Food Chemistry 124 (2011) 514517

Contents lists available at ScienceDirect

Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem

Essential oils of Zingiber ofcinale var. rubrum Theilade and their

antibacterial activities
Yasodha Sivasothy a, Wong Keng Chong b, Abdul Hamid b, Ibrahim M. Eldeen c,d, Shaida Fariza Sulaiman c,
Khalijah Awang a,*
a
Department of Chemistry, Faculty of Science, University Malaya, 50603 Kuala Lumpur, Malaysia
b
School of Chemical Sciences, Universiti Sains Malaysia, 11800 Minden, Penang, Malaysia
c
School of Biological Sciences, Universiti Sains Malaysia, 11800 Minden, Penang, Malaysia
d
Faculty of Forestry, University of Khartoum, Shambat Campus, 13314 Khartoum Bahri, Sudan

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

Article history: The essential oils obtained by hydrodistilation of the leaves and rhizomes of Zingiber ofcinale var. rubrum
Received 23 February 2010 Theilade were analysed by capillary GC and GCMS. Forty-six constituents were identied in the leaf oil,
Received in revised form 4 May 2010 while 54 were identied in the oil from the rhizomes. The leaf oil was clearly dominated by b-caryophyl-
Accepted 16 June 2010
lene (31.7%), while the oil from the rhizomes was predominantly monoterpenoid, with camphene
(14.5%), geranial (14.3%), and geranyl acetate (13.7%) the three most abundant constituents. The evalua-
tion of antibacterial activities using the micro-dilution technique revealed that both the leaf and rhizome
Keywords:
oils were moderately active against the Gram-positive bacteria Bacillus licheniformis, Bacillus spizizenii and
Zingiber ofcinale var. rubrum Theilade
Halia bara
Staphylococcus aureus, and the Gram-negative bacteria Escherichia coli, Klebsiella pneumoniae and Pseudo-
Essential oils monas stutzeri.
Antibacterial activity 2010 Elsevier Ltd. All rights reserved.
b-Caryophyllene
Camphene

1. Introduction
The genus Zingiber comprises about 85 species of herbs mostly
distributed in East Asia and tropical Australia. Many of these are
used as food and for traditional treatment of a variety of ailments
(Sabulal et al., 2006). The essential oil composition of many of
these herbs and their biological activities has been the subject of
numerous previous studies (Bordoloi, Sperkova, & Leclercq, 1999;
Kami, Nakayama, & Hayashi, 1972; Prakash, Pant, & Mathela,
2006; Sabulal et al., 2006; Sacchetti et al., 2005; Srivastava, Srivast-
ava, & Shah, 2002; Vahirua-Lechat, Menut, Lamaty, & Bessiere,
1996; Zhannan, Shiqiong, Quancai, Chao, & Zhengwen, 2009). Phy-
tochemical investigation of the rhizomes of several Zingiber sp. has
revealed the presence of bioactive compounds, such as gingerols,
which are antibacterial agents and shogaols (Kim et al., 2008; Park,
Bae, & Lee, 2008), diarylheptanoids (Zhou et al., 2007), phenylbut-
enoids (Jitoe, Masuda, & Nakatani, 1993), avanoids (Dae, Han,
Park, Jhon, & Seo, 2004), diterpenoids (Akiyama et al., 2006), and
sesquiterpenoids (Dae & Seo, 2005).
Zingiber ofcinale var. rubrum Theilade is distributed mainly in
Peninsular Malaysia, where it is known as halia bara. This herb is
* Corresponding author. Tel.: +60 3 79674064; fax: +60 3 79674193.
E-mail address: khalijah@um.edu.my (K. Awang).
cultivated for its medicinal value. Its rhizome is a common ingredi-
ent in folk medicine (jamu) for treating stomach discomfort,
tumours, relieving rheumatic pains, and as a post partum medicine
(Ibrahim et al., 2008). Halia bara is morphologically similar to the
common ginger (halia), but the rhizomes of this variant are smaller
and more pungent, red on the outside with a yellow to pinkish
cross-section, while the base of its leaf shoot is red. Unlike the
common ginger, the petiole of halia bara is reddish when young,
and the lip is scarlet red mottled with cream (Ibrahim et al.,
2008). Little is known about the chemical constituents of this
variety apart from a paper which reported the composition of the
rhizome oil, which comprised mainly geranial, neral and geranyl
acetate (Malek et al., 2005).
Infectious diseases are the leading cause of death worldwide.
The emergence of multidrug resistant pathogens threatened the
clinical efcacy of many existing antibiotics. This situation fuels
the ongoing research to discover antimicrobial agents from natural
origins (Eldeen, Van Heerden, & Van Staden, 2010). The methanol
extract of Zingiber ofcinale rhizomes was reported to possess sig-
nicant antibacterial activities against Escherichia coli, Salmonella
enteriditis and Staphylococcus aureus during an in vitro investigation
(Anbu Jeba Sunilson, Suraj, Rejitha, & Anandarajagopa, 2009).
Hence, in continuation of our investigation on the essential oils
of the Zingiberaceae family and their antimicrobial activities

0308-8146/$ - see front matter 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodchem.2010.06.062
 Y. Sivasothy et al. / Food Chemistry 124 (2011) 514517
(Wong, Sivasothy, & Boey, 2006a, 2006b, 2006c; Ibrahim et al.,
2009a, 2009b), this prompted us to investigate the chemical com-
position of the leaf and rhizome oils of halia bara in detail, and uti-
lise these oils in an attempt to explore alternative sources of
antibacterial agents to treat multidrug resistant pathogens that
cause infections and food poisoning, which to the knowledge of
the authors have not been previously reported.
2. Materials and methods
2.1. Plant material
Fresh leaves and rhizomes of halia bara were purchased from a
market in Negeri Sembilan in September, 2009, and a voucher
specimen (KU 0107) has been deposited with the herbarium of
University of Malaya.
2.2. Solvents and chemicals
Pentane (GCMS grade) and ethanol (analytical grade) were
purchased from Merck (Germany) and Systerm (Malaysia), respec-
tively. The homologous series of n-alkanes (C6C30) was purchased
from Dr. Ehrenstorfer Gmbh (Germany). Reference compounds
were obtained from SigmaAldrich (USA). MuellerHinton broth
was purchased from OXOID (England), and Tetracap 250 from Ho-
vid (Malaysia). p-Iodonitrotetrazolium violet (INT) was obtained
from SigmaAldrich (USA).
2.3. Isolation of essential oils
Fresh leaves (45 g) and homogenised rhizomes (125 g) were
separately hydrodistiled for 4 h in an all-glass apparatus similar
to that described in the British Pharmacopoeia, using pentane as
the collecting solvent. The solvent was carefully removed using a
gentle stream of nitrogen gas, yielding yellow aromatic oils in each
case. The oil yields (w/w) were 0.03% (leaves) and 0.02% (rhi-
zomes), all on a fresh weight-basis.
2.4. Gas chromatography (GC)
GC analysis was carried out using an Agilent 7890A GC System
equipped with a FID and an Agilent 7683B Series auto-injector.
HP-5MS UI (30 m  0.25 mm id, lm thickness 0.25 lm) fused-silica
capillary column (J.W. Scientic) was employed. The operating con-
ditions were as follows: initial oven temperature, 50 C for 5 min,
then to 150 C at 4 C min 1 and held for 5 min, then to 250 C at
4 C min 1 and held for 10 min; injector and detector temperatures,
275 C; carrier gas, 1.0 ml min 1 N2; injection volume, 0.2 ll; split
ratio, 50:1. The quantitative data were obtained electronically from
FID area per cent without the use of correction factors.
2.5. Gas chromatographymass spectrometry (GCMS)
GCMS analysis was performed using an Agilent 6890 N Net-
work GC System equipped with an Agilent 7683B Series auto-injec-
tor, coupled to an Agilent 5975 Inert Mass Selective Detector and
the same capillary GC conditions as described above. The carrier
gas used was He at 1.0 min 1. The signicant MS operating param-
eters were: ionisation voltage, 70 eV; ion source temperature
230 C; mass range 50600 U.
2.6. Identication of constituents
The constituents were identied by comparison of their mass
spectra with those of authentic compounds or with reference
515
spectra in the computer library (NIST 05), and conrmed by com-
parison of retention indices with those of authentic compounds, or
with data in the literature (Adams, 2001).
2.7. Micro-dilution antibacterial assay
The serial dilution technique by Eloff in 1998 (Eldeen, Elgorashi,
& van Staden, 2005), using 96-well micro-plates was employed to
determine the minimum inhibitory concentration (MIC) of the
essential oils for antibacterial activity. Two millilitres cultures of
three Gram-positive bacterial strains, Bacillus licheniformis
(ATCC12759), Bacillus spizizenii (ATCC6633) and Staphylococcus
aureus (ATCC12600), and three Gram-negative bacterial strains,
Escherichia coli (ATCC25922), Klebsiella pneumoniae (ATCC13883)
and Pseudomonas stutzeri (ATCC17588), were prepared and placed
in an incubator overnight at 37 C. The overnight cultures were di-
luted with sterile MuellerHinton (MH) broth (1 ml bacteria/50 ml
MH) to yield a density of bacterial cells between 106108 cells/ml.
The extracts were resuspended to a concentration of 10 mg/ml
with ethanol, to yield a nal concentration of 2.5 mg/ml in the as-
say. For each of the six bacteria used, 100 ll of redissolved extract
were serially diluted twofold with 100 ll of sterile distilled water,
in a sterile 96-well micro-plate. A similar twofold serial dilution of
tetracycline (1 mg/ml) was used as a positive control against each
bacterium. Ethanol (100%) was used as a negative control to yield a
nal concentration of 25% in the assay. One hundred microlitres of
each bacterial culture were added to each well. The plates were
covered and incubated overnight at 37 C. To indicate bacterial
growth, 50 ll of 0.2 mg/ml p-iodonitrotetrazolium violet (INT)
were added to each well, and the plates were incubated at 37 C
for 30 min. Bacterial growth in the wells was indicated by a red
colour, whereas clear wells indicated the absence of active bacte-
rial growth. The assay was repeated three times.
3. Results and discussion
3.1. Composition of the essential oils
Table 1 lists the oil constituents identied in the leaves and rhi-
zomes of halia bara, the relative GC peak areas of these constitu-
ents, and their experimental retention indices on the HP-5 MS UI
column.
Forty-six compounds, constituting 91.7% of the leaf oil of halia
bara, were identied. Sesquiterpenoids (47.1%) and monoterpe-
noids (42.6%) were dominant, although these gures were largely
due to b-caryophyllene (31.7%), geranial (13.1%), neral (9.8%) and
caryophyllene oxide (6.3%). Other quantitatively signicant
constituents included geraniol (4.4%), a-pinene (4.1%) and trans,-
trans-a-farnesene (3.2%). The most abundant component, b-caryo-
phyllene, is known for its anti-inammatory and local anaesthetic
activities. It is used in spice blends, citrus avours, soaps, deter-
gents, creams and lotions and also in a variety of food products.
It has also been identied as a volatile compound emitted by plants
into the atmosphere in response to herbivore attack (Sabulal et al.,
2006).
The oil from the rhizomes of this variety yielded 54 identied
constituents, accounting for 95.5% of the sample. The oil was very
rich in monoterpenoids (81.9%), comprising mainly camphene
(14.5%), geranyl acetate (13.7%), geranial (14.3%), neral (7.7%),
geraniol (7.3%), and 1,8-cineole (5.0%). The presence of neral and
geranial possibly contributed to the strong aroma reminiscent of
lemon in the rhizomes similar to those of the common ginger from
Australia (Wohlmuth, Smith, Brooks, Myers, & Leach, 2006). Bor-
neol, bornyl acetate and 1,8-cineole, together, probably accounted
for a trace of its camphoraceous odour (Bauer, Garbe, & Surburg,
516 Y. Sivasothy et al. / Food Chemistry 124 (2011) 514517

Table 1 in the oil from the rhizomes. A previous investigation of the rhi-
Constituents identied in the leaf and rhizome oils of Z. ofcinale var. rubrum Thielade zome oil of halia bara by Malek et al. (2005) also revealed a high
(halia bara).
content of monoterpenoids (64.6%). They, however, identied only
Constituent RI (HP-5MS UI) Area (%)a 19 constituents among which 17 were common to the present
Leaves Rhizomes study, and found much lower levels of camphene (1.8%) and gera-
2-Heptanol 902 0.9 0.1
nyl acetate (8.8%). They did not detect geraniol but reported much
Tricyclene 922 0.2 higher levels of neral (14.2%), geranial (28.4%) and b-sesquiphel-
a-Pineneb 934 4.1 3.6 landrene (9.9%). These marked differences in the composition of
Campheneb 949 t 14.5 the rhizome oil determined by Malek et al. (2005) from that of
Sabinene 974 0.2 0.1
the present study could be attributed to the source, cultivation,
b-Pineneb 977 2.0 0.6
6-Methyl-5-hepten-2-one 988 0.2 0.2 vegetative stage and growing season of the plant under investiga-
Myrceneb 992 1.3 2.0 tion (Sari et al., 2006).
a-Phellandreneb 1004 0.2 0.2 There are also signicant differences when the present results
d-3-Carene 1010 0.1 0.1
are compared with the composition of the rhizome oil of the com-
p-Cymene 1025 0.1 0.1
Limonene 1029 2.5
mon ginger collected from various locations, as the rhizome oil of
b-Phellandrene 1030 2.6 the common ginger is typically characterised by high percentages
1,8-Cineole 1032 0.7 5.0 of sesquiterpene hydrocarbons, in particular, a-zingiberene, ar-
cis-b-Ocimene 1039 0.1 curcumene b-bisabolene and b-sesquiphellandrene (Norajit, Lao-
2-Heptyl acetate 1044 0.2 0.3
hakunjit, & Kerdchoechuen, 2007; Onyenekwe & Hashimoto,
Trans-b-ocimene 1049 0.2
c-Terpinene 1060 0.1 0.1 1999; Pino, Marbot, Rosado, & Batista, 2004; Singh, Maurya, Cata-
Terpinolene 1089 0.4 lan, & de Lampasona, 2005; Wohlmuth et al., 2006).
2-Nonanone 1093 0.2
Linaloolb 1100 1.1 2.3
Trans-sabinene hydrate 1122 0.1 3.2. Antibacterial activity of the essential oils
Camphorb 1147 0.3
Camphene hydrate 1151 0.2 The leaf and rhizome oils were tested against three Gram-posi-
Citronellal 1155 0.1 0.1
tive (B. licheniformis, B. spizizenii, S. aureus) and three Gram-negative
Isoborneol 1160 0.1
Borneolb 1168 2.9 (E. coli, K. pneumoniae, P. stutzeri) bacteria. The results (Table 2)
Terpinen-4-ol 1180 0.3 0.3 from the bioassays revealed that the leaf oil and the oil from the
a-Terpineolb 1193 0.4 1.1 rhizomes of halia bara possessed moderate antibacterial activity
Myrtenal 1199 0.2 0.1
(MIC values of 0.160.63 mg/ml) against all tested bacterial strains,
Linalyl formate 1216 0.5
b-Citronellol 1229 0.4
which could have resulted from the presence of caryophyllene
Neralb 1243 9.8 7.7 oxide, a-pinene, a-terpineol, linalool, 1,8-cineole and geraniol,
Geraniol 1256 4.4 7.3 compounds that are known to possess antibacterial activity.
Trans-2-decenal 1259 0.3 Although present in low concentrations, the aforementioned con-
Geranialb 1273 13.1 14.3
stituents could have imparted a signicant effect on the antibacte-
Bornyl acetateb 1289 1.4
2-Undecanone 1295 0.2 0.1 rial activities of the oils via a synergistic effect (Giles, Zhao, An, &
Myrtenyl acetate 1329 0.1 Agboola, 2010; Vagionas, Graikou, Ngassapa, Runyoro, & Chinou,
Neryl acetate 1366 0.1 2007a; Vagionas et al., 2007b). In general, both oils exhibited bet-
a-Copaene 1380 0.6 0.2 ter antibacterial activity against the Gram-positive bacteria (with
Geranyl acetateb 1384 1.0 13.7
b-Elemene 1395 0.2
MIC values of 0.160.31 mg/ml) than against the Gram-negative
Isocaryophyllene 1411 0.1 bacteria (with MIC values of 0.310.63 mg/ml). This is in accor-
b-Caryophyllene 1424 31.7 1.0 dance with previous reports indicating that Gram-negative bacte-
a-Humuleneb 1458 0.9 1.1 ria are more resistant to essential oils compared to Gram-
Allo-aromadendrene 1465 0.3 0.2
positive bacteria (Kivrak et al., 2009; Oyedeji, Lawal, Shode, &
Ar-curcumeneb 1485 1.0
Germacrene D 1486 0.2 Oyediji, 2009; Sari et al., 2006). Based on our ndings, the sensitiv-
a-Zingibereneb 1495 3.2 ity of the bacterial strains to the leaf oil decreases in the order B.
a-Selinene 1496 0.3 licheniformis = S. aureus > B. spizizenii > P. stutzeri > K. pneumoniae >
a-Muurolene 1503 1.1 0.3 E. coli, while for the rhizome oil, the order is: B. licheniformis > B.
Trans,trans-a-farnesene 1508 3.2 1.8
b-Sesquiphellandreneb 1524 1.6
spizizenii > S. aureus = E. coli > K. pneumoniae > P. stutzeri. S. aureus,
d-Cadinene 1525 0.3 E. coli and Bacillus sp. are agents of food poisoning (Kivrak et al.,
a-Elemol 1549 0.6 2009). The low MIC values of the leaf, rhizome and root oils seen
Trans-nerolidol 1561 0.6 0.1 here against B. licheniformis, B. spizizenii, S. aureus and E. coli would
Caryophyllene oxide 1587 6.3 0.2
suggest that the oils from halia bara could possibly be used as nat-
c-Eudesmol 1653 0.6
Caryophyllenedienol I 1641 0.4 ural preservatives against food-borne pathogens or for delaying
b-Eudesmol 1652 0.3 0.1
Table 2
a-Bisabolol 1690 0.3
Antibacterial activity (MIC) of the leaf and rhizome oils of Z. ofcinale var. rubrum
Cis,cis-farnesol 1717 0.3 0.1
Thielade (halia bara) as determined by the micro-dilution assay.
Trans,trans-farnesol 1723 0.2
Trans,trans-farnesal 1730 0.3 0.1 Bacterial Strains MIC (mg/ml)
Phytol 2058 0.2
Leaf oil Rhizome oil Tetracycline
91.7% 95.5%
3
Bacillus licheniformis (ATCC12759) 0.16 0.16 1.0  10
a 3
Percentage of total FID area obtained on HP-5 MS UI column, t = (<0.05%). Bacillus spizizenii (ATCC6633) 0.24 0.24 1.8  10
b 3
Previously reported by Malek et al. (2005). Staphylococcus aureus (ATCC12600) 0.16 0.31 7.7  10
3
Escherichia coli (ATCC25922) 0.63 0.31 15.6  10
3
Klebsiella pneumoniae (ATCC13883) 0.47 0.47 3.7  10
2001). It is interesting that b-caryophyllene, the most abundant 3
Pseudomonas stutzeri (ATCC17588) 0.31 0.63 8.1  10
constituent of the leaf oil, was only found at a low level of 1.0%
 Y. Sivasothy et al. / Food Chemistry 124 (2011) 514517
food spoilage. However, further investigation on the activities of
these oils against other food-borne pathogens (Listeria sp., Salmo-
nella sp.) should be conducted.
4. Conclusions
The leaf oil and the oil from the rhizomes of halia bara differed
in chemical composition, the former comprising mainly sesquit-
erpenoids and monoterpenoids in approximately equal amounts,
while the latter was dominated by monoterpenoids. Antimicrobial
assays of these oils have demonstrated that the Gram-positive bac-
teria in this study were more sensitive to both the oils compared to
the Gram-negative bacteria. Toward the leaf oil, B. licheniformis and
S. aureus were the most sensitive strains, while E. coli was the most
resistant strain. B. licheniformis and P. stutzeri were the most sensi-
tive and resistant strains, respectively, toward the oil of the rhi-
zomes. The sensitivity of the B. licheniformis, B. spizizenii, S.
aureus and E. coli strains toward both oils would suggest that these
oils may be promising natural preservatives in the food industry.
However, it is commendable that further analysis should be carried
out on other food poisoning agents, such as Listeria sp., Salmonella
sp.
Acknowledgements
The authors acknowledge the research grant 5702031007 (Sci-
ence Fund) provided by the French Government that has resulted
in this article. The authors wish to thank Mr. Teo, Mr. Ray and
Mr. Din in assisting with the preparation of the voucher specimen,
and Ms. Saripah in assisting with the GCMS analysis.
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