Journal of Tropical Forest Science 28(1): 39–47 (2016) Jantamas S et al.

IMPROVEMENT OF ANTIFUNGAL ACTIVITY OF CITRONELLA

OIL AGAINST ASPERGILLUS FLAVUS ON RUBBERWOOD (HEVEA
BRASILIENSIS) USING HEAT CURING
S Jantamas1, N Matan2, 3, *, N Matan1, 3 & T Aewsiri2

1Schoolof Engineering and Resources, Walailak University, Thasala, Nakonsithammarat 80161, Thailand
2Schoolof Agricultural Technology, Walailak University, Thasala, Nakonsithammarat 80161, Thailand
3Research Center of Excellence in Wood Science and Engineering,Walailak University, Thasala, Nakonsithammarat

80161, Thailand

Received May 2014

JANTAMAS S, MATAN N, MATAN N & AEWSIRI T. 2016. Improvement of antifungal activity of citronella
oil against Aspergillus flavus on rubberwood (Hevea brasiliensis) using heat curing. Optimisation of the
inhibitory effect of citronella oil (10, 30 and 50 µg mL-1) with heat curing (30, 90 and 150 °C) and drying
periods (1, 12 and 24 hours) against a major mould (Aspergillus flavus) found on the surface of rubberwood
was investigated using response surface methodology. Specimens were incubated at 25 °C in 100% relative
humidity for 90 days and individually rated for the period it took to achieve zero mould growth on
rubberwood. Citronella oil components were analysed by gas chromatography–mass spectrometry. Citronella
oil (50 µg mL-1) with heat curing (30 and 90 °C) and drying periods (1 to 24 hours) completely inhibited
spore germination for at least 90 days. Microscopy investigation confirmed that no spore germination
was found in treated rubberwood. Citronellal (27.5%), geraniol (20.4%), citronellol (13.4%) were major
constituents of citronella oil. Heat curing may be important for transformation of components and
enhancement of antifungal activity of citronella oil. This study showed that a combination of citronella oil
and heat curing could protect rubberwood.

Keywords: Optimisation, drying, response surface methodology, enhancement

INTRODUCTION

Although chemical protection from boron, chemicals for termite prevention with reduced
borate, vapour boron, chromated copper environmental impact (Roszaini et al. 2013).
arsenate and volatile borate ester (Cameron & For this research, citronella oil was selected to
Pizzi 1985, Tsunoda 2001) is found to be suitable be applied on rubberwood (Hevea brasiliensis)
for preventing mould growth, decay fungi and to reduce mould growth.
insects on wood and wood products because of Citronella oil has white to yellow colour,
their broad spectrum (Williams & Amburgey good flavour and can be produced by steam
1985), chemical leaching of treated wood under distillation of Cymbopogon plants (Wany et al.
wet conditions (Grace et al. 2006) can cause 2013). Citronellol, geraniol (Nhu-Trang et al.
contamination. This is a serious environmental 2006) and d-limonene (Jaroenkit et al. 2011) were
problem as contaminated wood can affect soil reported to be main components. Antifungal
and drinking water and may be found in children activity of citronella oil against Aspergillus niger (Li
playground (Stilwell & Graetz 2001, Townsend et et al. 2013), A. flavus, Asparagus racemosus (Singh
al. 2005, Lesar et al. 2012). The use of essential et al. 2010) and Colletotrichum gloeosporioides
oils or other natural compounds from plants (Sellamuthu et al. 2013) has been reported.
for wood preservation has been recommended Insect protection with citronella oil has also
because they are less harmful (Matan & Matan been noted (De La Puente et al. 2009, Songkro
2012, Mohareb et al. 2013). Another benefit of et al. 2012). Citronellol can also be used against
essential oils is termite control (Saeki et al. 1971, the formosan subterranean termite, Coptotermes
Zhu et al. 2001) and the development of new formosanus (Zhu et al. 2001).

*[email protected]

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Journal of Tropical Forest Science 28(1): 39–47 (2016) Jantamas S et al.

Due to its strong flavour, citronella oil Specimens were kept in a conditioned room
should not be added directly into products or (20 °C and 65% relative humidity (RH)) for
on rubberwood surface. Therefore, to reduce the 1 month or until moisture content was 12%.
amount of citronella oil used and to improve its
antifungal activity, heat curing using response Mould strain
surface methodology was selected to determine
optimal conditions against the growth of A. flavus Aspergillus flavus (WU 0813) was isolated from
on rubberwood. the surface of rubberwood. The strain was from
the culture of Walailak University’s Cellulose
MATERIALS AND METHODS Protection Technology Laboratory. Aqueous
spore suspension of the mould was obtained from
Essential oil 7-day-old potato dextrose broth after incubation
at 25 °C. Spore suspension was counted using
The citronella oil (Cymbopogon nardus ) used in heamacytometer and adjusted to 106 spores mL-1
this study was provided by Thai China Flavors with sterile distilled water. The viability of mould
and Fragrances Industry Company, Thailand. was checked using quantitative colony counts at
106 CFU mL-1.
Gas chromatography–mass spectrometry
(GC–MS) analysis Inhibition of mould spore germination
on rubberwood
This analysis was carried out on trace GC.
The average helium carrier gas flow rate was The variables (concentration, drying period and
1 mL min-1. The split ratio of the column was heat curing) used to determine the period in
150:1. Injector and detector temperatures were which zero mould growth (PZMG) is found on
set at 250 and 260 °C respectively. The column the surface of rubberwood are shown in Table 1.
oven temperature was held at 60 °C for 1 min and Five rubberwood specimens were used and each
then programmed at 150 °C for 15 °C min-1 up was immersed in citronella oil at concentrations
to 300 °C. After that, it was changed to 2 °C min-1 of 10, 30 and 50 µg mL-1 for 10 min. Specimens
for 10 min. Citronella oil (1.0 μL) was injected were dried at different heat curing temperatures
manually. Constituent identification was based (30, 90 and 150 °C) and drying periods (1, 12
on comparisons of retention times with those and 24 hours) in an oven. Aspergillus flavus spores
of authentic samples comparing their Kovats were inoculated by spraying on treated specimens
indices and also by computer matching with the and specimens were stored at 25 °C and 100% RH
NIST 08.L (database/chem-station data system). in an environmental chamber. The rubberwood
specimens were individually rated for spore
Preparation of rubberwood germination on a scale of 0 to 5, with ‘0’ denoting
clean specimen and ‘5’ representing heavy mould
Rubberwood was obtained from a local growth (0 = clean, 1 = 20%, 2 = 40%, 3 = 60%,
rubberwood plantation located in Krabi province 4 = 80% and 5=100% of mould growth) according
of southern Thailand. It was cut into 2 cm (width) to ASTM D4445-91 (ASTM 2003). Observations
× 7 cm (length) × 0.5 cm (thick) specimens. were carried out until each specimen reached

Table 1 Maximum and minimum levels of variables used in full factorial design

Factor Parameter Actual level of code factor

-1 0 1
X1 Concentration (µg ml-1) 10 30 50
X2 Drying time (hours) 1 12 24
X3 Heat curing temperature (°C) 30 90 150

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Journal of Tropical Forest Science 28(1): 39–47 (2016) Jantamas S et al.

score 0. PZMG on the rubberwood surface (in 90 °C for 1 hour on the 90th day and on control
days) was also reported. treatment (tested with methanol for 3 days).
The independent variables used in this study
were X1, X2 and X3 where X1 = concentration RESULTS AND DISCUSSION
of citronella oil (µg mL-1), X2 = drying periods
(hours) and X3 = heat curing temperature (°C). GC–MS analysis of citronella oil
Other variables include Y (PZMG), b0 (intercept),
b1, b2 and b3 (linear coefficients), b11, b22 and The components of citronella oil are shown
b33 (squared coefficients) and b12, b13 and b23 in Table 2. Citronellal (27.5%), geraniol
(interaction coefficients). The model equation (20.4%) and citronellol (13.4%) were the
for a 3-factor system is: major components of citronella oil. These
main components of citronella oil agreed
Y = b0 + b1X1 + b2X2 + b3X3 + b12X1X2 +
b13X1X3 + b23 X2X3 + b11X12 + b22X22 + (1) with other findings (Zhu et al. 2001, Solomon
b33X23 et al. 2012).

Statistical analysis was per formed using Effect of heat curing on growth of mould
Statistica software. on rubberwood

Fourier transform infrared (FTIR) The surface plots in Figures 1a, b and c suggested
spectroscopy that the optimum points were within the design
limits. All surface plots showed that, as the
FTIR spectra of treated specimens concentration of the citronella oil increased,
(50 µg mL -1, 1 hour, 90 °C) were analysed the PZMG on rubberwood surface increased
using a Spectrum One FTIR spectrometer. The up to a certain level. For drying periods, no
spectra were acquired at resolution of 4 cm-1 and PZMG difference was found when it increased
measurements ranged from 800 to 4000 cm-1 at from 1 to 24 hours. The PZMG decreased
room temperature. The horizontal attenuated when temperature increased (> 90 °C).
total reflectance accessory was mounted into the Maximum PZMG was obtained at approximately
sample compartment. The internal reflection 90 days after (1) using concentration of
crystal, which was made of zinc selenide, had 50 µg mL -1 , (2) setting the temperature
45 °C angle of incidence to the infrared beam. at 30 or 90 °C and (3) drying periods from
Analysis of spectral data was carried out using 1 to 24 hours.
Spectrum One software program. Results of full factorial experiments to
determine effects of concentration (X1), drying
Wettability measurement period (X2) and heat curing temperature (X3)
are shown in Table 2. The PZMG is best predicted
Rubberwood treated with 50 µg mL-1 of citronella by the following equation:
oil with heat curing at 90 °C for 1 hour (n = 3)
was prepared. Wettability measurement was done Y = -3.91 – 1.84X1 + 0.64X3 + 0.07X12 –
0.01X1X3 – 0.002X23 (2)
by contact angle goniometer. Distilled water was
dropped on each specimen surface. The angle
made between the droplet and the specimen where Y predicted PZMG via concentration
surface was measured after 5 s. Measurements (X 1), drying period (X 2) and heat curing
were repeated five times at different locations temperature (X3).
for each sample and average values were used The coefficient of determination (r 2)
as contact angles. was 0.94, which indicated that the equation
adequately fitted the data. As seen from Table 3,
Microscopy when the temperature increased from 30 to 90 °C,
the efficacy of citronella oil against A. flavus
A microscope was used to observe mould growth was not affected. Therefore, this confirmed
on rubberwood surface after being treated with that heat curing (30–90 °C) could be used to
citronella oil at 50 µg mL-1 and heat curing at enhance the antifungal activity of citronella

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Journal of Tropical Forest Science 28(1): 39–47 (2016) Jantamas S et al.

Table 2 Chemical composition of citronella oil

Component % Area
Eugenol 1.1
Limonene 4.7
Citronellal 27.5
Linalool 1.0
Citronellol 13.4
Geraniol 20.4
Citronellyl acetate 4.8
Geranyl acetate 4.6
Germacrene D 3.6
Muurolene 1.3
Cadinene 4.4
Sum 86.8

(a) (b)
PZMG (days)

PZMG (days)

-1 )
Ti mL -1 )
m L
e (μL Te m
(h
ou ion m (μL
at pe tio
n
rs ntr ra tra
) nce tu n
Co re n ce
( °C Co
)
(c)
PZMG (days)

Te
m )
pe urs
ra ho
tu e(
re
(°C Tim
)

Figure 1 Response surface plots showing effects of citronella oil with different (a) drying times and
concentrations, (b) temperatures for heat curing and concentrations and (c) temperatures
and drying times on zero mould growth (PZMG) on rubberwood surface

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Journal of Tropical Forest Science 28(1): 39–47 (2016) Jantamas S et al.

oil. Higher heat curing temperature (> 90 °C), et al. 2008). At (4) 1656 cm-1, the band was
also showed decrease in A. flavus (Table 3). attributed to C-O stretching bands and the
Mild temperatures (60–70 °C) were reported bands at (5) 1360 to 1460 cm-1 were associated
to enhance the effect of essential oil (Ait- with C-H deformation in lignin, cellulose and
Ouazzou et al. 2011, Matan et al. 2013). Low hemicelluloses groups (Kartal et al. 2013).
concentrations of three commercial citrus fruit The position of (6) 1226 cm-1corresponded to
essential oils (orange, lemon and mandarin aromatic phenol C-O stretching. Bands in the
from Spain) at 0.2 µL mL -1 in combination (7) 900–1180 cm-1 region were associated with
with heat treatment for 10 min at 54 °C were C-O-C stretching and C-O ester bond stretching
reported to show synergistic lethal effects of (structure of glycosidic linkage) of cellulose,
bacteria (Enterococcus faecium, Staphylococcus hemicelluloses and lignin groups (Cao & Tan
aureus, Pseudomonas aeruginosa and Salmonella 2004). In addition, after rubberwood was treated
enteritidis) (Espina et al. 2011). Therefore, the with citronella oil (50 µg mL-1, 90 °C, for 1 hour)
results from this study were in agreement with after both the first day and 90th day of storage,
other reports. Curing citronella oil between slight changes in absorbance and a pattern of
30–90 °C can be utilised together with wood spectra were observed compared with the control.
drying in factories because temperatures in Treated rubberwood had slight decrease in the
kiln dryers are normally 70–90 °C. On the other amplitude of some bands (4 and 7). However,
hand, higher temperature can decrease the the peaks occurring in citronella oil were not
stability of some essential oils and components. found in treated rubberwood. The disappearance
For example, the retention of cinnamaldehyde of a dominant FTIR peak of citronella oil on
(main component of cinnamon oil) decreased treated rubberwood might be associated with the
to 17.4% after incubation at 100 °C for 8 hours incubation of treated rubberwood at 50 °C for
(Yeh et al. 2013). 1 hour. High temperature affects essential oil
Concentration of citronella oil is significant content and its components (Argyropoulos
to A. flavus inhibition. A concentration of & Müller 2014). From these results, it can be
citronella oil at 0.5% (v v-1) was threshold in hypothesised that treatment of rubberwood
killing the conidia of A. niger (Li et al. 2013). In a using citronella oil with incubation at 90 °C for
medium containing 0.5 to 2.0% citronella oil, it 1 hour may induce either the incorporation of
was found that no mould survived after 10 days. In some citronella oil derivative into rubberwood
this experiment, at concentration of 50 mg mL-1 surface or change the surface structure, resulting
(and with heat curing), citronella oil reduced the in an increase of antifungal activity.
amount of A. flavus on rubberwood surface by
five times for at least 90 days. Therefore, using Possible mode of action
a concentration of citronella oil at 50 mg mL-1
on rubberwood products may be acceptable. Microscopy (Figures 3a and b) and wettability
measurement (during storage) results showed
FTIR spectra that the spores of A. flavus could not germinate
for at least 90 days on the rubberwood surface
The FTIR spectra of untreated rubberwood and after using heat curing at 90 °C for 1 hour
rubberwood treated with citronella oil are shown with 50 µg mL-1 of citronella oil when kept
in Figure 2. Generally, rubberwood without at accelerated conditions (100% RH, 25 °C).
citronella oil (control) showed characteristic Although reversible growth of spores of A. flavus
absorption of (1) around 3000–3700 cm -1, on rubberwood surface could be observed,
attributed to the hydroxyl groups in the phenolic the spores were not able to germinate on
and aliphatic structures. Bands at (2) around treated specimens. Results from the wettability
2850 and 2920 cm -1 predominantly arose test suggested that there was no significant
from the stretching of methyl and methylene change in the contact angle between treated
groups of cellulose and lignin. The band at (14 ± 2°) and control rubberwood (13 ± 2°).
(3) 1740 cm-1 was caused by C=O stretching While hydrophobicity is one of the important
in unconjugated ketones, carbonyls and ester characteristics of essential oil, results from
groups of the carbohydrate origin (Bodirlău this study demonstrate that water can be

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Journal of Tropical Forest Science 28(1): 39–47 (2016) Jantamas S et al.

Table 3 Full factorial design (33) matrix with experimental values of period with zero mould growth
(PZMG) on rubberwood surface (days)

Run Uncoded process variable PZMG (days)

Concentration (%) Time (min) Temperature (°C) Aspergillus
(X1) (X2) (X3) flavus
1 10 1 30 3
2 10 12 30 3
3 10 24 30 3
4 10 1 90 3
5 10 12 90 3
6 10 24 90 3
7 10 1 150 3
8 10 12 150 3
9 10 24 150 3
10 30 1 30 3
11 30 12 30 7
12 30 24 30 20
13 30 1 90 45
14 30 12 90 7
15 30 24 90 7
16 30 1 150 7
17 30 12 150 3
18 30 24 150 3
19 50 1 30 90
20 50 12 30 90
21 50 24 30 90
22 50 1 90 90
23 50 12 90 90
24 50 24 90 90
25 50 1 150 45
26 50 12 150 45
27 50 24 150 45
28 30 12 90 7
29 30 12 90 7
30 30 12 90 7
31 30 12 90 7

absorbed into treated specimens. Therefore, while citronellol indicated an increase. The
no hydrophobic effect from citronella oil was change of main citronella oil components in
found. Based on the components of citronella heat curing to create a new compound and/
oil, citronellal and geraniol were found to or a minor component synergic effect would
be significant. However, in heat curing, both be possible to enhance the effect of citronella
components could be changed according to oil on mould growth. A synergy of the minor
FTIR results. Furthermore, Argyropoulos and essential oil components during heat curing
Müller (2014) found that the percentage of was also reported by Matan et al. (2013). In
citronellal and geranial in lemon balm leaves addition, Li et al. (2013) hypothesised that
decreased when using hot-air drying at 60 °C, citronella oil could destroy the A. niger hypha

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Journal of Tropical Forest Science 28(1): 39–47 (2016) Jantamas S et al.

citronella oil

rubberwood + citronella oil (90 days)

rubberwood + citronella oil (1 day)

rubberwood

Wavenumber cm-1

Figure 2 Fourier transform infrared spectra of rubberwood treated with and without
citronella oil (50 µg mL-1, 90 °C for 1 hour)

Spore

(a) (b)

Figure 3 Spores of Aspergillus flavus observed on the surface of rubberwood treated with
50 µg mL-1 of citronella oil at 90 °C for 1 hour on the (a) 90th day and (b)
mycelium of A. flavus on rubberwood without citronella oil on the third day

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Journal of Tropical Forest Science 28(1): 39–47 (2016) Jantamas S et al.

cell walls and then act on the sporoplasm to kill Espina L, Somolinos M, Lorán S, Conchello P, García
the conidia. This result also confirmed that no D & Pagán R. 2011. Chemical composition
spore germination was found after 90 days of of commercial citrus fruit essential oils and
evaluation of their antimicrobial activity acting
storage of treated rubberwood. alone or in combined processes. Food Control 22:
896–902.
CONCLUSIONS Grace JK, Byrne A, Morris PI & Tsunoda K. 2006.
Performance of Borate-Treated Lumber After 8 Years in
The change of some components in citronella an Above-Ground Termite Field Test in Hawaii. IRG/WP
06-30390. International Research Group, Stockholm.
oil during heat curing could have significant
Jaroenkit P, Matan N & Nisoa M. 2011. In vitro and in vivo
impact on germination of A. flavus. Citronella oil activity of citronella oil for the control of spoilage
could be used to increase PZMG under efficient bacteria of semi dried round scad (Decapterus
incubation conditions. The increased antifungal maruadsi). International Journal of Medicinal and
activity of citronella oil after heat curing at the Aromatic Plants 1: 234–239.
concentrations studied had fungistatic effect Kartal SN, Aysal S, Terzi E, Yılgör N, Yoshimura T &
Tsunoda K. 2013. Wood and bamboo-PP composites:
inhibiting only spore germination. fungal and termite resistance, water absorption, and
FT-IR analyses. BioResources 8: 1222–1244.
ACKNOWLEDGEMENTS Lesar B, Budija F, Kralj P, Petrič M & Humar M. 2012.
Leaching of boron from wood impregnated with
This study was supported by the Research Center preservative solutions based on boric acid and
liquefied wood. European Journal of Wood and Wood
of Excellence in Wood Science and Engineering, Products 70: 365–367.
the Institute of Research and Development of Li WR, Shi QS, Ouyang YS, Chen YB & Duan SS.
Walailak University and the Thailand Research 2013. Antifungal effects of citronella oil against
Fund (Grant no. MRG555E090). Aspergillus niger ATCC 16404. Applied Microbiology
and Biotechnology 97: 7483–7492.
Matan N & Matan N. 2012. Waterborne paints modified
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