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Original article http://dx.doi.org/10.1016/j.apjtb.2017.09.009
Chemical profiling and antimicrobial activity of essential oil from Curcuma aeruginosa
Roxb., Curcuma glans K. Larsen & J. Mood and Curcuma cf. xanthorrhiza Roxb.
collected in Thailand
Nararat Akarchariya, Sasithorn Sirilun, Jakaphun Julsrigival, Sunee Chansakaowa
*
Department of Pharmaceutical Sciences, Faculty of Pharmacy, Chiang Mai University, Chiang Mai 50200, Thailand
ARTICLE INFO
Article history:
Received 30 Jun 2017
Received in revised form 3 Aug 2017
Accepted 8 Sep 2017
Available online 20 Sep 2017
Keywords:
Curcuma aeruginosa Roxb.
Curcuma glans K. Larsen & J. Mood
Curcuma cf. xanthorrhiza Roxb.
Essential oil
Antimicrobial activity
ABSTRACT
Objective: To investigate chemical constituents and new antimicrobial agents among
essential oils from the rhizomes of Curcuma aeruginosa (C. aeruginosa) Roxb., Curcuma
glans K. Larsen & J. Mood and Curcuma cf. xanthorrhiza Roxb.
Methods: The essential oils were obtained by hydro-distillation and analyzed by gas
chromatography/mass spectroscopy. Agar-well diffusion assay was used to study the anti-
microbial activity and also broth-micro dilution techniques were examined for minimum
inhibitory concentration (MIC) against four bacterial strains and yeast.
Results: The gas chromatography/mass spectroscopy analysis showed monoterpenes
predominantly (88.53%) in the rhizome oil of Curcuma cf. xanthorrhiza. Sesquiterpenes
(50.10%) was the most abundant component in the essential oil of C. glans, while
monoterpenes (45.55%) and sesquiterpenes (45.81%) were found in C. aeruginosa with a
significant amount. The major components of C. aeruginosa were characterized as
camphor (29.39%) and germacrone (21.21%). Germacrone (15.76%),
b
-pinene (9.97%)
and camphor (9.96%) were found as major compounds in the rhizome oils of C. glans
while
a
-terpinolene (24.86%) and p-cymen-7-ol (12.17%) were found as major compo-
sitions in Curcuma cf. xanthorrhiza. The essential oils were tested against four bacterial
strains and yeast. As a result, the rhizome oil of C. aeruginosa exhibited potent activity
against Staphylococcus aureus [inhibition zone (21.94 ± 0.24) mm, MIC 125
m
g/mL],
Bacillus cereus [inhibition zone (20.83 ± 0.36) mm, MIC 125
m
g/mL], and Candida
albicans [inhibition zone (11.60 ± 0.30) mm, MIC 250
m
g/mL].
Conclusions: The essential oils from three Curcuma species possessed greater activity
against the gram-positive bacteria (Staphylococcus aureus and Bacillus cereus) than
gram-negative bacteria (Escherichia coli and Pseudomonas aeruginosa). The results
suggest that the essential oils from the fresh rhizome of Curcuma spp. might be a po-
tential source of natural antimicrobial substances.
1. Introduction
The members in Zingiberaceae have been recognized in
widely uses of food, medicine, and traditional knowledge
[1]
.
Curcuma is a perennial rhizomatous herb, which is one of the
largest genera in the Zingiberaceae family, with about eighty
species distributed mostly in Southeast Asia, Papua New
Guinea and Northern Australia
[1,2]
. Among them, 43 species
are normally found in Thailand
[1–3]
. Most species in
Curcuma are usually aromatic in at least one part. In Thailand,
various kinds of Curcuma are well known for their medicinal
values or as ornamental plants, especially Turmeric [Curcuma
longa (C. longa) L.] and Siam Tulip (Curcuma alismatifolia
Gagnep.)
[1–6]
. Previous reports of phytochemical studies and
bioactivities of Curcuma species presented several
monoterpenoids in essential oils, diarylheptanoids of which
curcuminoids are the significant bioactive compounds in some
species and phenolics in extracts. The utilization of the
*Corresponding author: Sunee Chansakaow, Department of Pharmaceutical
Sciences, Faculty of Pharmacy, Chiang Mai University, Chiang Mai 50200, Thailand.
Tel: +66 5394 4399
Fax: +66 5394 4390
E-mails: chsunee@gmail.com,sunee.c@cmu.ac.th (S. Chansakaowa).
Peer review under responsibility of Hainan Medical University. The journal
implements double-blind peer review practiced by specially invited international
editorial board members.
Contents lists available at ScienceDirect
Asian Pacific Journal of Tropical Biomedicine
journal homepage: www.elsevier.com/locate/apjtb
Asian Pac J Trop Biomed 2017; 7(10): 881–885 881
2221-1691/Copyright © 2017 Hainan Medical University. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://
creativecom mons.org/li censes/by-nc -nd/4.0/).
Zingiberaceous plants can be attributed to biological activities
which are antimicrobial, antioxidant, antityrosinase activities,
and anti-inflammatory effect of some species which were re-
ported in the previously published data
[7–9]
. The antimicrobial
properties of essential oils and plant extracts have been
recognized for many years. The members of the family
Zingiberaceae were also reported as natural antimicrobial
agents, especially their essential oils
[10–14]
. From folk
wisdom, many of Curcuma species usually known as a
medicine were used to alleviate antidiarrhea, infectious wound
or abscess
[14]
. Three species, Curcuma aeruginosa
(C. aeruginosa) Roxb., Curcuma glans (C. glans) K. Larsen
& J. Mood and Curcuma cf. xanthorrhiza (C. cf.
xanthorrhiza) Roxb., were found in Thailand especially in the
North with the history of their utilization which followed the
indigenous wisdom. C. aeruginosa is known as Kamindam in
Thailand
[3]
. The ethnomedical uses of this plant included a
treatment of flatulence, dyspepsia, diarrhea and parasitic
infection
[5,6]
. Traditionally, the rhizome of C. glans has been
used medicinally to treat a sore throat, tonsillitis, wound or
abscess in mouth, throat, and nose and herpes simplex virus
[5]
.C. cf. xanthorrhiza, Wan-Salika-Linthong in Thai, is
known as a kind of sacred plant. In the northern part of Thailand
have been used the fresh rhizome or dried powder for skin
disease
[6]
. The practical uses of some species especially
C. glans are based on the knowledge and experiences of the
ancestor without sufficient scientific support. The present
study is focused on the study of chemical constituents and to
investigate the antimicrobial activities of three species of
Curcuma compared with the well-known species C. longa.
2. Material and methods
2.1. Plant materials
Rhizomes of C. aeruginosa (voucher number WP.5811),
C. glans (WP.5810) and C. cf. xanthorrhiza (WP.5818) were
collected from an herbal market at Chiang Dao district, Chiang
Mai Province, Thailand. The plants were identified by taxono-
mists and voucher specimens have been deposited at the Queen
Sirikit Botanic Garden Herbarium and Faculty of Science,
Chiang Mai University, Thailand.
2.2. Extraction of essential oil
The fresh rhizome of each sample (3 000 g) was cleaned with
tap water, reduced their size and then subjected to hydro-
distillation for 5 h using a cleavenger-type apparatus. The
essential oils were dried over anhydrous sodium sulfate and
stored in air-tight containers at 4
C before analyzed and tested.
2.3. Gas chromatography/mass spectroscopy analysis
A Shimadzu GCMS-QP 2010 Plus system was used, with a
mass-selective detector with electron impact ionization. The
samples were separated using a DB-5 MS capillary column (5%
phenylmethylpolysiloxane, 30 m × 0.25 mm, 0.25
m
mfilm
thickness) with helium as the carrier gas (0.99 mL/min). The
temperature program used for analysis was as follows: the initial
temperature was 70
C and programmed to 150
C with the rate
of 5
C/min held for 5 min, and then ramped to 230
C with the
rate of 3
C/min and kept constant for 3 min. The split flow ratio
was 1:100. The injection temperature was 150
C and the gas
chromatography/mass spectroscopy interface temperature was
set at 250
C.
2.4. Identification of components
The identification of volatile components was based on
computer matching with WILLEY 7 and NIST 2005 Library, as
well as by comparison of the mass spectra and Kovats retention
indices with a series of n-alkanes (C
8
–C
20
).
2.5. Antimicrobial assay
2.5.1. Microbial culture
The following bacterial species were used: gram-positive
bacteria [Staphylococcus aureus (S. aureus) (ATCC 25923)
and Bacillus cereus (B. cereus) (ATCC 11778)], gram-negative
bacteria [Escherichia coli (E. coli) (ATCC 25922) and Pseu-
domonas aeruginosa (P. aeruginosa) (ATCC 27853)] and yeast
[Candida albicans (C. albicans) (ATCC 90028)].
The antimicrobial assays were carried out by the agar disc-
diffusion method and the microdilution method modified by
Lorian in 1991, Sirilun in 2005 and Sirilun et al.
[15–17]
. These
assays were used to determine the antimicrobial activity of the
essential oils against human pathogenic bacteria and yeast.
2.5.2. Disc diffusion method
Essential oil samples were aseptically prepared by steriled
membrane filtration (Pall Gelman, 0.45 and 0.22
m
m millipore).
Bacteria and yeast were cultured in tryptic soy broth and sabo-
uraud dextrose broth, respectively. The density of microbial test
cultures was standardized using McFarland 0.5 turbidity stan-
dard at 1.0 × 10
8
CFU/mL of bacteria and 1.0 × 10
6
CFU/mL of
yeast. The culture tests were swabbed and spread on the culture
plate of Mueller-Hinton agar and Sabouraud dextrose agar for
bacteria and yeast, respectively and allowed to dry for 15 min.
The discs were loaded with 10.0
m
L essential oils and placed on
the medium surface. The positive controls were gentamicin
(10
m
g/disc) and cyclopiroxolamine (10
m
g/disc) against bacte-
rial and yeast growth, respectively. The negative control was
dimethyl sulfoxide (DMSO) (10
m
L/disc). After (24–48) h of
incubation at (35–37)
C, the diameters of the growth inhibition
zones were measured for each test in triplicate.
2.5.3. Minimum inhibitory concentration (MIC) determi-
nation
MIC was analyzed using broth microdilution assay in
Mueller-Hinton Broth and Roswell Park Memorial Institute
1640 (RPMI-1640) for bacteria and yeast test, respectively,
described by Das et al.
[18]
with modification. The stock
solutions of essential oil were prepared in DMSO (1.00 mg/
mL), filtrated by using the sterile membrane (0.22
m
m) and
subsequent two-fold serial dilution as final concentration at
(0.49–1 000.00)
m
g/mL in reaction mixture well. The microbial
strains were grown and the density of cultures was standardized
using McFarland 0.5 turbidity standard at 1.0 × 10
8
CFU/mL of
bacteria and 1.0 × 10
6
CFU/mL of yeast. The positive control
was gentamicin with stock concentration at 10 mg/mL and
cyclopiroxolamine with stock concentration at 10 mg/mL to
against bacterial and yeast growth, respectively. The negative
Nararat Akarchariya et al./Asian Pac J Trop Biomed 2017; 7(10): 881–885882
control was DMSO. After (24–48) h of incubation at (35–37)
C,
the turbidity of the microbial growth was determined for each test
in triplicate.
2.6. Statistical analysis
All experiments were conducted repeatedly in triplicate
(n= 3). Analysis of one-way-ANOVA were performed
(P<0.05) for each microbial species and overall activity of each
sample (agar disc-diffusion assay). The differences among
means were determined by Duncan's test (P<0.05).
3. Results
The percentage oil yields of C. aeruginosa,C. glans and C.
cf. xanthorrhiza were 0.35%, 0.32% and 0.29% v/w, respec-
tively. The GC–MS analysis of the identified constituents is
revealed in Table 1.
The rhizome oils showed monoterpenes and sesquiterpenes
as major components with a different of their chemical profiles.
The major components of C. aeruginosa were characterized as
camphor (29.39%) and germacrone (21.21%). The most abun-
dant compositions in the rhizome oils of C. glans were germa-
crone (15.76%), followed by
b
-pinene (9.97%) and camphor
(9.96%).
C. aeruginosa,C. glans,C. cf. xanthorrhiza, were a broad
inhibitory spectrum, against the growth of bacteria both of gram-
negative and gram-positive and yeast. The activity of the
essential oil was determined by comparison with positive
control, gentamicin (bacterial tests) and cyclopiroxolamine
(yeast test), and DMSO as a negative control. The activity of
DMSO with low concentration was not detected against the
growth of microbial tests (data was not shown). The MIC evi-
denced that the rhizome oil of C. aeruginosa,C. glans, and C.
cf. xanthorhiza exhibited promising antibacterial activity
against S. aureus,B. cereus,E. coli and P. aeruginosa with MIC
values of (125–1 000)
m
g/mL and antifungal activity against
C. albicans with MIC values of (250–500)
m
g/mL. The rhizome
oil of C. aeruginosa,C. glans,C. cf. xanthorhiza and C. longa
showed weak activity against the gram-negative bacteria E. coli
(MIC 1 000
m
g/mL). However, the C. aeruginosa showed strong
activity in comparison to positive control against the growth of
S. aureus,B. cereus,P. aeruginosa and C. albicans.Itis
interesting that the rhizome oil of C. aeruginosa,C. glans, and
C. cf. xanthorrhiza showed activity against the growth of
S. aureus and C. albicans.Candida species are the leading
causes of nosocomial bloodstream infection and has become a
major health problem as an opportunistic infection such as oral
candidiasis (Fareid, 2014)
[19]
. The results indicate that the
rhizome oils are potential oils with an ability to control
opportunistic fungal C. albicans (Table 2). These results can
be ascribed to them containing oxygenated monoterpenes, 1,8-
cineole (2.68%–4.87%) and camphor (2.49%–29.39%) in a great
proportion. Some oxygenated monoterpenes especially 1,8-
cineole were previously observed to be the potential compounds
for high antibacterial properties
[20]
. Additionally, germacrone
was found as an important constituent in C. aeruginosa and
C. glans. Germacrone possessed potent bacterial activity
Table 1
Chemical composition (%) of the essential oils from C. aeruginosa (CA), C. glans (CG) and C. cf. xanthorrhiza (CX).
Retention time KI
a
KI
b
Identified compound CA CG CX Chemical group
3.458 905 904 2-Heptyl alcohol 0.15 5.04 –Alcohol
3.960 940 940
a
-Pinene 0.18 1.52 2.46 Monoterpenes
4.240 958 955 Camphene 1.17 1.38 3.19 Monoterpenes
4.702 985 983
b
-Pinene 0.35 9.97 6.78 Monoterpenes
4.816 992 992
b
-Myrcene ––1.50 Monoterpenes
5.069 1007 1009 2-Octanol –0.39 0.39 Alcohol
5.190 1015 1013 a-Phellandrene ––0.78 Monoterpenes
5.549 1037 1034 p-Cymene ––8.09 Monoterpenes
5.627 1042 1040 Limonene 0.35 0.50 1.90 Monoterpenes
5.683 1046 1034
b
-Phellandrene ––0.32 Monoterpenes
5.736 1049 1048 1,8-Cineole 2.68 4.33 4.87 Monoterpenes
6.218 1076 1069
g
-Terpinene ––0.40 Monoterpenes
6.819 1042 1079
a
-Terpinolene ––24.86 Monoterpenes
7.156 1118 1108 2-Nonanol 0.43 6.89 –Alcohol
8.320 1139 1141 Camphor 29.39 9.96 2.49 Monoterpenes
8.692 1161 1159 Borneol 7.27 3.06 0.48 Monoterpenes
8.897 1173 1172 endo-Borneol 2.86 2.16 0.69 Monoterpenes
8.989 1179 1179 Isopinocamphone –0.12 0.44 Monoterpenes
9.068 1183 1182 Terpinen-4-ol 0.37 0.22 0.59 Monoterpenes
9.237 1192 1189 p-Cymen-7-ol ––12.17 Monoterpenes
13.985 1392 1392
b
-Elemene 1.35 2.32 –Sesquiterpenes
14.704 1424 1424 trans-Caryophyllene 0.11 0.23 0.32 Sesquiterpenes
15.536 1461 1460 a-Humulene 0.58 –0.60 Sesquiterpenes
16.429 1498 1480 Curzerene 4.84 1.00 –Sesquiterpenes
16.718 1511 1504 Germacrene A 0.76 0.49 –Sesquiterpenes
17.933 1564 1561 Germacrene B 5.20 0.43 –Sesquiterpenes
19.770 1600 –Isocurcumenol –2.43 –Sesquiterpenes
20.031 1610 1617 (+) Spathulenol –0.92 –Sesquiterpenes
21.530 1662 1666 Isospathulenol –0.18 –Sesquiterpenes
22.473 1693 1693 Germacrone 21.21 15.76 0.74 Sesquiterpenes
a: Kovat retention index investigated relative to C8–C20 n-alkanes on DB-5 MS column; b: Kovat retention index from literature data (NIST Chemical
Web Book).
Nararat Akarchariya et al./Asian Pac J Trop Biomed 2017; 7(10): 881–885 883
against gram-negative bacteria, P. aeruginosa (MIC 15.6 mg/
mL; MBC 31.2 mg/mL)
[21]
.
4. Discussion
The monoterpenes,
a
-pinene,
b
-pinene, sesquiterpenes and
germacrone, are most often found in the rhizome oil of Zingi-
beraceous plants collected from Ban Thum, Chiang Dao district,
Chiang Mai Province
[6]
. There are several reports in the
chemical composition of the essential oil from the rhizome of
Curcuma species
[6–8,14,20,22]
, but none for C. glans. Chemical
analysis of the essential oils from rhizomes of the
aforementioned Curcuma species collected in Thailand and
their antimicrobial activities compared to the worldwide-
cultivated species, C. longa, were mentioned in this present
study. Monoterpene and sesquiterpene hydrocarbons represented
the most common chemical groups found in the essential oils
from the rhizomes of the investigated Curcuma species
[6]
:
C. aeruginosa (45.55%, 45.81%, respectively); C. glans
(34.79%, 50.10%); and C. cf. xanthorrhiza (88.53%, 2.72%).
Germacrone and camphor were found in the greatest amount in
C. aeruginosa and C. glans while C. cf. xanthorrhiza found
a
-
terpinolene and p-cymen-7-ol as major components. It has been
reported that terpenes have antibacterial activity because of
their bacteriostatic and bactericidal effects
[23]
. Many aromatic
herbs (i.e. lemongrass, basil, and cinnamon, etc.)
[23–25]
including species of Curcuma
[13,20–22,26]
are comply with this
basis.
This study is the first report of chemical compositions in the
rhizome oil of C. glans.
a
-terpinolene (24.86%) and p-cymen-7-
ol (12.17%) were found as major compositions in C. cf. xan-
thorrhiza. Previously reported by Helen et al.
[27]
, xanthorrhizol
was found in the rhizome oil of Curcuma xanthorrhiza (64.38%)
as major compounds, followed by camphene (8.27%), curcumin
(5.85%), and
a
-pinene (1.93%). Curcumene (41.40%) and
xanthorrhizol (21.50%) were the major compositions in the
rhizome oil collected in Netherlands
[28]
. Jarikasem et al.
[20]
reported that 1,8-cineol (37.58%) and curzerenone (13.70%)
were the highest proportions found in the rhizome oil
collected in Thailand. The chemical profile of this present
study revealed more similarity with Jarikasem et al.
[20]
than
the samples collected in India and Netherlands
[23,27]
.
Although the samples were collected in Thailand in the
previous report
[20]
, the quantity of chemical compositions
showed differences with this present study might be affected
by geography, harvesting period or variety. Three major
compounds, germacrone (23.49%), curzerenone (11.78%) and
1, 8-cineol (10.92%), were previously reported by Theanphong
et al.
[22]
. Ethoxybenzene, santolinatriene, benzofuran, 6-
ethenyl-4,5,6,7-tetrahydro-3,6-dimethyl-5-isopropenyl-, trans-
were reported as major components by George
[28]
in the
rhizome oil of C. aeruginosa from India. Sirat et al.
[28]
reported curzerenone and 1, 8-cineol as the principal
compositions but has a low amount of germacrone. The
present study showed differences in the quantity of chemical
components found in the rhizome oil from those previous
reports
[28–30]
as geography, climate, harvesting period may
affect the chemical profile.
The antimicrobial activity could be ascribed to them con-
taining monoterpenes and sesquiterpenes as major components,
especially oxygenated monoterpenes, camphor, 1,8-cineole
sesquiterpenes and germacrone, which were previously observed
to be the potential compounds for high antibacterial properties
[21,25]
.
The essential oils from Curcuma species possessed greater
activity against the gram-positive bacteria (S. aureus and
B. cereus) than gram-negative bacteria (E. coli and
P. aeruginosa). Interestingly, the rhizome oil of C. aeruginosa,
C. glans, and C. cf. xanthorrhiza showed activity against the
growth of C. albicans with an ability to control opportunistic
fungal C. albicans. The results indicated that the essential oils of
Curcuma species are able to have a potential for further appli-
cation for the treatment of infectious diseases and as alternative
natural products to substitute synthetic antimicrobial agents.
Conflict of interest statement
We declare that we have no conflict of interest.
Acknowledgments
This work was supported by the grants from the Biodiversity-
Based Economy Development Office Public Organization -Na-
tional Research Council of Thailand (Grant number.
R000012298), Department of Pharmaceutical Sciences, the
Faculty of Pharmacy and the Graduate School, Chiang Mai
University, Chiang Mai, Thailand. Queen Sirikit Botanic Gar-
den, Chiang Mai, Thailand for providing plants samples and
plant identification.
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