Composition and Antibacterial Activity of Essential Oils from Leaves of Etlingera species...

INTERNATIONAL JOURNAL FOR THE ADVANCEMENT OF SCIENCE & ARTS, VOL. 1, NO. 2, 2010 1

Composition and Antibacterial Activity

of Essential Oils from Leaves of Etlingera

species (Zingiberaceae)

1Eric Chan Wei Chiang,

2Lim Yau Yan and

3Nor Azah Mohd. Ali

1Faculty of Applied Sciences, UCSI University, Cheras, Kuala Lumpur, Malaysia

2School of Science, Monash University Sunway Campus, Petaling Jaya, Selangor, Malaysia 3Medicinal Plants Division, Forest Research Institute Malaysia, Kepong, Selangor, Malaysia

[email protected]

___________________________________________________________________________

Abstract

The composition of essential oils from leaves of four Etlingera species in Peninsular

Malaysia were analysed using GC and GC-MS. Antibacterial activity was screened using the

wet disc diffusion method and expressed as minimum inhibitory concentration (MIC). Oil

from leaves of Etlingera rubrostriata was the most diverse with 23 compounds identified.

Oils of Etlingera elatior and Etlingera fulgens were different in composition despite having

similar aroma. Leaves of Etlingera maingayi had the highest yield of oil (1317 mg/100 g) comprising mainly dodecanoic acid (44.6%) and decanoic acid (42.6%). Oils of all four

species inhibited Gram-positive bacteria with no activity against Gram-negative bacteria. Oil

of E. maingayi had the strongest activity with MIC of 6.3 mg/ml against Bacillus cereus and

Micrococcus luteus, and 12.5 mg/ml against Staphylococcus aureus. Based on MIC, ranking

was of the order: E. maingayi > E. rubrostriata > E. elatior > E. fulgens. Variability in

antibacterial activity of the leaf oils can be attributed to qualitative and quantitative

differences in the constituents of individual oils.

Keywords: Etlingera, essential oils, antibacterial activity

___________________________________________________________________________

1. INTRODUCTION

Etlingera of the tribe Alpinieae and family Zingiberaceae are tall forest plants reaching 8 m in height and often dominate gaps in disturbed forests [1,2]. Inflorescences are borne on

stalks protruding from the ground (Phaeomeria group) or are found at the soil level (Achasma

group) [3,4]. The varying shades of pink and red colours of bracts and flowers make them

very attractive plants. In Peninsular Malaysia, 15 Etlingera species have been recorded [4].

Plants of Etlingera have various traditional and commercial uses as food, condiment,

medicine and ornamentals [2]. In Sabah, Malaysia, the hearts of young shoots, flower buds

and fruits of Etlingera elatior and Etlingera littoralis are consumed by indigenous

communities as condiment, eaten raw or cooked [5]. In Thailand, fruits and cores of young

stems of E. littoralis are edible, and flowers of Etlingera maingayi are eaten as vegetables [6].

Inflorescences of E. elatior are widely cultivated throughout the tropics as spices for food

flavouring and as ornamentals [7]. Fruits of E. elatior are used traditionally to treat earache,


while leaves are applied for cleaning wounds [8]. Leaves of E. elatior, mixed with other

aromatic herbs, are used by post-partum women for bathing to remove body odour. There are

no reports on the use of rhizomes of Etlingera species.

Most studies on antioxidant properties (AOP) of ginger species are confined to rhizomes.

Although leaves of ginger species have been used for food flavouring and as traditional medicine, hardly any research has been carried out on their AOP and other bioactivities. In

our previous studies, total phenolic content (TPC) and ascorbic acid equivalent antioxidant capacity (AEAC) of leaves and rhizomes of 26 ginger species belonging to nine genera were

screened [9]. Results showed that leaves of Etlingera had the highest values. In E. elatior and E. maingayi, AOP values of leaves were seven to eight times higher than those of rhizomes.

Subsequently, leaves of five Etlingera species were assessed for TPC, AOP, antibacterial

activity and tyrosinase inhibition [10,11]. Highest TPC, AEAC and ferric reducing power

(FRP) were found in leaves of E. elatior followed by Etlingera rubrostriata. Leaves of E.

maingayi, with the lowest TPC, AEAC and FRP, had the highest ferrous ion chelating (FIC)

ability and lipid peroxidation inhibition (LPI) activity. FIC ability of Etlingera fulgens and E.

maingayi was much higher than that of young tea leaves (Camellia sinensis). All Etlingera

species studied showed high LPI activity superior to that of young leaves of C. sinensis.

Ranking of TPC and AOP of the different plant parts of E. elatior was in the order: leaves >

inflorescences > rhizomes. Leaves of highland populations of Etlingera species displayed

higher TPC and AEAC values than lowland counterparts. Leaves of Etlingera species

exhibited antibacterial activity against Gram-positive bacteria and displayed strong tyrosinase

inhibition. Based on bioactivities studied, the overall score and ranking were of the order: E.

elatior > E. rubrostriata > E. fulgens > E. littoralis > E. maingayi.

The phytochemistry of E. elatior has received some attention. Flavonoids of kaempferol 3-

glucuronide, quercetin 3-glucuronide, quercetin 3-glucoside and quercetin 3-rhamnoside have been reported in leaves [12]. Two new and six known compounds of diarylheptanoids,

labdane diterpenoids and steroids have been isolated from rhizomes [13]. Six phenolic compounds isolated from leaves were 3-O-caffeoylquinic acid, 5-O-caffeoylquinic acid

(chlorogenic acid), 5-O-caffeoylquinic acid methyl ester, isoquercitrin, quercitrin and (+)-

catechin [14,15]. Chlorogenic acid in leaves of E. elatior was significantly higher in content

than flowers of Lonicera japonica, the commercial source.

Essential oils of commercial ginger species such as Alpinia galanga, Curcuma longa and

Zingiber officinale are well-studied. More recently, oils from wild ginger species have also

been analysed. They include Alpinia conchigera [16], Alpinia malaccensis [17], Alpinia

smithiae [18], Alpinia zerumbet [19], Elettariopsis elan [20], Elettariopsis slahmong [21] and

Scaphochlamys kunstleri [22].

In terms of bioactivities, the antifungal activity of rhizome oils of nine ginger species against

five dermatophytes, three filamentous fungi and five strains of yeast has been assessed [23].

Oil of Boesenbergia rotunda was effective against all the fungi. Oil of Kaempferia galanga

showed selective toxicity against Aspergillus fumigatus while oils of Z. officinale and

Zingiber montanum exhibited high activity against the yeasts. Rhizome oils of seven ginger species were investigated for their larvicidal activity against Aedes aegypti [24]. Ranking of

larvicidal activity of oils was in the order: C. longa > Curcuma zanthorrhiza > Zingiber

zerumbet > Curcuma aeruginosa > B. rotunda > Z. officinale > Z. montanum. The

antibacterial activity of rhizome oils of five ginger species against Escherichia coli,


Staphylococcus aureus, Bacillus cereus and Listeria monocytogenes has been reported [25].

Rhizome oils of B. rotunda and Amomum xanthioides inhibited the growth of all tested

bacteria. Oils of Z. officinale, A. galanga and C. longa had no effect on E. coli. In terms of

efficiency, Z. officinale was most effective against S. aureus, B. cereus and L. monocytogenes.

In this study, the composition of essential oils from leaves of four Etlingera species were analysed and their antibacterial activity evaluated. The relationship between the components

and their antibacterial activity was discussed.

2. MATERIAL AND METHODS

2.1 Plant Species

Four species of Etlingera studied were E. elatior, E. fulgens and E. maingayi of the

Phaeomeria group, and E. rubrostriata of the Achasma group (Figure 1). Leaves were

collected from Janda Baik in Pahang, Peninsular Malaysia. Their identification in the field

was based on documented taxonomic descriptions and photographic illustrations [1,3,4].

Characteristic pleasant sour scent of leaves when crushed was another useful cue for species

identification. The identity of the four species was verified by botanists of the Forest

Research Institute Malaysia (FRIM) and voucher specimens were deposited in the herbarium

of institute as EC03, EC04, EC06 and EC07, respectively.

E. elatior E. fulgens

E. maingayi E. rubrostriata

Figure 1: Species of Etlingera studied


2.2 Extraction of Oils

Leaves of each species were sorted, cleaned and their mid-ribs removed. After cutting them

into small pieces, 500 g were immersed in 1 L of deionised water and hydro-distilled for 16 h in a 5 L flask attached to an Allihn condenser with continuous cooling with ice cold water.

Essential oils extracted were collected with a modified Clavenger apparatus.

2.3 Analysis of Oils

Oils were analysed using GC and GC-MS. GC analysis, used to quantify essential oils, was carried out using a Shimadzu GC-2010 gas chromatograph equipped with a flame ionization

detector (FID) using fused silica capillary column CBP-5 (25 x 0.25 mm; 0.25 µm film

thickness). Helium was used as the carrier gas, and the injector and detector temperature were

set up at 220o and 280

oC, respectively. The oven temperature was programmed from 60

o to

230oC at 3

oC/min and finally held at 230

oC for 10 min whilst the volume injected was 1.0 µl.

The peak areas and retention times were measured by electronic integration. GC-MS analysis,

used to identify essential oils, was performed using a HP 5975-7890 GC-MSD system

operating in the electron ionization (EI) mode at 70 eV, equipped with HP-5MS fused silica

capillary column (30 m x 0.25 mm; 0.25 µm film thickness). The column and injector

temperature were the same as those for GC. Essential oil components were identified by

comparing their retention times (RT) with literature values [26,27] and their mass spectral

data with those from Wiley HPCH2205.L and NIST05a.L mass spectral databases. The

composition of essential oils was expressed as percentage of total peak area.

2.4 Antibacterial Activity of Oils

Antibacterial activity of essential oils was screened using the wet disc diffusion method [28].

Agar cultures of Gram-positive bacteria of B. cereus, Micrococcus luteus and S. aureus, and Gram-negative bacteria of E. coli, Pseudomonas aeruginosa and Salmonella choleraesuis

were prepared. Suspensions of bacteria (100 µl) were spread evenly onto 20 ml Mueller–Hinton agar preset in 90 mm Petri dishes. Paper discs (6 mm diameter) were impregnated

with 10 µl of essential oils serially diluted two-fold with dimethylsulphoxide (DMSO).

Impregnated discs were transferred onto inoculated agar together with streptomycin

susceptibility discs (10 µg) as positive controls and DMSO discs as negative controls. After

incubation overnight at 37oC, inhibition zones were measured and recorded as mean diameter

(mm). Results were expressed as minimum inhibitory concentration (MIC), the minimum

concentration of essential oils required to show a zone of inhibition.

3. RESULTS AND DISCUSSION

Essential oils from leaves (500 g) of four Etlingera species were extracted by hydro-

distillation. Leaves of E. maingayi yielded the most oil of 1317 mg/100 g. The yields of the

other three species, namely, E. elatior, E. fulgens and E. rubrostriata were 86, 133 and 39 mg/100 g, respectively. The chemical composition of essential oils from leaves of four

Etlingera species as determined by GC-MS is presented in Table 1. The quantity and types of compounds in each species are shown in Table 2. The number of compounds identified in E.

elatior, E. fulgens, E. maingayi and E. rubrostriata was 15, 11, 4 and 23, respectively. Of these species, only the leaf oil of E. elatior has been studied [29].


Table 1: Composition of essential oils from leaves of Etlingera

Essential oil Type RT Percentage of total peak area

E. elatior E. fulgens E. maingayi E. rubrostriata

α-Thujene cdegh

Monoterpene

7.68

0.09

Sabinene bcdgh

Monoterpene 10.47 0.11

Undecane Alkane 18.91 0.02 0.09

Linalool bcefh Monoterpenol 19.32 1.45

Terpinen-4-ol abef

Monoterpenol 23.77 2.78

α-Terpineol abcf

Monoterpenol 24.69 0.90 0.11 2.55

Decanal bd

Aldehyde 25.26 0.39

Octanoic acid Fatty acid 25.28 0.40

Geraniol acfh

Monoterpenol 28.31 0.22

Methyl myrtenate Monoterpenic ester 29.97 0.87 Undecanal Aldehyde 30.56 0.24

Methyl decanoate Fatty acid ester 31.38 0.19

Myrtenyl acetate Monoterpenol ester 31.38 0.15

Tetradecene Alkene 34.53 0.54

β-Elemene bgh

Sesquiterpene 34.54 0.26

Dodecanal Aldehyde 35.51 3.09 8.08

(E)-Caryophyllene bcde


Decanoic acid Fatty acid 36.53 42.6

(E)-Farnesene bcd

Sesquiterpene 37.57 13.6 0.36

Tridecanone Ketone 37.35 0.41

Isodaucene Sesquiterpene 39.39 1.84 β-Bisabolene

fh Sesquiterpene 39.82 0.32 0.57

β-Sesquiphellandrene abe


Hedycaryol Sesquiterpenol 41.88 0.25

(E)-Nerolidol cdh

Sesquiterpenol 42.35 0.27 1.53

Caryophyllene oxide agh

Sesquiterpene epoxide 43.10 5.15

Dodecanoic acid Fatty acid 44.03 44.6 4.41

Dodecyl acetate Ester 44.15 6.68 21.6 6.01

γ-Eudesmol cg

Sesquiterpenol 45.22 0.64

α-Eudesmol cg


Pentadecanol Alcohol 47.13 6.39 14.1 1.01

(E,E)-Farnesol ac


Octadecene Alkene 50.94 1.95 Hexadecanol Alcohol 51.65 1.66 3.60

Phytol Diterpenol 56.59 0.28 1.35

Cyclohexadecanolide Cyclic ester 56.97 0.75

Geranyl linalool Diterpenol 59.35 0.93

Oleic acid Fatty acid 63.35 1.38

Docosene Alkene 64.32 1.24

abcdefgh

Previously reported in leaves of Elettariopsis elan [20], Alpinia conchigera [16], Alpinia galanga

[34], Etlingera elatior [29], Curcuma longa [35], Alpinia malaccensis [17], Alpinia zerumbet [19] and

Alpinia smithiae [18], respectively. Composition of essential oils was expressed as percentage of total peak

area. RT = retention time (min).


Table 2: Composition and types of essential oils from leaves of Etlingera

Type of

essential oil

Percentage of total peak area

E. elatior E. fulgens E. maingayi E. rubrostriata

Alcohol 8.05 (2) 17.7 (2) 1.01 (1)

Aldehyde 3.09 (1) 8.32 (2) 0.39 (1)

Cyclic ester 0.75 (1)

Ester 6.68 (1) 21.6 (1) 6.01 (1)

Fatty acid 1.38 (1) 87.6 (3) 4.41 (1)

Fatty acid ester 0.19 (1)

Hydrocarbon 3.73 (3) 0.02 (1) 0.09 (1)

Ketone 0.41 (1)

Monoterpene 0.20 (2)

Monoterpene derivative 1.77 (2) 0.11 (1) 7.15 (5)

Sesquiterpene 24.5 (5) 1.19 (3)

Sesquiterpene derivative 5.15 (1) 0.27(1) 4.73 (5)

Diterpene derivative 0.28 (1) 2.28 (2)

Total 53.0 (15) 50.4 (11) 87.8 (4) 27.9 (23)

Composition of essential oils was expressed as percentage of total peak area. Figures in brackets indicate

the diversity of a given type.

Sesquiterpenes were the major constituents of oil from E. elatior leaves, comprising (E)-

farnesene (13.6%), (E)-caryophyllene (8.56%), isodaucene (1.84%), β-bisabolene (0.32%)

and β-sesquiphellandrene (0.18%) (Figure 2). (E)-Farnesene and (E)-caryophyllene, the

major constituents, have been reported earlier [29]. Oil of E. fulgens consisted mainly of

dodecyl acetate (21.6%), pentadecanol (14.1%) and hexadecanol (3.60%) (Figure 2). These

compounds were also present in E. elatior but in much smaller amounts. Dodecanal, detected

in leaves of E. elatior (3.09%) and E. fulgens (8.08%), was previously reported in

inflorescences of E. elatior [30]. It can be seen that essential oils from leaves of E. elatior and

E. fulgens were different in composition despite having similar aroma and leaf morphology.

Leaves of E. maingayi yielded the most oil (1317 mg/100 g) but had the least number of

compounds (Figure 3). The oil consisted almost entirely of three fatty acids (87.6%) and one fatty acid ester (0.19%). The two major fatty acids were dodecanoic acid C12H24O2 (44.6%)

and decanoic acid C10H20O2 (42.6%). The unpleasant sour scent of E. maingayi leaves may be attributed to their high fatty acid content. Oil from leaves of E. rubrostriata was the most

diverse with 23 different compounds identified (Figure 3). However, they only represented 27.9% of the total composition, implying the presence of uncommon compounds. Despite

having many different types of compounds, leaves of E. rubrostriata do not emit any scent. This is probably due to their low essential oil content of only 39 mg/100 g.


Figure 2: GC chromatograms of leaf oils of Etlingera elatior

and Etlingera fulgens showing the peaks of components

b

c

a

f

h

e

g

a = (E)-Caryophyllene b = (E)-Farnesene c = Dodecyl acetate d = Pentadecanol

e = Dodecanal f = Dodecyl acetate g = Pentadecanal h = Hexadecanol

d

Etlingera elatior

Etlingera fulgens


Figure 3. GC chromatograms of leaf oils of Etlingera maingayi

and Etlingera rubrostriata showing the peaks of components

Oils from leaves of all four Etlingera species inhibited Gram-positive bacteria of B. cereus,

M. luteus and S. aureus with no activity on Gram-negative bacteria of E. coli, P. aeruginosa and S. choleraesuis. Leaf oil of E. maingayi had the strongest activity with MIC of 6.3 mg/ml

against B. cereus and M. luteus, and 12.5 mg/ml against S. aureus (Table 3). Of the Gram-positive bacteria, M. luteus was the most susceptible with all Etlingera species having MIC of

6.3 mg/ml. Based on MIC of oils, ranking was of the order: E. maingayi > E. rubrostriata > E.

elatior > E. fulgens.

i

j

m k = Terpinen-4-ol l = α-Terpineol m = Dodecanoid acid

i = Decanoid acid j = Dodecanoid acid

k l

Etlingera maingayi

Etlingera rubrostriata


Table 3: Minimum inhibitory concentration (MIC) of essential oils

from leaves of Etlingera species against Gram-negative bacteria

Etlingera

species

Minimum inhibitory concentration (mg/ml)

Bacillus cereus Micrococcus luteus Staphylococcus aureus

E. elatior 25.0 6.30 50.0

E. fulgens 25.0 6.30 100

E. maingayi 6.30 6.30 12.5

E. rubrostriata 12.5 6.30 50.0

The strong antibacterial activity of leaf oil of E. maingayi may be due to their high content of fatty acids, notably, dodecanoic (lauric) acid and decanoic (capric) acid, which constitute

more than 87% in content. In leaf oils of E. rubrostriata, which ranked second in antibacterial activity, lauric acid (4.41%) is also found. These two acids are known to have antibacterial

activity. They displayed antibacterial activity against all nine types of bacteria tested, with lauric acid showing much stronger inhibition than capric acid [31]. Out of eight types of fatty

acids tested, lauric acid has been reported to display the strongest inhibition against meat spoilage bacteria of Carnobacterium piscicola, Lactobacillus curvatus and Lactobacillus sake

[32].

Fatty acids have been shown to possess antibacterial activities and Gram-negative bacteria

are generally more resistant than Gram-positive bacteria due to antagonistic effects of fatty acids with their cell wall lipopolysaccharides [32]. Recently, the antibacterial activities of

fatty acids and their mechanisms of action have been reviewed [33].

There are few studies on the antibacterial activity of essential oils from leaves of ginger species. One early study reported that essential oil from leaves, rhizomes and stems of A.

zerumbet inhibited Gram-positive bacteria of Bacillus subtilis, Mycobacterium phlei, Sarcina

lutea and S. aureus, and Gram-negative bacteria of E. coli and P. aeruginosa [19]. Based on

antibacterial activity, ranking of A. zerumbet oil was of the order: stems > leaves > rhizomes.

A recent study showed that oil from A. conchigera leaves had weak activity against S. aureus,

Staphylococcus epidermidis, Pseudomonas cepacia and P. aeruginosa [16]. Antibacterial

activity of leaf oil of A. conchigera was however stronger than stem and rhizome oils.

4. CONCLUSION

Comparing essential oils from leaves of four Etlingera species, E. rubrostriata had the

highest diversity with 23 different compounds identified. Composition of oils from leaves of

E. elatior and E. fulgens was very different despite having a very similar aroma and leaf morphology. Leaves of E. maingayi had the highest yield of oil, comprising mainly fatty

acids, notably, dodecanoic and decanoic acids. Oils of all four Etlingera species inhibited Gram-positive bacteria with no activity against Gram-negative bacteria. Based on MIC of oils,

ranking was of the order: E. maingayi > E. rubrostriata > E. elatior > E. fulgens. Variability in antibacterial activity of the leaf oils of the four species can be attributed to qualitative and

quantitative differences in the constituents of individual oils.


5. ACKNOWLEDGEMENTS

The authors are thankful to the Ministry of Science, Technology and Innovations (MOSTI) of

Malaysia for funding the project, Monash University Sunway Campus (MUSC) and Forest Research Institute Malaysia (FRIM) for providing the research facilities, and Ms. S.K. Wong

for assisting in the collection of leaves and extraction of leaf oils.

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Composition and Antibacterial Activity of Essential Oils from Leaves of Etlingera species...

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Transcript of Composition and Antibacterial Activity of Essential Oils from Leaves of Etlingera species...