Antioxidant and Antimicrobial Activity of Zingiberaceae Plants in Taiwan

Plant Foods Hum Nutr (2008) 63:15–20
DOI 10.1007/s11130-007-0063-7
ORIGINAL PAPER
Antioxidant and Antimicrobial Activity of Zingiberaceae
Plants in Taiwan
I-Nan Chen & Chen-Chin Chang & Chang-Chai Ng &
Chung-Yi Wang & Yuan-Tay Shyu & Tsu-Liang Chang
Published online: 20 December 2007
# Springer Science + Business Media, LLC 2007
Abstract The rhizomes of the Zingiberaceae family are a
Keywords Antimicrobial . Antioxidant . Ginger .
vegetable widely used in many Asian countries, and their
Reducing power . Zingiberaceae
medicinal functions have been broadly discussed and
accepted in many traditional recipes. In this study, 18 species
of five genus of Zingiberaceae plants from Taiwan area were
Introduction
collected and analyzed for their functional properties.
Methanolic extracts of the plants were analyzed for their
The Zingiberaceous plants are characterized by their
total phenol compounds, ?,?-diphenyl-?-picrylhydrazyl
tuberous or non-tuberous rhizomes, which have strong
(DPPH) scavenging activity, and reducing power. Antimi-
aromatic and medicinal properties. It is commonly known
crobial activity of these samples was also determined. The
as ginger, and exists in about 50 genera and 1,300 species
results showed that the total phenol compounds of the Alpinia
worldwide, distributed mainly in South and Southeast Asia
genus averaged 17, 30 mg/g for Curcumas, and the highest,
[1]. Turmeric of Zingiberaceous plants in powder form is
36.5 mg/g for Vanoverberghia sasakiana. Antioxidant
widely applied as a food additive in many Asian countries.
performances were best observed in Vanoverberghia and
Medicinal functions for treatment of diseases such as
Hedychium, both 89%, and DPPH scavenging activity
diarrhea, coryza, dermatosis disorders and rheumatism are
followed similar trends. Particularly, Zingiber oligophyllum,
also widely mentioned in traditional remedies [2–5].
considered as a traditional medicinal plant used in Taiwan
Zingiberaceae plants contain many essential oils, including
exhibited low DPPH scavenging activity and reducing
terpenes, alcohols, ketones, flavonoids, carotenoids and phy-
power. Most Zingiberaceae plant extracts exhibited antimi-
toestrogens [6–8]. For instance, the water extract of Zingiber
crobial activity against all tested food microorganisms.
officinale exhibits 6-Gingerol, and is mostly found in the
Hedychium and Vanoverberghia, did not show antimicrobial
rhizome in concentrations of 130–7,138 ppm. The major
activities on Escherichia coli and Vibrio parahaemolyticus.
functional compound in Curcuma turmeric is curcumin,
This study is a positive demonstration of the utility of
which has concentrations as high as 38,000 ppm in certain
screening Taiwan’s endemic Zingiberaceous plants for their
species [8]. Less-polar constituents including curcuminoids,
food and medicinal uses.
kava pyrones and gingerols isolated from Zingiberaceous
plants, which have been reported for their biological activities
I.-N. Chen : C.-C. Ng : C.-Y. Wang : Y.-T. Shyu :
in antifungal, antioxidant, insecticidal, and anti-inflammatory
T.-L. Chang (*)
activities [9–11] are particularly important and relevant for
Department of Horticulture, National Taiwan University,
these applications.
140 Keelung Rd. Section 4,
This study reveals the bioactive and medicinal potentials
Taipei 10600 Taiwan, Republic of China
e-mail: ghouse@ntu.edu.tw
of ginger species in Taiwan. Six genera and 25 species of
Zingiberaceae plants are native to Taiwan. Among these,
C.-C. Chang
Alpinia is the largest genus, with 14 species recorded so far
Department of Living Sciences, Tainan University of Technology,
[12]. The antioxidant and antimicrobial properties of
529 Jhongjheng Rd., Yongkang,
Tainan 71002 Taiwan, Republic of China
Taiwan’s endemic and imported Zingiberaceae plants have

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Plant Foods Hum Nutr (2008) 63:15–20
not yet been thoroughly explored [7]. This work evaluated
Antioxidant Activity Determination
the antioxidant and antimicrobial properties of 18 Taiwan
endemic species collected from all over the island. The
The antioxidant capacity of samples was measured by the
concentrations of phenolic compounds, antioxidant capac-
method described by Miller and Rice-Evans, and Arnao et al.
ity, ?,?-diphenyl-?-picrylhydrazyl (DPPH) scavenging
[14, 15] with little modifications. Peroxidase (4.4 units/ml,
activity and reducing power of the samples were deter-
Sigma, MO, USA), H2O2 (50 ?M, Merck, Germany), 2,
mined. The activities of ginger rhizomes against different
2-azino-bis (3-ethylbenz-thiazoline-6-sulphonic acid)
food-related microorganism were also measured. This
[100 ?M, Sigma, MO, USA] and distilled water (1 ml)
investigation evaluates the potential medicinal applications
were mixed and kept in dark for 1 h for reaction. One ml of
of Taiwan’s endemic Zingiberaceae plants.
plant extract was subsequently added and determined by
absorbance at 734 nm. The antioxidant capacity was
calculated by the following formula:
Materials and Methods
Antioxidant activity (%) = [1?(A734 nm, sample/
A734 nm, control)] × 100
Rhizome Collection
DPPH Free Radical Scavenging Activity Test
Plant materials were collected and purchased from the
Taiwan Endemic Species Research Institute, the Council of
The capacity of Zingiberaceae to remove 1,1-diphenyl-2-
Agriculture, traditional markets, and local growers from
picryl-hydrazyl radical (Sigma, MO, USA) was determined
whole Taiwan Island. The rhizomes were removed from the
by the method described by Shimada et al. [16]. Briefly,
plant and cleaned for use.
1 ml of methanolic extract and 5 ml of freshly prepared
0.1 mM DPPH methanolic solution were thoroughly mixed
Sample Treatment and Extraction
and kept in the dark for 60 min. The absorbance of the
reaction mixture at 517 nm was measured with a spectro-
Peeled and washed samples were further chopped into 2×
photometer. The blank was prepared by replacing the
2 cm dice and dried with freeze-dryer (Freeze dryer Alpha
extract with methanol (1 ml). The percentage of free radical
1-2/LD-2, Vacuum pump RZ-5, Christ, Germany) for 48 h.
scavenging activity was calculated as follows:
Dried samples were subsequently milled using commercial
Scavenging activity (%) = [1?(A517 nm, sample/
hand-carry milling machine. For methanol extraction,
A517 nm, blank)] × 100
sample powders (1.25, 2.5, 3.75, or 5 g) were mixed with
20 ml methanol (Sigma, St. Louis, MO, USA) in a rotary
Reducing Power Test
shaker for 12 h. The mixtures were then filtered (Whatman
No.1, Middlesex, England). The filtrate was then concen-
Reducing power was measured according to the method
trated in a rotary evaporator (Büchi R-210, Flawil, Switzer-
described by Duh and Yen [17]. One ml of plant extract,
land) until dried. The weight of extract was then measured
phosphate buffer (0.2 M, pH 6.6, 0.5 ml), and potassium
and recorded. The yield of methanolic extract was
hexacyanoferrate solution (1% v/w, 2.5 ml; both from
expressed as milligram of extract per gram of ginger fresh
Merck) were placed in a test tube and heated at 50 °C for
weight, calculated as follows:
20 min. The tube was cooled on ice and 0.5 ml 10%
Yield = weight of Rotavapor dried sample (mg)/fresh
trichloroacetic acid (Merck) were added. After centrifuga-
sample (g) × 100%
tion at 3,000×g for 10 min, a 1 ml of aliquot supernatant
was mixed with 1 ml distilled water and 0.1 ml ferric
Total Phenolics Determination
chloride (0.1%) and reacted for 10 min. Finally, the
absorbance at 700 nm was measured, increased absorbance
The total phenolics content of ginger extracts was deter-
of the reaction mixture indicated increased reducing power.
mined by the Folin–Ciocalteau method [13]. Briefly, 0.5 ml
diluted extract solution was shaken for 1 min with 100 ?l of
Antimicrobial Activity
Folin–Ciocalteau reagent and 6 ml of distilled water. The
mixture was shaken and 2 ml of 15% Na2CO3 were added
To screen the activity of methanolic extracts of Zingiberaceae
and shaken once again for 30 s. Finally, the solution was
plants against food related microorganism, a filter paper disc
brought up to 10 ml by adding distilled water. After 1.5 h,
method was used as described by Gülçin et al. [18].
the absorbance at 750 nm was evaluated using a spectro-
Escherichia coli Bioresources Collection and Research
photometer (Beckman Coulter DU-640, CA, USA). The
Center (BCRC) 10675, Salmonella enterica BCRC 10242,
results were expressed as gallic acid equivalents.
Staphylococcus aureus spp. aureus BCRC 10451 and Vibrio

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Plant Foods Hum Nutr (2008) 63:15–20
17
parahaemolyticus BCRC 12863 were purchased from BCRC,
Table 1. Extraction yield ranged from lowest 41 mg/g
Republic of China. E. coli stock cultures were maintained on
(Alpinia pricei Hayata) to highest 127 mg/g (Alpinia
potato dextrose agar (Difco, Detroit, MI, USA) and the other
zerumbet (Pers.) Burtt & Smith), notably Vanoverberghia
three were kept on nutrient agar (Difco, Detroit, MI, USA)
sasakiana, the endemic species Taiwan has second high in
according to the culture manual. Culture concentrations of 1×
extraction rate of 177 mg/g. Average extraction rate was
108 colony-forming unit/ml were plated on their respective
found to be 0.084% (84 mg/g). Habsah et al. [6] has
agar plates. Sterile filter paper discs with 6 mm diameter
displayed the methanolic extraction rate of Alpinia, Costus
(Whatman) were immersed with 500 ?l of Zingiberaceae
and Zingiber, which ranged 0.09–0.57% in various samples.
extract. After thorough absorption, they were then placed on
In general, freeze drying preserves more reducing power of
agar plate for cultivation. Salmonella plates were incubated at
plant extract, such as yam (Dioscorea sp.) extract as
30 °C, while E. coli, Staphylococcus and Vibrio plates were
compared to hot-air drying and drum drying [20]. The color
kept at 37 °C for 72 h. The results were recorded by
and appearance of our vacuum-dried samples remained
measuring the zones of growth inhibition surrounding the
unchanged and intact. V. sasakiana showed a 36.5 mg/g of
disc. Clear inhibition zones around the discs indicated the
total phenol content (Table 1), highest in Taiwan endemic
presence of antimicrobial activity. All data on antimicrobial
species.
activity are the average of triplicate analyses. Amoxicillin–
clavulanic acid (ACA; 20 ?g /1 ml per disc); ofloxacin
Antioxidant Capacity, DPPH Scavenging and Reducing
(20 ?g /1 ml per disc; Sigma) were used as references. Ginger
Power
extracts with antimicrobial activity were serially diluted into
concentration ranging from 1.0–0.01 mg/ml for determination
On average, antioxidant activity of our nine Alpinia samples
of their minimum inhibitory concentration (MIC) according
was 67%, which was the lowest of the total antioxidant
to Habsah et al. [6] and Wilson et al. [19].
performance. The activity was highest in Vanoverberghia
and Hedychium, both 89% (Table 2). In DPPH scavenging
activity and reducing power, Vanoverberghia and
Results
Hedychium extract exhibited similar levels as those of total
antioxidant contents. Particularly, Zingiber sp. exhibited
Extraction Yield
poorest performances in DPPH and reducing power. The
rest of the Zingiberaceae plant extracts displayed an average
Extraction yield was expressed as weight (mg) of crude
of 70–78% in DPPH scavenging properties and 0.87
extract per gram of vacuum-dried plant material as shown in
(Alpinia) to 1.13 (Curcuma) in absorbance A700 (Table 2).
Table 1 Extraction yield and contents of total phenolics of gingers
Species
Collection site
Extraction yield (mg/g)
Total phenols (mg/g)
1
Alpinia japonica (Thunb.) Mig
Hsinchu county
58.8±7.7
18.3±6.3
2
Alpinia kawakamii Hayata
TESRI, Jiji township, Nantou county
79.3±15.6
18.7±3.4
3
Alpinia kusshakuensis Hayata
Sindian city, Taipei county
64.3±6.4
19.5±1.45
4
Alpinia mesanthera
Fusing township, Taoyuan county
82.6±5.8
19.5±4.3
5
Alpinia officinarum
Sansia township, Taipei county
52.2±6.3
19.3±2.5
6
Alpinia pricei Hayata
Hengchun, Pingtung county
41.1±11.7
19.2±5.1
7
Alpinia shimadai
Jhudong township, Hsinchu county
107.5±19.4
20.2±5.3
8
Alpinia uraiensis Hayata
Yilan county
89.5±13.9
17.6±1.5
9
Alpinia zerumbet (Pers.) Burtt & Smith
TESRIa, Jiji township, Nantou county
127.5±3.8
15.3±2.2
10
Costus speciosus (Koenig) Smith
Sioushuei township, Changhua county
93.2±9.7
22.9±2.3
11
Curcuma domestica
Jhongpu township, Chiayi county
87.1±6.3
35.6±5.5
12
Curcuma longa L.
Ren-ai township, Nantou county
94.2±7.5
21.4±1.7
13
Curcuma viridiflora
Fongshan city, Kaohsiung county
91.4±5.8
29.4±3.7
14
Curcuma zedoaria
Pingtung city, Pingtung county
92.5±7.6
33.4±5.7
15
Hedychium coronarium Koenig
Jinshan county, Taipei county
32.6±5.8
25.8±4.4
16
Vanoverberghia sasakiana
Lanyu township, Taitung county
117±12.6
36.5±8.9
17
Zingiber kawagoii Hayata
Beinan township, Taitung county
95.6±7.4
28±2.9
18
Zingiber oligophyllum K. Schumann
Jhongpu township, Chiayi county
74±4.3
20±4.5
a All value in this table represent the mean ± SD (n=3)

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Plant Foods Hum Nutr (2008) 63:15–20
Table 2 Multiple antioxidant capacity of gingers
Ginger sample
Antioxidant capacity
DPPH free radical scavenging activity
Reducing power (absorbance
(%)
(%)
700 nm)
1
Alpinia japonica (Thunb.) Mig
69.5a±6.7b
71.8±6.4
0.8±0.2
2
Alpinia kawakamii Hayata
73.5±4.6
76.7±5.3
0.9±0.1
3
Alpinia kusshakuensis Hayata
70.9±5.67
76.7±6.3
0.8±0.1
4
Alpinia mesanthera Hayata
62.3±7.6
64.6±7.4
0.8±0.3
5
Alpinia officinarum
75.4±9.6
80.5±9.3
1.4±0.2
6
Alpinia pricei Hayata
70.6±7.9
74.9±5.4
0.7±0.15
7
Alpinia shimadai
72.2±1.3
69.3±7.3
1.0±0.3
8
Alpinia uraiensis Hayata
62.5±5.8
68.6±4.3
0.8±0.4
9
Alpinia zerumbet (Pers.) Burtt & Smith
53.8±8.6
59.4±3.5
0.47±0.2
10
Costus speciosus (Koenig) Smith
81.3±6.7
78.5±4.4
1.3±0.3
11
Curcuma domestica
89±7.4
81.3±6.3
1.6±0.4
12
Curcuma longa L.
76.1±5.1
72.1±5.2
1.2±0.5
13
Curcuma viridiflora
53±5.3
76.4±5.0
1.1±0.2
14
Curcuma zedoaria
76±6.4
65.4±6.1
0.9±0.2
15
Hedychium coronarium Koenig
89.6±11.6
90.1±7.2
1.6±0.3
16
Vanoverberghia sasakiana Funak. &
89±6. 9
89.5±7.1
1.01±0.2
H. Ohashi
17
Zingiber kawagoii Hayata
79±4.8
42±7.8
0.9±0.08
18
Zingiber oligophyllum K. Schumann
88±5.9
32±9.3
0.34±0.08
a Concentration of each methanolic extract was adjusted to 100 mg/ml
b All values in this table represent the mean ± SD (n=3)
Antimicrobial Activity
Alpinia sp. showed no inhibition zone against Vibrio. Three
cultivars Alpinia japonica, Alpinia kawakamii and Alpinia
Most Zingiberaceae plant extracts exhibited antimicrobial
kusshakuensis, now acclimated cultivars in Taiwan, showed
activity against all tested microorganisms (Table 3). Few
resistance to all of the four microorganisms (Table 3).
Table 3 Antimicrobial activities of gingers, and amoxicillin–clavulanic acid, ofloxacin (parenthesis indicates minimum inhibitory concentration
(mg/ml) for antimicrobial activity of Zingiberaceae extracts)
Species
Escherichia coli
Salmonella enterica
Staphylococcus aureus
Vibrio parahaemolyticus
1
Alpinia japonica (Thunb.) Mig
13a (0.05)
8 (0.05)
8 (0.08)
15 (0.05)
2
Alpinia kawakamii Hayata
12.5 (0.05)
9 (0.05)
7 (0.05)
12 (0.05)
3
Alpinia kusshakuensis Hayata
7 (0.05)
10 (0.08)
9 (0.05)
8 (0.05)
4
Alpinia mesanthera
9 (0.05)
10 (0.05)
13 (0.08)
11 (0.05)
5
Alpinia officinarum
11 (0.05)
–
5 (0.05)
–
6
Alpinia pricei Hayata
4 (0.05)
9 (0.05)
10 (0.05)
–
7
Alpinia shimadai
9 (0.08)
11 (0.05)
9 (0.05)
–
8
Alpinia uraiensis Hayata
12 (0.05)
12 (0.05)
14 (0.08)
–
9
Alpinia zerumbet (Pers.) Burtt & Smith
6 (0.05)
7 (0.08)
9 (0.05)
8 (0.05)
10
Costus speciosus (Koenig) Smith
11 (0.05)
8 (0.05)
11 (0.05)
–
11
Curcuma domestica
15 (0.05)
17 (0.05)
20 (0.05)
18 (0.05)
12
Curcuma longa L.
17 (0.05)
6 (0.05)
–
13 (1.0)
13
Curcuma viridiflora
15.6 (0.05)
19 (1.0)
18 (0.05)
20 (0.05)
14
Curcuma zedoaria
16 (0.05)
13.5 (0.05)
11 (0.05)
–
15
Hedychium coronarium Koenig
–
9 (0.05)
14 (0.05)
–
16
Vanoverberghia sasakiana
–
8 (0.05)
9 (0.05)
–
17
Zingiber kawagoii Hayata
11 (0.05)
9 (0.02)
11 (0.05)
8 (0.05)
18
Zingiber oligophyllum K. Schumann
9 (0.08)
–
6.5 (0.05)
8 (0.08)
19
ACAb
20
18
15
15
20
Ofloxacinc
18
15
–
12
a Diameter of zone (mm)
b Amoxicillin-clavulanic acid (20 ?g /1 ml per disc)
c Ofloxacin (20 ?g /1 ml per disc)

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Plant Foods Hum Nutr (2008) 63:15–20
19
1.6
1.4
1.4
1.2
1.2
Untreated
ACA
1. 1
0
1.0
Ofloxacin
m
Curcuma viridiflora
0n
0nm
60
0.8
Curcuma domestica
60 0.8
OD
OD 0.6
0.6
0.4
0.4
0.2
0.2
0
0
0 1
6
12
18
24
30
0 1
6
12
18
24
30
Time (h)
Time (h)
a
b
1.6
1.6
1.4
1.4
1.2
1.2
1.0
m
1.0
0n
60 0.8
0nm
60 0.8
OD 0.6
OD 0.6
0.4
0.4
0.2
0.2
0
0
0
6
12
18
24
30
0
6
12
18
24
30
Time (h)
Time (h)
c
d
Fig. 1 Effect of Curcuma extracts on the growth of E. coli (a), Salmonella enterica (b), Staphylococcus aureus (c) and Vibrio parahaemolyticus (d)
Curcuma sp., of which the antimicrobial properties have
active against E. coli, S. enterica and S. aureus, but not for
been widely studied [3, 6, 8], also exhibited strong
V. parahaemolyticus. The MIC ranged from 0.05 to 1.0 mg/
inhibition in this study. However, Hedychium and Vano-
ml (Table 3), among these, A. japonica, A. mesanthera and
verberghia, both with high antioxidant activities did not
A. uraiensis need higher concentration to inhibit Staphylo-
showed antimicrobial activities on E. coli and V. para-
coccus (0.08 mg/ml). However, in the findings of Habsah et
haemolyticus (Table 3). The species which performed best
al. [6], most potent inhibitory activity against Bacillus
in the inhibition zone tests, Curcuma domestica and
substilis and Staphylococcus was brought by Alpinia mutica
Curcuma viridiflora were chosen for the further test of
and Aspergillus ochraceous. Inconsistence of concentration
inhibition in culture broths. Figure 1 shows that two of the
may due to species variation.
Curcuma species have similar antimicrobial activities as
ACA and ofloxacin. Wilson et al. [19] compared the
antimicrobial effects of Curcuma zedoaria and Curcuma
Discussion
malabarica against S. aureus. Their finding indicated that
C. zedoaria does not inhibit growth of this food bacteria
Zingiberaceae plants have received much attention, since
and our results were similar to it. Three of the other
they produce many complex compounds that are useful in
Curcuma species exhibited strong inhibition against above
food as herbs and spices, flavoring and seasoning, and in
food bacteria. Generally, most of the plant extracts gave a
the cosmetics and medicinal industries as antioxidant and
MIC of 0.05 mg/ml (Table 3). Notably, C. zedoaria showed
antimicrobial agents. The theory of oxygen-stress on aging
MIC of 0.05 mg/ml against Staphylococcus, the results
and age-degenerated diseases places an importance on
were not similar to that of Wilson et al. [19]. This could be
daily use of natural phytochemicals and compounds [21].
explained because different microorganisms were used and
Bhandari et al. [22] administered an ethanolic extract of Z.
different extraction procedures were used. In general,
officinale abstract for diabetic rats. A dosage of 200 mg/kg
methanolic extracts of samples were almost completely
produced effects such as lowered serum total cholesterol

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Plant Foods Hum Nutr (2008) 63:15–20
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reduced lipid peroxidation in tissues [23]. However, they
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The authors would like to thank Taiwan Endem-
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appreciated.
92
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