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ASIA
LIFE
SCIENCES
The Asian International
Journal of Life Sciences
ISSN 0117-3375
REPRINT
Beyond Excellence©
VOLUME 27(2) JULY-DECEMBER 2018
Chemical composition and bioactivity of essential oil
from the leaves of Scorodocarpus borneensis Becc.
(Olacaceae) grown in Indonesia
HARLINDA KUSPRADINI, SAAT EGRA,
INDAH WULANDARI and AGMI SINTA PUTRI
e-mails: asialifesciences@yahoo.com wsmgruezo@gmail.com
Website - http://www.sersc.org/journals/ALS/
©Rushing Water Publishers Ltd., 2018 Printed in the Philippines
ASIA
Printed in the Philippines
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ASIA LIFE SCIENCES 27(2): 343-353, 2018
The Asian International Journal of Life Sciences
Received 02 September 2018; Accepted 22 October 2018
©Rushing Water Publishers Ltd. 2018
Chemical composition and bioactivity of essential oil
from the leaves of Scorodocarpus borneensis Becc.
(Olacaceae) grown in Indonesia
HARLINDA KUSPRADINI1*, SAAT EGRA1,
INDAH WULANDARI1 and AGMI SINTA PUTRI1
The essential oil of Scorodocarpus borneensis Becc. (Olacaceae) was obtained from
its leaves by steam distillation. In this study, S. borneensis leaves yielded a clear yellowish
essential oil. Its chemical composition was analyzed by GC-MS. Six chemical compounds
were identied, and most components of the essential oil of S. borneensis leaves were sulfur-
containing compounds, such as trisulde, dimethyl, methyl (methylsulnyl) methyl sulde,
2,4,6-trithiaheptane-2,2-dioxide, and methane, (methylsulnyl) (methylthio). The major
compounds are 2,4,6-trithiaheptane-2,2-dioxide (43.35%), and methyl (methylsulnyl)
methyl sulde (34.03%). Anti-microbial properties were determined using the agar diffusion
method. Four different microorganisms were used in this study: Streptococcus sobrinus,
S. mutans, Staphylococcus aureus and Candida albicans. The zone of inhibition and activity
index were measured and compared against a known synthetic standard. The essential oil
showed strong activity against all tested microorganisms. Anti-oxidant activity was assayed
with 1,1-diphenyl-2-picrylhydrazyl (DPPH) with ascorbic acid as a positive control. The
essential oil has potency to inhibit free radicals at concentrations of 25-1,000 µg/mL. The
results indicated that S. borneensis leaves oil is a good, new natural anti-microbial agent for
oral pathogens.
Keywords: Scorodocarpus borneensis Becc., Olacaceae, essential oil, distillation,
agar diffusion, DPPH, GC/MS, sulf ur-containing compounds, anti-oxidant activity,
anti-microbial agent, oral pathogens, Streptococcus sobrinus, S. mutans, Staphylococcus
aureus, Candida albicans
1Faculty of Forest ry, Mulawar man University, Jl. Ki Hajar Dewantara, Gunung Kelua, Samarinda,
East Kalimant an, Indonesia
*Corresponding author: e-mail - hkuspradini@fahutan.unmul.ac.id
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Asia Life Sciences 27(2) 2018
INTRODUCTION
Scorodocarpus borneensis Becc. (Olacaceae) is a tall tree that grows naturally
on the island of Borneo and in the Malay Peninsula. The local people refer to it as
“wood garlic” due to its strong garlic odor. The aroma of garlic is present in the
leaves, flowers and fruits. The falling fruit has a rugged hard skin and is similar in
shape and size to a walnut (Burkill 1935). The older leaves are used as a seasoning
rather than consumed as a vegetable (Hoe & Siong 1999). The decoctions of
S. borneensis roots are taken orally to cure hemorrhoids (Mohammad et al. 2012).
In Sarawak, the leaves and bark are boiled and drunk to treat leprosy and diabetes
(Lim et al. 2012).
Sesquiterpenscodopin and scorodocarpines are found in the fruits of
S. borneensis and hemi-synthetic sesquiterpene and cadalene-β-carboxylic acid
are found in its bark (Wiart et al. 2001). In previous studies, other compounds
have been isolated and identif ied from the fruits of S. borneensis, including
sulfur-containing compounds, such as 2,4,5-trithiahexane, 2,4,5,7-tetrathiaoctane,
2,4,5,7-tetrathiaoctane 2,2-dioxide, and 2,4,57-tetrathiaoctane 4,4-dioxide
(Kubota et al. 1999a, b; Lim et al. 1998). Kubota & Kobayashi (1994)9 found that
components from the fruits of S. borneensis were useful as a natural preservative.
Most components in the fruits of S. borneensis were sulfur-containing compounds,
such as methyl methylthiomethyl disulfide and bis(methylthiomethyl) disulfide.
Many higher and aromatic plant-derived medicines used in folk medicinal
systems have been reported as agents used to treat infectious diseases, and a number
of these medicines have been investigated for their eff icacy against oral pathogens.
Essential oils from several plant species, namely: Cinnamomum zeylanicum Blume
(L aurac eae), Citrus aurantiifolia (Christm.) Swingle (Rutaceae), Lippia graveolens
Kunth (Verbenaceae), and Origanum vulgare L. (Lamiaceae) can control
microorganisms related to oral bacteria (Miller et al. 2 015).
To the best of our knowledge, no reports on the chemical compounds of
essential oil from the leaves of S. borneensis have been published so far and little is
known about the anti-microbial activity against oral pathogens or the effects
on dental plaque formation in vitro. Thus, in the present study, essential oil was
distilled from plant leaves collected in East Kalimantan, and oil composition was
analyzed by gas chromatography mass spectrometry (GC/MS). Furthermore, its
anti-microbial activity against four oral pathogens and anti-oxidant activities were
assayed.
MATER IALS AND METHODS
Leaves of Scorodocarpus borneensis were collected from t he Botanical Garden
of Mulawarman University, East Kalimantan, Indonesia. The leaves were dried and
prepared in one day. Glucose, nutrient broth and anhydrous sodium sulfate were
obtained from Merck (Darmstad, Germany). DPPH (1,1-diphenyl-2-picrylhydrazyl)
was purchased from Wako Crude Chemical Industries, Ltd., Japan. Other chemicals
were commercially available. The plant name was verified as the accepted name
of the species in the genus Scorodocarpus (Olacaceae) at www.theplantlist.org. A
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Bioactivity of essential oil from leaves of Scorodocarpus borneensis
Asia Life Sciences 27(2) 2018
voucher specimen was deposited in the Dendrology Laboratorium of Mulawarman
Un iver s ity.
Steam distillation method. Steam distillation is used widely in isolating liquids
from natural sources. The leaves into the kettle are placed on a hollow plate over
boiling water. The essential oil is evaporated for 4 hours or more. The oils were
collected and separated using a separatory funnel after the steam distillation
process. Oil and water will separate and form two layers. Oil that has a higher
density of air will sink to the bottom while some oil does not sink and will be
trapped at the top of the separation funnel. The process of separating and collecting
oil is repeated several times until no oil is left in the separation funnel and nothing
else can be obtained. Anhydrous sodium sulfate was used to adsorb the residual
water that fused with the oil. The quantity of oil was determined according to the
yield (Kuspradini et al. 2 016 ).
The percent and yield of essential oil was calculated by following formula
(Siddiqui et al. 2006):
%Yield = [Weight of oil (grams)/Weight of sample taken (grams)] x 100%
Anti-microbial assay.Anti-microbial susceptibility testing was done using the well
diffusion method to detect the presence of anti-bacterial and anti-fungal activities
of the plant samples. Nutrient agar for microbial cultures were prepared according
to the manufacturer’s instructions.
Anti-microbial assays were conducted using the agar diffusion method with
modification (Donaldson et al. 2005). The microorganisms used in this study were
Streptococcus sobrinus, S. mutans, Staphylococcus aureus, and Candida albicans.
All materials were sterilized by autoclaving at 15 lbs per square inch pressure
(121ºC) for 15 min. Microbes were inoculated in nutrient agar (NA). Approximately
5 ml of sterile media was poured into 5 cm-diameter petri dishes. After the media
solidified, 25 µl of microbial suspension was inoculated using a sterile swab and
was spread over the surface of the media three times. Next, 6 mm-diameter wells
were bored into the solidified media using sterile cork borer. Serial dilutions of S.
borneensis essential oil were prepared with 40% ethanol. The cr ude essential oils
were diluted to serial dilutions at the following concentration 1, 1/10, and 1/100
(v/v). Twenty microliters of each essential oil concentration were added into the
wells. Chlorhexidine (10 µg per well), a standard synthetic antibiotic, was used as
a positive control, and 40% ethanol was used as a negative control. All plates were
incubated at 37˚C for 24-48 hours. After incubation, the petri dishes were observed
for formation of a clear inhibition zone around the well, indicating the presence
of anti-bacterial activity. The zone of inhibition was calculated by measuring
the diameter of the inhibition zone around the well. All tests were performed in
duplicates. AI was calculated using the formula adopted from Arya et al. (2010):
AI = Inhibition zone of sample/Inhibition zone of standard
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Kuspradini et al. 2018
Asia Life Sciences 27(2) 2018
Anti-oxidant assay.The anti-oxidant activity of the essential oil was determined by
the DPPH radical scavenging method (Bachrouch et al. 2015) with modification.
Five hundred microlitres of the sample in methanol solution weres added to
500 mL of a methanolic DPPH solution with final concentration at 25, 50, 100, 250,
500, 1,000 µg/mL. Ascorbic acid was used as a positive control. The measurement
of absorbance was made against a blank prepared for each concentration at
517 n m using a Shimadz u UV-VIS 1200 spectrophotometer (Shimadzu Cor p., Kyoto,
Jap an). The anti-radical activity (three replicates per treatment) was expressed as
IC50 (mg/mL), the concentration required to cause a 50% DPPH inhibition. The
ability to scavenge the DPPH radical was calculated using the following equation:
SA% = [(Acontrol – Asample)/Acontrol] ×100
where: Aco ntrol is the absorbance of the control reaction (containing all reagents
except the test compound); Asample is the absorbance of the test samples. Samples
were analyzed in triplicates.
Gas chromatography-mass spectrometry (GC/MS) analysis. The essential oil was
analyzed by GC-MS (Shimadzu-QP-5050A) with the following setting: column -
HP-5 MS, 60 m x 250 µm ID x 0.25μm film thickness; temperature program - from
70 to 290°C (40 minutes) at 15°C.minute-1, and injection temperature - 290°C. The
injection port temperature was 290°C, and the detector temperature was 250°C.
The injection mode was split (50:1), and the inlet pressure was 18.03 psi. The carrier
gas was helium with a flow rate of 1 ml.minute-1. The mass spectrometer conditions
were as follows: ionization voltage: 70 eV; MS source temperature at 250°C; MS
quadruple temperature at 150°C; interface temperature at 290°C and electron
ionization mass spectra were acquired over the mass range of 40-800 m/z.
Statistical data analysis. The experimental results were expressed as mean
± standard deviation (SD) of three replicates. Regression analysis with polynomial
model of dose-response curve plotting between different concentration and percent
inhibition were used to obtained the IC50 value. Microsoft Excel 2010 statistical
package was used for all analyses.
RESULTS
Essential oil from the leaves of S. borneensis was clear and yellowish. The
results of the yield and refractive index were 0.39% and 1.435, respectively. The
GC-MS chromatogram of the essential oil of S. borneensis showed 6 peaks,
indicating the presence of six compounds (Table 1). The chemical compounds were
identified by comparing their retention time, molecular formula, molecular weight
and area (Table 1).
The most abundant compounds identified in the essential oils were
2,4,6-trithiaheptane-2,2-dioxide, methyl (methylsulfinyl) methyl sulfide, and
1,5-heptadien-3-yne (Figure 1). GC-MS analysis revealed that the essential oil of
S. borneensis is mainly composed of sulfur-containing compounds. Most
components in the essential oil of S. borneensis leaves were sulfur-containing
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Bioactivity of essential oil from leaves of Scorodocarpus borneensis
Asia Life Sciences 27(2) 2018
compounds, and 35.99 and 47.5% of these compounds consisted of sulfides with
two and three sulfur atoms, respectively.
Table 1. Chemical constituents of the essential oil of Scorodocarpus borneensis by
GC-MS.
No. Retention
Time (min) Compound names*Molecular
Formulas
Molecular
Weights
Area
(%)
1 6.45 Trisulde, dimethyl C2H6S3126.26 4.15
2 9.18 Methyl (methylsulnyl)
methyl sulde C3H8OS2124.22 34.03
3 14.56 1,5-Heptadien-3-yne C7H892.14 10.50
4 18.51 2,4,6-trithiaheptane-2,2-
dioxide C4H10S3154.32 43.35
5 24.15
Furan, tetrahydro-2,2-
dimethyl-5-(1-methyl-1-
propenyl)
C10H18O 154.25 6.01
6 27.09 Methane, (methylsulnyl)
(methylthio) C3H8OS2124.225 1.96
*Compounds were identied using the NIST, Wiley Mass Spectr al Library and the mass spectroscopy
data analysis.
Figure 1. Major compounds identied in the essential oil of Scorodocarpus
borneensis: (a) Methyl (methylsulnyl) methyl sulde; (b) 2,4,6-trithiaheptane,
and (c) 1,5-Heptadien-3-yne.
In this study, four microbes were investigated in susceptibility tests with
different concentrations of the essential oil. The essential oil showed better activity
than the commercial antibiotics, chlorhexidine and chloramphenicol (Table 2). The
essential oil was found to be highly effective at inhibiting the growth of all tested
microbes.
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Kuspradini et al. 2018
Asia Life Sciences 27(2) 2018
Table 2. Anti-microbial activity of essential oil of Scorodocarpus borneensis
against four microbes.
Sample
concentration
Diameter of inhibition (mm)
Streptococcus
sobrinus
Streptococcus
mutans
Candida
albicans
Staphylococcus
aureus
CHX* 20.70±0.00 21.00±0.00 17.70±0.00 17.00±0.00
CMP* 28.70±0.00 31.30±0.00 17.30±0.00 23.30±0.00
1 51.57±0.94 53.67±0.94 52.67±0.47 52.89±0.51
1/10 50.33±0.00 51.67±0.47 51.33±0.47 51.78±1.01
1/100 18.00±0.94 18.50±0.24 18.17±0.71 15.67±0.58
Remarks : CHX= Chlorhexidine, CMP= Chloramphenicol, * at concentration (10 mg)
Estimation of the potential antimicrobial can be measured quantitatively. It
can be measured by the activity index (AI) values by comparing the inhibition zone
of sample to inhibition zone of respective standards. The AI against chlorhexidine
showed that the essential oil of S. borneensis exhibited the strongest bactericidal
activity at a concentration of 1 (crude essential oil, v/v) against S. aureus. The AI
decreased in the following order: S. aureus > C. albicans > S. mutans > S. sobrinus
(Figure 2a). Furthermore, the AI against chloramphenicol showed that the essential
oil of S. borneensis exhibited the strongest bactericidal activity on crude essential
oil (concentration 1, v/v) against C. albicans. The activity index of essential oil
against chloramphenicol decreased in the following order: C. albicans > S. aureus>
S. sobrinus > S. mutans (Figure 2b). Based on the activity index, the essential oil
had the best activity index of 3.11 in S. aureus.
Figure 2. Compar ison of essential oil and antibiotics activit y index: (a) Chlorhexidine
and (b) Chloramphenicol.
The essential oil of S. borneensis showed a dose-dependent inhibitory effect
against radical scavenging DPPH with an IC50 value of 715.97 µg/mL. The essential
oil did not have good radical scavenging compared to ascorbic acid (Table 3).
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Bioactivity of essential oil from leaves of Scorodocarpus borneensis
Asia Life Sciences 27(2) 2018
Table 3. Anti-oxidant activity of essential oil of Scorodocarpus borneensis.
No. Samples
Percentages of Anti-oxidant Activity
(%) IC50
(µg/
mL)
1000
µg/
mL
500
µg/
mL
250
µg/
mL
100
µg/
mL
50
µg/
mL
25
µg/
mL
1 Ascorbic acid*- - - 97.01 96.81 97.1 -
2S. borneensis 54.52 37.18 36.34 7.63 4.15 3.28 715.97
*There were no tests for concentrations of 250-1,000 µg/mL.
DISCUSSION
Steam distillation appears to be a good method for extracting the essential oil
from leaves of S. borneensis as it results in good yield and is a simple technique.
The advantage of this technique is the favored material distills at a temperature
below 10 0oC. Therefore, the decomposition may be prevented if an unstable or
excessively boiling essential ingredient is removed from the mixture. Because all
gases mix, the two materials can be mixed in the evaporation and co-distil. Once
the distillate is cooled, the desired components which are miscible, are separated
from the water (Pavia 2011). In this study, we report the presence of a methyl
(methylsulfinyl) methyl sulfide and 2,4,6-trithiaheptane-2,2-dioxide in the essential
oil of S. borneensis leaves. Similar results have been obtained, but these compounds
were found in another part of S. borneensis plant. Methyl (methylsulfinyl) methyl
sulfide was the main component in the fruits of S. borneensis. This compound has
natural preservative properties (Kubota & Kobayashi 1994). 2,4,6-Trithiaheptane-
2,2-dioxide was previously isolated from the fruits of S. borneensis. Trisulfide,
dimethyl or DMTS is a sulfur-based molecule found in garlic, onion, broccoli
and similar plants, and it has been reported to act as a sulfur donor-type cyanide
counter measure and key mediator of pollinator attraction in brood-site deceptive
plants (Rockwood et al. 2 016 , Zit o et al. 2014). 1,5-Heptadien-3-yne were fatty acid
compounds that are also found in the flower fragrance of Cypripedium tibeticum
(Li et al. 2006). Furan, tetrahydro-2,2-dimethyl-5-(1-methyl-1-propenyl) has a citrus
odor and categorized as a f lavoring agent (Burdock 2010). Methane, (methylsulfinyl)
(methylthio) is also found in the essential oil of Allium atroviolaceum and Sonchus
arvensis leaves (Lorigooini et al. 2 014).
Scorodocarpus borneensis leaf oil has strong activity against all microbial
tested in this study and this result agreed with Kuspradini et al. (2016) that screened
the anti-microbial activity of several essential oils. It has been reported that the
crude oil of S. borneensis leaves had anti-microbial activity against S. aureus and
C. albicans with no comparisons of different concentrations. Compared to results
from the previous study, the inhibition activity of S. borneensis essential oil against
S. aureus is stronger in this study. This difference in activity is probably due to
variations in the essential oil composition at different sample collection times. The
biological and pharmacological activities of essential oils rely upon the species,
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Kuspradini et al. 2018
Asia Life Sciences 27(2) 2018
ecological factors and e nviron mental conditions (La hlou 2004). Based on the activity
index (AI), the essent ial oil had good potency as an ant i-microbial agent. The ranges of
AI were 0.59-1.05, 1.65-3.04, 1.79-3.11 at d ifferent diluted concentr ation of 1, 1/10 and
1/100, respectively. Activity index of positive controls/antibiotics was 1. The AI
value of more than 1 indicated the considerable role of sample. Interestingly, high
activity indexes (AI > 1) were observed at essential oil concentration of 1/10 and
1. According to Hosamath (2011) and Awan et al. (2013), the activity index of the
test substance above 0.5 was considered as significant activity and the more AI
values evaluated the more significant the results. The anti-microbial activity of a
given essential oil may depend on only one or two of the oil’s major constituents.
However, increasing evidence indicates that the inherent activity of essential oils
may rely on not only the ratio of the main active constituents but also the interactions
between them and the oil’s minor constituents (Singh et al. 2014). In this study,
most components of the essential oil of S. borneensis leaves were sulfur-containing
compounds, with 93.49% consisting of sulfides with two or three sulfur atoms.
Researchers have demonstrated that sulfur-containing compounds may be useful as
anti-microbials (Naganawa et al. 1996, Lim et al. 1998, Kim et al. 2006). According
to earlier studies (e.g. Kim et al. 2004), sulfides, especially those with three or
more sulfur atoms, apparently possess potent anti-microbial activity. It has been
suggested that the strong anti-microbial activity of S. borneensis leaf oil is due to
the availability of its major constituent with three sulfur atoms: 2,4,6-trithiaheptane-
2,2-dioxide.
The half maximal inhibitory concentration 50 (IC50) were used to determine
anti-oxidant capacity of sample compared to standard. Samples that had IC50 values
lower than 50 µg/ml were very strong anti-oxidant, 50-100 µg/ mL were strong
anti-oxidant, 101-150 µg/mL were medium anti-oxidant, while weak antioxidant
with IC50 higher than 150 µg/ mL (Blois 1958). Based on this, the essential oil of
S. borneensis could be classified as weak anti-oxidant with an IC50 of more than 150
µg/ mL. Researchers have demonstrated that sulfur-containing compounds may
be useful as anti-oxidants (Dansette et al. 1990, Pappa et al. 2007). But, in many
essential oils due to the absence of phenols, most of them exhibit no or low anti-
oxidant activities (Sharopov et al. 2015). It can be assumed that the anti-oxidant
activity of the tested essential oils as nonpolar extracts could be linked to their
phenolic concentration. However, it is important to realize that in certain cases, anti-
oxidants can be pro-oxidant and can stimulate free radical reactions. The methods
of expressing anti-oxidant activity appear to be as varied as the methods of anti-
oxidant measurement. The measurement of anti-oxidant activities, especially for
anti-oxidants that are mixtures, multi-functional or acting in complex multi-phase
systems, cannot be evaluated satisfactorily by a simple anti-oxidant test without
considering the many variables influencing the results (Antolovich et al. 20 02).
CONCLUSION
In this study, the leaves of S. boornensis can produce the essential oil with
the strong anti-microbial activities against oral pathogens. To the best of our
knowledge, no reports on the chemical compounds of essential oil from the leaves
351
Bioactivity of essential oil from leaves of Scorodocarpus borneensis
Asia Life Sciences 27(2) 2018
of S. borneensis have been published so far. This is the first report that discusses the
essential oil isolated from S. borneensis leaves, its anti-microbial, anti-oxidant and
its chemical composition. The most components of the essential oil of S. borneensis
leaves were sulfur-containing compounds, with 93.49% consisting of sulfides with
two and/or three sulfur atoms. Therefore, this property could be used to develop new
anti-microbial ingredients from S. borneensis leaf oil for oral or personal products.
ACKNOWLEDGMENTS
The authors gratefully acknowledge the generous assistance of the Members of the
Laborator y of Forest Products Chemist ry, Faculty of Forestr y, Mulawarman University, East
Kalimantan, Indonesia. This work was supported by the Ministry of Research, Technology
and Higher Education of the Republic of Indonesia (Grant Number: 347/UN17.41/KL/2017).
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ASIA LIFE SCIENCES
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Volume 27 Number 2 July-December 2018
CONTENT
343 Chemical composition and bioactivity of
essential oil from the leaves of Scorodocarpus
borneensis Becc. (Olacaceae) grown in Indonesia
HARLINDA KUSPRADINI1*, SAAT EGRA1,
INDAH WULANDARI1 and AGMI SINTA PUTRI1
1Faculty of Forestry, Mulawarman University,
Jl. Ki Hajar Dewantara, Gunung Kelua, Samarinda,
East Kalimantan, Indonesia
*Corresponding author: e-mail - hkuspradini@fahutan.unmul.
ac.id
©Rushing Water Publishers Ltd. 2018 Printed in the Philippines
