber spectabile was
Received in revised form evaluated using three different assays; 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical scavenging assay,
3 September 2012
ferric reducing antioxidant power assay (FRAP) and b-carotene bleaching assay, while their antibacterial
Accepted 8 September 2012
activities against eight different food-borne bacteria; Escherichia coli, Klebsiella pneumoniae, Proteus
vulgaris, Salmonella typhimurium, Vibrio parahaemolyticus, Bacillus cereus, Bacillus licheniformis and
Keywords:
Staphylococcus aureus were determined using broth microdilution assay. The highest antioxidant activity
Zingiber spectabile Griff.
Spectaflavoside A
in all assays was demonstrated by kaempferol (6), with more that 89% of activity. This was followed by
Kaempferol curcumin (8) and demethoxycurcumin (7). These two curcuminoids were found to have the potential in
Dimeric flavonol glycoside extending the shelf-life of different food products as compared with other tested compounds due to the
Flavonol glycosides higher antioxidant activities that are ranging from 56.27% in FRAP assay to 77.27% in b-carotene
Curcuminoids bleaching assay, and minimum inhibitory concentrations against six food-borne bacteria are ranged from
62.50 mg/mL to 500 mg/mL. Hence, this would suggest that the rhizomes of Z. spectabile may be
a promising source of natural preservative in the food industry.
Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction phenolic secondary metabolites, in particular the flavonoids, from

edible and medicinal plants, culinary herbs and spices have been
Microbial contamination is also an important issue leading to the effectively employed for this purpose (Ho, Noryati, Sulaiman, &
deterioration and poisoning of food products by food-borne path- Rosma, 2010; Wong & Kitts, 2006). They must be non-toxic, inex-
ogens (Ebrahimabadi et al., 2010; Ebrahimi, Hadian, Mirjalili, pensive, effective, have a carry-through effect during processing and
Sonboli, & Yousefzadi, 2008). Food additives with antioxidant and not alter the quality and sensory property of the end-product
antimicrobial properties can be applied to extend the shelf-life of (Jayaprakasha, Rao, & Sakariah, 2006).
food and maintain their safety, nutritional quality, functionality and Zingiber spectabile Griff., locally known as tepus tanah, is native in
palatability. The preference for naturally and biologically produced the moist lowland forests of Peninsular Malaysia. The leaves and
antioxidants and antimicrobials in protecting the human body from rhizomes are used to flavour food. Its young rhizomes are sliced,
diseases and reducing food spoilage has become increasingly soaked in vinegar and used as an appetizer (Jones, 1993).
popular rather than those of synthetic origin which have undesir- Z. spectabile is employed in the treatment of various ailments and in
able side effects (Bounatirou et al., 2007; Ebrahimabadi et al., 2010). the preparation of traditional medicine. The pounded leaves are
The plant kingdom with a remarkable diversity in producing applied as a poultice to inflamed eyes and on to the body to reduce
natural compounds has attained special interest and, today, swelling (Jones, 1993). The rhizomes are used as a germicide,
accessing to plant materials with dual antioxidant and antimicrobial stimulant, and tonic, and in the treatments of cancer, cough and
capabilities is an ideal goal in the field of research on food additives asthma (Sadhu, Khatun, Ohtsuki, & Ishibashi, 2007).
(Bounatirou et al., 2007; Ebrahimabadi et al., 2010). Essential oils We have recently reported the isolation and metal chelating
and nonvolatile secondary metabolites especially those rich in activities of a new dimeric flavonol glycoside; spectaflavoside A (1),
along with kaempferol-3-O-(300 ,400 -di-O-acetyl)-a-L-rhamnopyrano-
* Corresponding author. Tel.: þ60 79674064; fax: þ60 79674193. side (2), kaempferol-3-O-(200 ,300 -di-O-acetyl)-a-L-rhamnopyranoside
E-mail address: [email protected] (K. Awang). (3), kaempferol-3-O-(200 ,400 -di-O-acetyl)-a-L-rhamnopyranoside (4),

0956-7135/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.foodcont.2012.09.012
 Y. Sivasothy et al. / Food Control 30 (2013) 714e720 715

kaempferol-3-O-(400 -O-acetyl)-a-L-rhamnopyranoside (5), kaemp- then incubated at 37  C for 5 min. In a well of a 96-well plate, 50 mL
ferol (6), demethoxycurcumin (7) and curcumin (8), from the of each compound (with an initial concentration of 1 mg/mL) was
dichloromethane and ethyl extracts of its rhizomes (Fig. 1) (Sivasothy allowed to react with 150 mL of the FRAP solution. The increase in
et al., 2012). Since the rhizomes of Z. spectabile are found to be rich in absorbance at 593 nm was measured using a Multiskan EX
phenolic secondary metabolites, this prompted us to investigate their microplate reader (Thermo Scientific, Finland) after 20 min of
antioxidant and antibacterial properties as alternative sources of incubation at 37  C. The FRAP percentage was calculated as follows:
natural preservative agents to increase the shelf-life of food. Thus the % inhibition ¼ [absorbance of sample/maximum absorbance
antioxidant activities of the isolates from the rhizomes of Z. spectabile (3.0)]  100%. All experiments were performed in three replicates.
were investigated via three different assays; DPPH-radical scavenging
assay, ferric reducing antioxidant power (FRAP) assay and b-carotene 2.3.3. b-Carotene bleaching assay
bleaching assay. Their antibacterial activities against Gram-negative The b-carotene bleaching activity was determined according to
strains; Escherichia coli, Klebsiella pneumoniae, Proteus vulgaris, a minor modification of the procedure described by Miller (1971).
Salmonella typhimurium and Vibrio parahaemolyticus, and Gram- Briefly, 1 mL of b-carotene solution (2 mg/mL in chloroform) was
positive strains; Bacillus cereus, Bacillus licheniformis and Staphylo- transferred into a round bottom flask (50 mL) containing 20 mL of
coccus aureus, known to cause infections and food poisoning, were linoleic acid and 200 mL of Tween 80 solution. After evaporating to
also evaluated. dryness under vacuum at room temperature, 50 mL of oxygenated
distilled water was added to the residue with energetic agitation to
2. Materials and method form an emulsion. The emulsion (150 mL) was mixed with 50 mL of
each compound (with an initial concentration of 1 mg/mL) in each
2.1. Plant material and chemicals well of the 96-well plate and the absorbance was immediately
measured at 470 nm using a Multiskan EX microplate reader
Z. spectabile was collected from Negeri Sembilan in November (Thermo Scientific, Finland). The reaction mixture was incubated at
2009 and a voucher specimen was deposited with the University 50  C for 120 min to induce auto-oxidation and the absorbance was
Malaya herbarium (KU 0108). measured again. A negative control mixture was prepared similar to
b-carotene, 1,1-diphenyl-2-picrylhydrazyl (DPPH), dimethyl the sample mixture with DMSO instead of the tested compounds.
sulphoxide (DMSO), 4,40 -(3-(2-pyridinyl)-1,2,4-triazine-5,6-diyl) The capacity of the sample to prevent the oxidation of b-carotene
bisbenzenesulfonic acid (ferrozine), linoleic acid and 2,4,6- was determined as follows: % inhibition ¼ [(absorbance of negative
tripyridyl-s-triazine (TPTZ) were purchased from SigmaeAldrich control at 0 mine120 min)  (absorbance of sample at 0 mine
Chemical (St. Louis, MO). Ferric chloride hexahydrate, ferrous 120 min)/(absorbance of negative control at 0 mine
chloride hexahydrate, and Tween 80 were obtained from Fluka 120 min)]  100%. All measurements were performed in three
(Switzerland), while acetic acid and hydrochloric acid (HCl) were replicates.
purchased from Fisher Scientific (Springfield, NJ). Dimethyl sulph-
oxide (DMSO) and p-iodonitrotetrazolium chloride (INT) were 2.3.4. Statistical analysis
purchased from SigmaeAldrich Chemical (St. Louis, MO) while The experimental results were expressed as mean  standard
Tween 80 and the nutrient broth were purchased from Fluka deviation (SD). Analysis of variance was determined by one-way
(Switzerland) and Oxoid (England), respectively. ANOVA using GraphPadPrism (San Diego, CA). Significant differ-
ences between the means were calculated according to Duncan’s
2.2. Isolation of compounds 1e8 multiple range tests. Differences at p < 0.05 were considered
statistically significant.
Compounds 1e8 were isolated and characterized according to
the methods described previously (Sivasothy et al., 2012). 2.4. Broth microdilution assay

2.3. Antioxidant assay Minimum inhibitory concentration (MIC) values of all the
isolates were evaluated using micro-well dilution method as
2.3.1. DPPH radical scavenging assay described by Eloff (1998) with some modifications. Overnight
The free radical scavenging activity of the isolates was measured cultures of eight food-borne bacteria i.e. three Gram-positive
using DPPH assay as described by Ramos et al. (2003) with strains; B. cereus (ATCC 10876) B. licheniformis (ATCC 12759) and
some modifications. In a well of a 96-well plate, 50 mL of each S. aureus (ATCC 12600), and five Gram-negative strains; E. coli
compound (with an initial concentration of 1 mg/mL) was added to (ATCC 25922), K. pneumoniae (ATCC 13883), P. vulgaris (ATCC 6380),
150 mL of ethanolic DPPH solution (300 mM). For the negative S. typhimurium (ATCC 14028) and V. parahaemolyticus (ATCC
control, only 50 mL of DMSO was added to the DPPH solution. The 17802), were adjusted to 0.5 McFarland turbidity standard
decrease in absorbance was determined at 515 nm using a Multiskan (108 CFU/mL) and then diluted 1:100 with sterile nutrient broth.
EX microplate reader (Thermo Scientific, Finland) after 30 min The compounds were dissolved in 99.9% (v/v) DMSO to obtain an
of incubation at 37  C. The DPPH scavenging percentage was initial concentration of stock solution of 10 mg/mL. Eight serial
calculated as follows: % inhibition ¼ [(absorbance of negative twofold dilutions of the stock solution were prepared (to obtain
control  absorbance of sample)/absorbance of negative a final concentration of 500 to 3.906 mg/mL). Briefly, each well of
control]  100%. All experiments were performed in three replicates. 96-well plate was filled with 5 mL of compound solution, 90 mL of
nutrient broth and 5 mL of bacteria inoculum. The antibiotic tetra-
2.3.2. Ferric reducing antioxidant power (FRAP) assay cycline and DMSO (in similar volume with test sample) were
The FRAP assay developed by Benzie and Strain (1996) was respectively included as positive and negative controls in each
modified to be performed in a 96-well plate. The FRAP solution was assay. The plates were covered and incubated overnight at 37  C. As
prepared by adding 10 mL of acetate buffer 300 mM (which was an indicator of bacteria growth, 40 mL of 0.4 mg/mL p-indoni-
adjusted to pH 3.6 by the addition of acetic acid) to 1 mL of ferric trotetrazolium chloride (INT) dissolved in distilled water was then
chloride hexahydrate 20 mM (dissolved in distilled water) and 1 mL added to the wells and incubated at 37  C for 30 min. Bacteria
of TPTZ 10 mM (dissolved in HCl 40 mM). The FRAP solution was growth in the wells was indicated by a reddish-pink colour,
716 Y. Sivasothy et al. / Food Control 30 (2013) 714e720

OH

HO O

O O CH3

OH O

HO OCOCH3

OH

OH

HO O

O O CH3

OH O

HO OCOCH3

OH
OH OH
1

HO O HO O

O O CH3
O O CH3
OH O
OH O
OH
H3COCO
OCOCH3
HO
OCOCH3
OCOCH3 3

2
OH OH

HO O HO O

O O CH3 O O CH3

OH O OH O

OCOCH3 OCOCH3
H3COCO HO

OH OH

4 5

OH
OCH3
HO OH
HO O

OH
O OH
OH O

6 7

OCH3 OCH3
HO OH

O OH

Fig. 1. Structures of compounds 1e8.

 Y. Sivasothy et al. / Food Control 30 (2013) 714e720 717

whereas clear/colourless wells indicated inhibition by the tested significantly lower than that of kaempferol (6) (Fig. 2), this
samples. MIC value was defined as the lowest concentration of compound was found to demonstrate the greatest activity in this
samples showing clear wells or with complete inhibition of bacteria assay. This was followed by its b-carotene bleaching activity
growth. The assay was performed in triplicate. (62.08  4.75%) (Fig. 4), and ferric reducing activity (56.27  0.16%)
(Fig. 3). As indicated in Fig. 2, no significant difference was observed
3. Results and discussion between the DPPH radical scavenging activity of demethox-
ycurcumin (7) and its parent compound (curcumin) (8). This
3.1. Antioxidant activity finding was in agreement with the results reported by Jayaprakasha
et al. (2006), stipulating the equal effectiveness of these two
Despite the extensive studies on antioxidant potentials of compounds in scavenging free radicals. Mounting evidences have
curcuminoids and kaempferol derivatives, the emphasis is mostly pointed out that the radical scavenging mechanisms of the natural
to verify their medicinal values in healing various degenerative antioxidants play a vital role in terminating and delaying lipid
diseases. Thus, their roles as food preservatives still remain oxidation chain reactions in food during storage and processing
obscured. Since a combination of antioxidant and antibacterial (Sun, Zhang, Lu, Zhang, & Zhang, 2011; Zhang, Li, & Zhou, 2010).
(food-borne pathogens) effects is well recognized as an important Therefore, the antiradical properties of kaempferol and curcumi-
attribute for natural preservatives, this is apparently the first noids might be accountable for their lipid peroxidation inhibitory
comparative analysis among the major compounds isolated from capacities, which facilitates to impede the lipid radical oxidation
the rhizomes of Z. spectabile towards these bioactivities. The and thereby prevents food rancidity. Moreover, the H-atom dona-
antioxidant capacities were systematically assessed using three tion from the b-diketone moiety to a lipid alkyl or a lipid peroxyl
different assays at an initial concentration of 1 mg/mL. The inter- radical was also described as a potential antioxidant action of
relationships between different mechanisms of antioxidant reac- curcuminoids (Ak & Gülçin, 2008).
tions of these assays would be useful for comparing the capabil- Meanwhile, the glycosylation at the 3-position was found to
ities of the isolated compounds in intercepting the radical chain decrease the primary antioxidant activities of spectaflavoside A (1),
propagation, restoring the redox potential and suppressing the kaempferol-3-O-(300 ,400 -di-O-acetyl)-a-L-rhamnopyranoside (2),
lipid peroxidation process (Bursal & Gülçin, 2011). The results kaempferol-3-O-(200 ,300 -di-O-acetyl)-a-L-rhamnopyranoside (3),
obtained from these three assays have led to the similar finding of kaempferol-3-O-(200 ,400 -di-O-acetyl)-a-L-rhamnopyranoside (4)
the marked activity of kaempferol (6), followed by curcumin (8) and kaempferol-3-O-(400 -O-acetyl)-a-L-rhamnopyranoside (5) as
and demethoxycurcumin (7) with a significant difference compared to their corresponding aglycone, kaempferol (6)
(p < 0.05) in the b-carotene assay and no significant differences (Soobrattee, Neergheen, Luximon-Ramma, Aruoma, & Bahorun,
(p > 0.05) in the DPPH and FRAP assays (Figs. 2e4). This strongly 2005). This might be due to the steric hindrance after the substi-
implied the direct involvement of these compounds in enhancing tution of glycosidic residues (Gao et al., 2011). In compliance with
the primary antioxidant activity with the highest ferric reducing their observation, the higher primary antioxidant activity of the
ability of kaempferol at 100% of inhibition. The highest antioxi- tested curcuminoids (7 and 8) in comparison to the acylated
dant activity of kaempferol could be related to its flavonol kaempferol-3-O-rhamnosides (2e5) could be associated with the
structural configuration having the required antioxidant func- phenolic hydroxyl and methoxyl groups and the conjugated diene
tional groups such as the hydroxyl group at the 3-position and the moiety (Portes, Gardrat, & Castellan, 2007; Ruby, Kuttan, Dinesh
2,3-double bond in conjugation with the 4-oxo function (Rice- Babu, Rajasekharan, & Kuttan, 1995). The antioxidant activity is
Evans, Miller, & Paganga, 1997). Hence, the compound can be known to increase when the phenolic hydroxyl group is at the ortho
described as a potent reductant as it assists in reducing the redox position with respect to the methoxyl group, which is crucial for
reactions. stabilizing the phenoxy radical after hydrogen transfer (Portes et al.,
The percentage of DPPH scavenging activity of curcumin (8) 2007). Thus, the differences in the antioxidant capacities of these
(75.01  0.67%) (Fig. 2) was comparable to its b-carotene bleaching compounds may be explained by their structural conformations,
activity (77.27  1.29%) (Fig. 4). Although the DPPH scavenging particularly by the distribution of hydroxyl groups and their posi-
activity of demethoxycurcumin (7) (73.62  0.17%) was found to be tion in relation to the other substitutions.

100
% DPPH scavenging activity

80 b b

60

40

c
20 e d
g f
0
1 2 3 4 5 6 7 8
spe ctaflavoside A kae mpfe rol kae mpfe rol kae mpfe rol kae mpfe rol kae mpfe rol de me thoxycurcumin curcumin
-3-O-(3",4"-di -3-O-(2",3"-di -3-O-(2",4"-di -3-O-(4"-
-O-ace tyl)- -L -O-ace tyl)- -L -O-ace tyl)- -L -O-ace tyl)- -L
-rhamnopyranoside -rhamnopyranoside -rhamnopyranoside -rhamnopyranoside

Isolated compounds
Fig. 2. DPPH scavenging activities of compounds 1e8. Values are mean  standard deviation of triplicate analyses. Values followed by different letters mean significant differences
(p < 0.05).
718 Y. Sivasothy et al. / Food Control 30 (2013) 714e720

% Ferric reducing activity 120

a
100

80

60 b b

40

20
c d e c
f
0
1 2 3 4 5 6 7 8
spe ctaflavoside A kae mpfe rol kae mpfe rol kae mpfe rol kae mpfe rol kae mpfe rol de me thoxycurcumin curcumin
-3-O-(3",4"-di -3-O-(2",3"-di -3-O-(2",4"-di -3-O-(4"-
-O-ace tyl)- -L -O-ace tyl)- -L -O-ace tyl)- -L -O-ace tyl)- -L
-rhamnopyranoside -rhamnopyranoside -rhamnopyranoside -rhamnopyranoside

Isolated compounds
Fig. 3. Ferric reducing activities of compounds 1e8. Values are mean  standard deviation of triplicate analyses. Values followed by different letters mean significant differences
(p < 0.05).

3.2. Antibacterial activity strongly suggested to enhance its bioavailability (cellular uptake)
and facilitate its binding at endocytosis receptor through a free
As all isolated compounds possess lipid peroxidation inhibition phenolic moiety. Wang, Lu, Wu, and Lv (2009) had improved the
effect (atleast 25% of inhibition), their potential roles in the stability and solubility of curcumin (8) by microencapsulation
prevention of food deterioration were further evaluated on technique. When our results were compared with the microcapsule
different food-borne pathogenic bacteria. During the initial stages curcumin and different strains of bacteria from China General
of antibacterial screening, eight different food-borne bacteria were Microbiological Culture Collection Center, similar MIC against
selected, however only six were found to be susceptible to the B. cereus at 125 mg/mL, was obtained. However their microcapsule
compounds at a final concentration of 1 mg/mL. As indicated in curcumin exhibited greater activities on E. coli (MIC ¼ 250 mg/mL)
Table 1, all the six tested bacteria were inhibited by demethox- and S. aureus (MIC ¼ 62.5 mg/mL) than curcumin (8) used in this
ycurcumin (7) with the lowest minimum inhibition concentration study.
(MIC) against B. licheniformis (62.50 mg/mL). This compound is The curcuminoids revealed higher antibacterial activity than that
relatively more effective towards Gram-positive bacteria than of kaempferol (6), the acylated kaempferol-3-O-rhamnosides (2e5)
Gram-negative bacteria, which could be the reason of their differ- and spectaflavoside A (1). The permeability of the bacterial cells to
ences in cell membrane constituents and structures. With excep- the tested compounds is one of the determining factors of their
tion of E. coli, curcumin (8) was found to inhibit the other five antibacterial activity. The presence of a higher number of hydroxyl
bacteria and it could be ranked the second active antibacterial groups in kaempferol (6) and its acylated rhamnoside derivatives as
compound. Besides, the MIC values of this compound against well as in spectaflavoside A (1) makes them more hydrophilic
P. vulgaris and B. cereus were comparable to that of demethox- compared to the curcuminoids, thus causing the penetration into the
ycurcumin (7). Hence, the demethoxylation of curcumin (8) is cell membrane of the bacteria to be more difficult, hence, resulting in

100
a
% Beta-carotene bleaching

80 b

c
activity

60
d
e
40 f
g fg

20

0
1 2 3 4 5 6 7 8
spe ctaflavoside A kae mpfe rol kae mpfe rol kae mpfe rol kae mpfe rol kae mpfe rol de me thoxycurcumin curcumin
-3-O-(3",4"-di -3-O-(2",3"-di -3-O-(2",4"-di -3-O-(4"-
-O-ace tyl)- -L -O-ace tyl)- -L -O-ace tyl)- -L -O-ace tyl)- -L
-rhamnopyranoside -rhamnopyranoside -rhamnopyranoside -rhamnopyranoside

Isolated compounds
Fig. 4. Beta-carotene bleaching activities of compounds 1e8. Values are mean  standard deviation of triplicate analyses. Values followed by different letters mean significant
differences (p < 0.05).
 Y. Sivasothy et al. / Food Control 30 (2013) 714e720 719

Table 1
Antibacterial activity of the isolated compounds as determined by broth microdilution assay.

Compounds Minimum inhibition concentration (mg/mL)

Gram-negative bacteria Gram-positive bacteria

Proteus vulgaris Vibrio Escherichia coli Staphylococcus Bacillus Bacillus

(ATCC 6380) parahaemolyticus (ATCC 25922) aureus cereus licheniformis
(ATCC 17802) (ATCC 12600) (ATCC 10876) (ATCC 12759)
Spectaflavoside A (1) e e e e e e
Kaempferol-3-O-(3",4"-di-O-acetyl)-a-L-rhamnopyranoside (2) e e e 500 e e
Kaempferol-3-O-(2",3"-di-O-acetyl)-a-L-rhamnopyranoside (3) e 500 e 500 500 500
Kaempferol-3-O-(2",4"-di-O-acetyl)-a-L-rhamnopyranoside (4) e 250 e 500 500 e
Kaempferol-3-O-(4"-O- e 500 e e e e
acetyl)-a-L-rhamnopyranoside (5)
Kaempferol (6) 500 500 e 500 500 e
Demethoxycurcumin (7) 500 250 500 125 125 62.50
Curcumin (8) 500 500 e 500 125 500
Tetracycline 0.98 3.91 3.91 3.91 1.95 3.91

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