Pharmaceutical Biology

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Antifungal Activity of the Essential Oils of Nine

Zingiberaceae Species

Ibrahim bin Jantan, Mohd Salleh Mohd Yassin, Chen Bee Chin, Lau Lee Chen
& Ng Lee Sim

To cite this article: Ibrahim bin Jantan, Mohd Salleh Mohd Yassin, Chen Bee Chin, Lau Lee Chen
& Ng Lee Sim (2003) Antifungal Activity of the Essential Oils of Nine Zingiberaceae Species,
Pharmaceutical Biology, 41:5, 392-397, DOI: 10.1076/phbi.41.5.392.15941

To link to this article: https://doi.org/10.1076/phbi.41.5.392.15941

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 Pharmaceutical Biology
2003, Vol. 41, No. 5, pp. 392–397
Antifungal Activity of the Essential Oils of Nine
Zingiberaceae Species
Ibrahim bin Jantan1, Mohd Salleh Mohd Yassin2, Chen Bee Chin2, Lau Lee Chen2 and Ng Lee Sim2
1
Department of Pharmacy, 2Department of Biomedical Sciences, Faculty of Allied Health Sciences, Universiti Kebangsaan
Malaysia, Jalan Raja Muda Abdul Aziz, Kuala Lumpur, Malaysia
Abstract
The rhizome oils of nine Zingiberaceae species [Zingiber
officinale Rosc., Z. cassumunar Roxb., Z. zerumbet Smith,
Curcuma aeruginosa Roxb., C. mangga Valeton and van
Zyp, C. xanthorrhiza Roxb., Kaempferia galanga Linn.,
Alpinia galanga Swartz and Boesenbergia pandurata (Roxb.)
Schlecht] were investigated for their antifungal activities
against five dermatophytes (Trichophyton mentagrophytes, T.
rubrum, Microsporum canis, M. nanum and Epidermophyton
floccosum), three filamentous fungi (Aspergillus niger, A.
fumigatus and Mucor sp.) and five strains of yeast (Saccha-
romyces cerevisiae, Cryptococcus neoformans, Candida
albicans, Ca. tropicalis and Torulopsis glabrata). The anti-
fungal testing was carried out by using the broth microdilu-
tion and the disc gel diffusion methods. Amongst the
essential oils studied, only the oil of B. pandurata was effec-
tive against all the fungi, exhibiting the lowest MIC values
of 0.63 mg ml-1 to Mucor sp., 1.25 mg ml-1 to both A. niger and
A. fumigatus, and 2.5 mg ml-1 to both T. rubrum and E. floc-
cosum, and the highest inhibition zone diameter of 20.6 mm
against S. cerevisiae. The essential oil of K. galanga showed
selective toxicity against A. fumigatus with a MIC value of
0.63 mg ml-1, while the essential oils of Z. officinale and Z.
cassumunar exhibited high activity against the yeasts
(11.7–15.7 mm). The chemical composition of the active
essential oils was investigated by GC and GC-MS.
Keywords: Zingiberaceae species, essential oils, antifungal
activity, yeasts, dermatophytes, filamentous fungi, disc gel
diffusion, broth microdilution.
Introduction
There are about 47 genera and 500 species of the Zingiber-
aceae family and they are distributed throughout the tropical
Accepted: November 15, 2002
Address correspondence to: Ibrahim bin Jantan, Department of Pharmacy, Faculty of Allied Health Sciences, Universiti Kebangsaan
Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, Tel.: (603)-40405331; Fax: (603)-26983271; E-mail: ibj@medic.ukm.my
1388-0209/03/4105-392$16.00
© Swets & Zeitlinger
and subtropical regions (Holttum, 1950). There are at least
23 genera and about 200 species in Peninsular Malaysia
(Burkill, 1966). Many of the species such as Zingiber offic-
inale (ginger), Curcuma domestica (tumeric), Kaempferia
galanga (cekur) and Alpinia galanga (lengkuas) are used
widely as spices to flavour native dishes and processed foods.
In traditional medicines, the powdered forms or aqueous
extracts of the rhizomes of several species have been used
to treat various symptoms and diseases such as abdominal
distensions, coughing, vomiting, diarrhoea, fever, stom-
achache, toothaches, skin infections, asthma, rheumatism,
yellow fever, urinary tract infections, malaria and gonorrhoea
(Burkill, 1966; Grosvenor et al., 1995).
The biological properties of the extracts of several species
of Zingiberaceae have been investigated by many workers.
Some of the reported biological and pharmacological effects
were antiemetic (Sharma et al., 1997), anticancer (Limtrakul
et al., 1997), antiinflammation (Claeson et al., 1996),
hypolipidemic (Babu & Srinivasan, 1997), antioxidant
(Selvam et al., 1995), antibacterial (Pattnaik et al., 1997) and
antifungal (Apisariyakul et al., 1995). The effectiveness of
the extracts have been shown in many studies to be attributed
to the chemical constituents of the essential oils of the plants
(Pattnaik et al., 1997).
In this study, the essential oils of nine Zingiberaceae
species [Zingiber officinale Rosc., Z. cassumunar Roxb., Z.
zerumbet Smith, Curcuma aeruginosa Roxb., C. mangga
Valeton and van Zyp, C. xanthorrhiza Roxb., Kaempferia
galanga Linn., Alpinia galanga Swartz and Boesenbergia
pandurata (Roxb.) Schlecht] were investigated for their anti-
fungal activities against five dermatophytes (Trichophyton
mentagrophytes, T. rubrum, Microsporum canis, M. nanum
and Epidermophyton floccosum), three filamentous fungi
(Aspergillus niger, A. fumigatus and Mucor sp.) and five iso-
 Antifungal activity of Zingiberaceae species
lates of yeast-like fungi (Saccharomyces cerevisiae, Crypto-
coccus neoformans, Candida albicans, Ca. tropicalis and
Torulopsis glabrata). The chemical composition of the active
samples were investigated by GC and GC-MS.
Materials and methods
Plant material
Rhizomes of Zingiber officinale, Z. cassumunar, Z. zerum-
bet, Curcuma aeruginosa, C. mangga, C. xanthorhiza,
Kaempferia galanga, Alpinia galanga and Boesenbergia
pandurata were collected from a farm in Sabak Bernam,
Selangor, Malaysia. The voucher specimens were identified
and deposited at the Department of Botany, University of
Malaya. The fresh rhizomes were washed, comminuted and
150 g of each sample was hydrodistilled in Clevenger-type
apparatus for 8 h. The oily layers obtained were separated and
dried with anhydrous sodium sulfate. The yields were aver-
aged over two experiments and calculated based on the dry
weight of the plant materials.
Essential oil analysis
GC analysis was performed using a Shimadzu GC 14A cap-
illary chromatograph equipped with a FID detector using a
DB-5 (30 m ¥ 0.25 mm, 0.25 mm film thickness) capillary
column. The samples dissolved in hexane were injected in
split mode, using pressured controlled nitrogen as carrier gas
at a linear velocity of 50 cm/s. Injector and detector temper-
ature was maintained at 250 °C. The oven temperature was
programmed at 75 °C (10 min) to 230 °C at 3 °C/min. Peak
areas and retention times were measured by electronic inte-
gration. The relative amounts of individual components are
based on peak areas obtained, without FID response factor
correction. Temperature program linear retention indices of
the compounds were also determined relative to n-alkanes.
GC-MS analyses were carried out on a Hewlett Packard
GC-MSD 5890 series, EI electron impact ion source, 70 EV
using a BPX5 (30 m ¥ 0.25 mm, 0.25 mm film thickness) with
similar condition as described in GC programs. Identification
of the chemical components was based on the comparison
of their mass spectral data with the existing Wiley library,
comparison of calculated retention indices with literature
values and co-chromatography of the some constituents with
authentic components on the DB-5 capillary column.
Fungi used
The following fungi were obtained from the Institute for
Medical Research, Kuala Lumpur; five yeast strains
[Saccharomyces cerevisiae (ATCC 9783), Cryptococcus neo-
formans, Candida albicans, Ca. Tropicalis, Torulopsis
glabrata], five dermatophytes (Trichophyton mentagro-
phytes, T. rubrum, Microsporum canis, M. nanum and Epi-
dermophyton floccosum) and three filamentous fungi
393
(Aspergillus niger, A. fumigatus and Mucor sp.). The yeasts
strains and the filamentous fungi were maintained on
Sabouraud dextrose agar (SDA) plates at 30°C while the der-
matophytic fungi were maintained on brain heart infusion
agar (BHIA) slants at 37°C. The fungi were subcultured in
antibiotic medium 3 agar (M-3) (Difco, USA) and incubated
at 37°C overnight. Each fungal culture was diluted with
sterile 0.85% sodium chloride solution to produce a cell sus-
pension containing 1–5 ¥ 106 organisms per ml and obtained
a turbidity comparable to that of McFarland standard tube
No. 0.5. The inoculum size was determined spectrophoto-
metrically at 530 nm and further confirmed by using
Neubauer Counting Chamber (Pfeller et al., 1988).
Determination of antifungal activity
Broth microdilution method
Serial dilutions of the essential oil solutions were placed in
tubes labeled A to F. Tube A was filled with 100 ml of essen-
tial oil stock solution (200 mg ml-1, DMSO). Only 50 ml of
the stock solution in tube A was transferred to tube B and
diluted with 50 ml of DMSO. The procedure was repeated for
solutions in tubes B to F. Each tube was then filled with
100 ml fungi suspension and 100 ml of M-3 broth to obtain
serial dilution of the test materials (40, 20, 10, 5, 2.5, 1.25
and 0.63 mg ml-1) and the mixtures were stirred thoroughly
and incubated at 27–30 °C overnight. Amphotericin B
(200 mg ml-1) was used as a positive control and DMSO
served as a negative control. Turbidity was taken as an indi-
cation of growth and the lowest concentration which
remained clear after macroscopic evaluation was recorded as
the minimum inhibitory concentration (MIC). The MIC
value was recorded as the mean concentration of duplicates.
Disc agar diffusion technique
A series of 90 mm Petri dishes containing M-3 agar was each
inoculated with the different cultures of the yeast-like fungi
by swabbing aseptically on the whole surface of the agar with
cotton wool. A 6 mm diameter filter paper disc (Whatman
No. 3) was impregnated with 15 ml of the essential oil solu-
tion in absolute ethanol (50 mg ml-1). The disc was air-dried
and placed aseptically at the centre of the M-3 agar. The plate
was left undisturbed for 30 min to allow the oil to diffuse into
the agar. Disc soaked with absolute ethanol and air-dried
served as control. Petri dishes without the oil and the solvent
were prepared to assess the healthy growth of organisms.
Amphotericin (0.075 mg) in absolute ethanol impregnated
onto the disc and air-dried was used as positive control. The
dishes were incubated at 30°C for 48 h except for Cr. neo-
formans which was incubated for 72 h. The evaluation of
inhibitory properties was carried out in triplicate. The growth
inhibition which was indicated by areas of clear zone, was
measured by vernier calipers and taken as the mean of two
diameters at right angle to each other.
394 I. bin Jantan et al.

Results and discussion
Hydrodistillation of the rhizome oils of the Zingiberaceae
species gave the following yields: Zingiber officinale (1.4%),
Z. cassumunar (2.8%), Z. zerumbet (1.5%), Curcuma aerug-
inosa (0.8%), C. mangga (4.8%), C. xanthorhiza (6.7%),
Kaempferia galanga (5.5%), Alpinia galanga (0.8%) and
Boesenbergia pandurata (3.3%) (calculated on a dry weight
basis).
Results obtained from the controls indicated that the sol-
vents had no effect on the fungi after 48 and 72 h of incuba-
tion and that the organisms grew well during incubation.
Sterility conditions were also maintained throughout the
experiments. Amongst the essential oils studied, only the oil
of B. pandurata was effective against all the fungi. The oil
showed high selectivity against S. cerevisiae, exhibiting a rel-
atively high inhibition zone diameter (20.6 mm) (Table 1).
The oil was the most effective against the filamentous and
dermatophytic fungi by giving the lowest MIC values of
0.63 mg ml-1 with Mucor sp., 1.25 mg ml-1 with both A. niger
and A. fumigatus and 2.5 mg ml-1 with both T. rubrum and E.
floccosum (Table 2).
K. galanga was particularly active against A. fumigatus
with a MIC value of 1.2 mg ml-1, but was not effective
against all the strains of yeasts studied. On the contrary, the
efficacy of the oil of Z. officinale towards the various yeast-
like fungi was non-selective as the inhibition zones showed
little variation (11.7–14.0 mm) (Table 1). However, the oil did
not show any activity against the dermatophytic and fila-
mentous fungi (Table 2). The essential oil of Z. cassumunar
was active against three yeast-like fungi with inhibition zone
diameters ranging from 14.0 to 15.7 mm. However, it was not
effective against the other fungi. The essential oils of C.
aeruginosa, C. mangga, Z. zerumbet and A. galanga showed
little or no inhibition on the growth of all the fungi tested.
Among the fungi tested, T. mentagrophtes appeared to be
the most resistant, with three oils exhibiting MIC values
≥20 mg ml-1 (Table 2).

Table 1. Effect of the essential oils of Zingiberaceae species (0.75 mg/disc) on the growth of various yeast-like fungi.

Zone of inhibition (mm)

Fungi S. cerevisiae Cr. neoformans Ca. albicans Ca. aropicalis T. glabrata

Sample
Z. officinale 12.7 ± 1.1 14.0 ± 1.7 12.3 ± 2.5 12.7 ± 2.1 11.7 ± 2.9
Z. cassumunar 15.7 ± 2.0 14.0 ± 1.7 14.0 ± 1.7 – –
Z. zerumbet – – – – –
C. aeruginosa – – – – –
C. mangga – – – – –
C. xanthorrhiza – – – – –
B. pandurata 20.6 ± 2.5 9.0 ± 1.0 9.0 ± 2.5 11.0 ± 1.0 8.3 ± 0.6
A. galanga – – – – –
K. galanga – – – – –
amphotericin* 26.0 ± 1.7 20.0 ± 1.5 21.3 ± 2.5 21.7 ± 1.1 19.3 ± 1.5

– no activity
* 0.075 mg

Table 2. The minimum inhibitory concentrations (mg ml-1) of the essential oils Zingiberacea species.

Species T. mentagrophtes T. rubrum M. nanum M. canis E. floccosum Mucor sp. A. niger A. fumigatus

C. xanthorhiza 40.0 – 10.0 – 40.0 40.0 40.0 –

C. aeruginosa – – 40.0 – – – – –
C. mangga – – – – – – – –
Z. zerumbet – – – – – – – –
Z. cassimunar – – – – – – 40.0 –
Z. officinale – – – – – – – –
K. galanga 20.0 40.0 40.0 40.0 – – 40.0 0.63
A. galanga – – – – – – – –
B. pandurata 40.0 2.5 5.0 10.0 1.25 0.63 1.25 1.25

– no activity
 Antifungal activity of Zingiberaceae species 395

Table 3. Chemical constituents of the rhizome oils of Boesenbergia pandurata, Curcuma

cassumunar, Zingiber officinale and Kaempferia galanga.

Percentage

Sample Method of
Compound (1) (2) (3) (4) RI Identification

tricyclene 0.1 – 0.1 – 921 a,b

a-thujene 0.2 0.5 – tr 927 a,b
a-pinene 0.6 0.9 0.1 0.2 937 a,b,c
camphene 5.8 – 1.1 0.3 953 a,b,c
sabinene tr 0.3 – tr 970 a,b,c
b-pinene 0.1 20.8 0.2 0.5 979 a,b,c
myrcene 0.3 1.0 0.3 0.2 990 a,b,c
a-phellandrene 0.2 0.1 – 0.1 1003 a,b,c
d-3-carene 1.7 2.4 – 0.7 1009 a,b,c
a-terpinene – 1.7 – – 1015 a,b,c
p-cymene – 0.8 0.1 – 1026 a,b,c
limonene – – – 0.1 1029 a,b,c
b-phellandrene – 0.4 – – 1030 a,b,c
1,8-cineole 13.9 – 3.2 0.1 1033 a,b,c
(Z)-b–ocimene – – 0.2 – 1037 a,b,c
(E)-b–ocimene – – tr – 1050 a,b,c
g-terpinene 0.3 5.1 – 0.1 1055 a,b,c
cis-linalool oxide 0.1 0.6 0.1 – 1075 a,b
trans-linalool oxide – – 0.1 – 1088 a,b
terpinolene 2.0 0.9 0.2 0.1 1089 a,b,c
linalool 0.6 0.6 1.6 tr 1099 a,b,c
isopulegol – 0.6 – – 1138 a,b
camphor 32.1 0.1 0.3 – 1149 a,b,c
citronellal – 0.3 – – 1153 a,b,c
isoborneol 0.2 – – – 1153 a,b,c
borneol 0.9 – 2.6 1.2 1166 a,b,c
terpinen-4-ol 0.4 37.7 0.2 0.1 1178 a,b,c
a-terpineol 1.2 0.7 1.0 tr 1188 a,b,c
cis-piperitol – 0.3 – – 1196 a,b
decanal – 0.4 – – 1205 a,b,c
nerol – – 0.1 – 1230 a,b,c
neral 1.0 – 5.8 – 1247 a,b,c
geraniol 16.2 – tr – 1262 a,b,c
geranial 3.7 – 20.1 – 1273 a,b,c
methyl 3-phenylpropionate 0.4 – – – 1278 a
geranyl formate 1.5 – – – 1298 a,b
d-elemene 0.6 0.2 1.2 – 1335 a,b
a-cubebene – – – 0.2 1350 a,b
neryl acetate 1.0 – – – 1365 a,b
methyl cinnamate 5.8 – – – 1378 a,b
geranyl acetate – – 18.1 – 1381 a,b
b-elemene – tr – 0.1 1388 a,b
b-caryophyllene – 0.3 0.4 0.1 1415 a,b,c
g-elemene 0.5 0.3 – – 1433 a,b
geranyl propionate 0.2 – – – 1444 a,b
(E)-ethyl cinnamate – – – 24.3 1452 a,b
(Z)-b-farnesene 0.2 – – – 1451 a,b
a-humulene – 0.1 – – 1453 a,b
ar-curcumene – – 6.6 – 1482 a,b
a-zingiberene – 0.3 1.5 – 1494 a,b
pentadecane – – – 1.7 1500 a,b,c
b-bisabolene – 0.8 1.0 – 1505 a,b
(E)-a-farnesene 0.1 – – – 1511 a,b
396 I. bin Jantan et al.

Table 3. Continued

Percentage

Sample Method of
Compound (1) (2) (3) (4) RI Identification

myristicin 0.2 – – – 1516 a,b

b-sesquiphellandrene – 0.2 0.8 – 1520 a,b
(Z)-nerolidol 0.1 0.2 0.2 – 1534 a,b,c
elemol – – 0.3 – 1548 a,b
b-thujaplicin 0.1 – – – 1559 a
(E)-nerolidol – 1.0 0.5 0.1 1560 a,b
(E)-1-(3,4-dimethoxy – 13.3 – – 1616 a
phenyl)but-1-ene
b-eudesmol – – 0.2 – 1654 a,b
(E)-1-(3,4-dimethoxy – 4.7 – – 1710 a
phenyl)butadiene
(Z,Z)-farnesol – – 0.1 – 1713 a,b
(E,E)-farnesol – – 0.1 – 1722 a,b
zerumbone – 0.4 – – 1733 a,b
ethyl p-methoxy cinnamate – – – 66.9 1760 a,b
methyl m-methoxy – 1.1 – – 1786 a,b
carbonylcinnamate

Percentages were calculated on the basis of results obtained on column DB 5; RI = retention

index; t a = mass fragmentation; b = retention index; c = co-chromatography with authentic
sample; 1 = B. pandurata; 2 = C. cassumunar; 3 = Z. officinale; 4 = K. galanga.

The influence of nature and proportion of individual con-
stituents of an essential oil and their synergistic effects on
the antimicrobial activity of the oil have been reported by
Pattnaik and co-workers (1997). The inhibitory activity may
be due to the different modes of action of the total compo-
nents of the oils towards the fungi. The relative antifungal
activity of the essential oils could not be easily correlated
with any individual component. A recent study suggested
that the antifungal activities of cinnamon and tyme oils were
probably due to their respective major components, cin-
namaldehyde (66.0%), and carvacrol (24.2%), respectively
(Ferhout et al., 1999). The chemical composition of the active
essential oils, viz., B. pandurata, Z. offinale, Z. cassumunar
and K. galanga was investigated in an effort to correlate the
constituents of the oils and their antifungal activities. The list
of constituents identified in the oils is shown in order of
elution on a DB-5 type column in Table 3. The chemical com-
position of the other oils have been reported elsewhere
(Jantan et al., 1999; in press).
The essential oil of B. pandurata contained high levels
of camphor (32.1%), geraniol (16.2%), 1,8-cineole (13.9%),
methyl cinnamate (5.8%) and camphene (5.8%). Previous
work on antimicrobial activities of several essential oil com-
ponents indicated that cineole, citral, geraniol, linalool and
menthol were active against several yeast-like and filamen-
tous fungi (Pattnaik et al., 1997). Essential oils containing
high levels of camphor exhibited strong antifungal activity
against T. mentagrophytes, A. flavus, A. fumugatus, Candida
albicans and other pathogenic fungi (Alvarez-Castellanos
et al., 2001; Hammerschmidt et al., 1993; Tirillini, 1996).
Based on these studies, it may be that the antifungal activity
of B. pandurata was contributed mainly by camphor, geran-
iol and 1,8-cineole.
The rhizome oil of C. cassumunar was rich in terpinen-
4-ol (37.7%), b-pinene (20.8%), (E)-1-(3,4-
dimethoxyphenyl)but-1-ene (13.3%), g-terpinene (5.1%) and
(E)-1-(3,4-dimethoxyphenyl)butadiene (4.7%). The presence
of a high concentration of terpinen-4-ol in this oil could
explain its moderate activity against the yeasts as a recent
study on the antifungal assay of standard sample of terpinen-
4-ol showed that the compound exhibited moderate to strong
activities against several fungi (Mastura et al., 1999). The
major components in the oil of Z. officinale were geranial
(20.1%), geranyl acetate (18.1%), ar-curcumene (6.6%) and
neral (5.8%). The antifungal activity of this oil could be
due to the presence of high levels of citral. The ethyl esters
of cinnamate (24.3%) as well as of p-methoxycinnamate
(66.9%) were the major constituents in the rhizome oil of
K. galanga. These compounds are believed to be the active
components in the oil as previous study indicated that both
compounds were active against C. albicans (Ibrahim &
Sadikun, 1990).
Acknowledgements
The authors are grateful to the Institute for Medical
Research, Malaysia for providing the fungi used in this study.
 Antifungal activity of Zingiberaceae species
The work was supported by Universiti Kebangsaan Malaysia
(UKM grant NTGF/11/2000).
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