Anti Fungal Potential of Essential Oil and Various Organic

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APPLIED MICROBIAL AND CELL PHYSIOLOGY

Antifungal potential of essential oil and various organic

extracts of Nandina domestica Thunb. against skin infectious

fungal pathogens

Vivek K. Bajpai & Jung In Yoon & Sun Chul Kang

Received: 2 March 2009 /Revised: 16 April 2009 /Accepted: 18 April 2009 /Published online: 5 May 2009# Springer-Verlag 2009

Abstract This study was undertaken to assess the in vitro

antifungal potential of the essential oil and n-hexane,

chloroform, ethyl acetate, and methanol extracts of Nandina

domestica Thunb. against dermatophytes, the casual agents

of superficial infections in animals and human beings. The

oil (1,000 g/disc) and extracts (1,500 g/disc) revealed

31.168.6% and 19.255.1% antidermatophytic effect

against Trichophyton rubrum KCTC 6345, T. rubrum

KCTC 6375, T. rubrum KCTC 6352, Trichophyton menta-

grophytes KCTC 6085, T. mentagrophytes KCTC 6077, T.

mentagrophytes KCTC 6316, Microsporum canis KCTC

6591, M. canis KCTC 6348, and M. canis KCTC 6349,

respectively, along with their respective minimum inhibito-

ry concentration values ranging from 62.5 to 500 and 125

to 2,000 g/ml. Also, the oil had strong detrimental effect

on spore germination of all the tested dermatophytic fungi

as well as concentration and time-dependent kinetic

inhibition of T. rubrum KCTC 6375. The present results

demonstrated that N. domestica mediated oil and extracts

could be potential sources of natural fungicides to control

certain important dermatophytic fungi.

Keywords Nandina domestica Thunb. .

Antifungal potential . Essential oil . Organic extracts .

Skin infectious fungal pathogens

Introduction

The incidence of dermatophytic infections has increased

considerably during the past decades. Dermatophytes are

responsible for serious human pathogenic disorders in

various parts of the world and, although control measures

are available, they are of limited effectiveness (Iwata1992).

The advent of HIV infection and immunosuppression

induced for organ transplants or by cancer chemotherapy

lead to increased pre-disposition to fungal infections (Walsh

et al. 2004). Also, the abuse of the antibiotics has resulted

in the development of drug resistance to fungal pathogens.

This is why fungal infections are the higher prevalence of

risk factors for the patients in hospital (Grewe et al. 1998).

As a result, work on alternative approaches to control such

pathogens is important. Dermatophytoses, considered as

zoonosis, have created more public health concerns due to

the close contact between humans, particularly children,

and animals. The clinical symptoms may not pose a serious

threat; however, effective treatment is usually costly and

time-consuming since the increasing resistance incidence in

known fungal pathogens to the currently available anti-

biotics has become apparent (Ghannoum and Rice 1999;

Neely and Ghannoum 2000). Also, conventional antifungal

agents such as chlorhexidine and imidazole derivatives

have limited uses in the pregnant and the young due to their

common side effects such as hepatotoxicity, nausea,

diarrhea, and impotency (Curtis 1998). Besides, the

mycotoxins produced by such fungal pathogens are the

most dangerous, and about 4.5 billion people in underde-

veloped countries are exposed to the deleterious effects of

such pathogens (Hawksworth et al. 2008). Some synthetic

fungicides can also cause environmental pollution owing to

their slow biodegradation in the environment.

Appl Microbiol Biotechnol (2009) 83:11271133

DOI 10.1007/s00253-009-2017-5

V. K. Bajpai : J. I. Yoon : S. C. Kang (*)Department of Biotechnology, College of Engineering,

Daegu University,

Kyoungsan, Kyoungbook 712-714, Republic of Korea

e-mail: [email protected]


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Resistance to traditional fungicides, the limitation of the

number of fungicides allowed for dermal application, and

increasing public concern regarding skin infectious fungal

diseases have also increased the need for the development of

new safe and biodegradable alternatives (i.e., the so-called

natural fungicides). Thus, there has been a growing interest

on the research of the possible use of natural products such as

plant-based essential oils and extracts, which can be relatively

less harmful for disease control and environmental pollution.

Moreover, antifungal substances from plant essential oils

and extracts have been investigated extensively to achieve

higher levels of human safety standards (Baker et al. 1989).

The screening of such natural products should offer

potential resources since their use in various industries of

applied microbiology and biotechnology including medical

mycology is widespread, with much of the research

population relying on them.

Nandina domestica (heavenly bamboo or sacred bam-

boo) is a suckering shrub in the barberry family, Berber-

idaceae; it is a monotypic genus, with this species as its

only member. It is native to eastern Asia from the

Himalaya, east to Japan. Despite the common name, it is

not a bamboo at all. It is an erect shrub growing to 2 m tall,

with numerous, usually, unbranched stems growing from

the roots. The leaves are evergreen; however, in spring, the

leaves are brightly colored pink to red before turning green.

The flowers are white, borne in early summer in conical

clusters held well above the foliage. It is widely grown in

gardens as an ornamental plant; over 60 cultivars have been

named. It has become naturalized in parts of eastern North

America. In the Southeastern United States, it is considered

by many as a pest due to its invasive nature.

Previously, we reported the chemical composition and

antimicrobial properties of the essential oil and various organic

extracts of N. domestica against foodborne/spoilage bacteria

and plant pathogenic fungi (Bajpai et al. 2008a, b). In the

present investigation, we assessed the antidermatophytic

potential of essential oil and various organic extracts of N.

domestica against nine skin infectious fungal pathogens.

Materials and methods

Fungal pathogens (dermatophytes)

The fungal pathogens used in this study were Trichophyton

rubrum KCTC 6345, T. rubrum KCTC 6375, T. rubrum

KCTC 6352, Trichophyton mentagrophytes KCTC 6085, T.

mentagrophytes KCTC 6077, T. mentagrophytes KCTC

6316, Microsporum canis KCTC 6591, M. canis KCTC

6348, and M. canis KCTC 6349, which were obtained from

the Korean agricultural culture collection, Suwon, Republic

of Korea. All the strains were maintained on Sabourauds

agar (SBA, Difco, MI, USA) at 4C.

Preparation of the spore suspension and test sample

The fungal pathogens were grown on SBA plates in the

dark at 282C for 79 days, after which time, spores were

harvested from sporulating colonies and suspended in

sterile distilled water containing 0.1% (v/v) Tween 20.

The concentration of spores in suspension was determined

using a hematocytometer and adjusted to 1.0108spores/ml

for each fungal pathogen.

To prepare the test solutions, essential oil and n-hexane,

chloroform, ethyl acetate, and methanol extracts were

dissolved in 5% dichloromethane, and the solvents (n-

hexane, chloroform, ethyl acetate, and methanol) used for

extraction, respectively, to prepare the stock solutions

with their respective known weights, which were further

diluted with their respective 5% solvent to prepare test

samples, where the final concentration of the solvent was

0.5% (v/v).

In vitro antidermatophytic activity assay

The in vitro antidermatophytic activity of essential oil and

the extracts (n-hexane, chloroform, ethyl acetate, and

methanol) was assessed by disc diffusion method using

SBA in 9-cm petri dishes (Duru et al. 2003). An agar plug

of fungal inoculum (6 mm in diameter) was removed

from a 10-day-old previous culture of all the fungal

pathogens tested and placed upside down in the center of

the SBA plate. Two sterile Whatman paper discs of

6 mm diameter with essential oil (1,000 g/disc),

controls (dichloromethane), extracts (1,500 g/disc), and

controls (n-hexane, chloroform, ethyl acetate, and meth-

anol) were pierced in the agar, equidistant in SBA plate

separately. The plates were incubated at 28 2C for 7

9 days until the growth in the control plates reaches the

edges of the plates. The assays were carried out in

triplicate. The relative growth inhibition of treatments

relative to control was calculated by percentage using the

following formula:

Inhibition % 1 radial growth of treatment mm =radial growth of control mm f g 100:

1128 Appl Microbiol Biotechnol (2009) 83:11271133


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In vitro antidermatophytic susceptibility assay

The in vitro susceptibility of dermatophytes was determined

by minimum inhibitory concentration (MIC) determination

method (Murray et al. 1995). The MICs of essential oil and

extracts were determined by twofold serial dilution against

the fungi tested. Essential oil and extracts (4 l each) were

dissolved in the same solvent employed to isolate and

extract the essential oil and organic extracts, respectively,

which were further serially diluted with their respective 5%

solvent (dichloromethane, n-hexane, chloroform, ethyl

acetate, and methanol) and were added to Sabourauds

broth (SDB) at final concentrations of 31.25, 62.5, 125,

250, 500, 1,000, 2,000, and 4,000 g/ml, respectively. A

10-l spore suspension (1.0 108spores/ml) of each test

pathogen was inoculated in the test tubes in SDB medium

and incubated at 282C for 2 to 7 days. The control tubes

containing SDB medium were inoculated only with fungal

spore suspension. The minimum concentrations at which no

visible growth was observed were defined as the MICs,

which were expressed in microgram/milliliter.

Spore germination assay

For spore germination assay of the nine human fungal

pathogens, test samples of oil (4 l) were dissolved in 5%

dichloromethane to obtain 31.25, 62.5, 125, 250, 500,

1,000, 2,000, and 4,000 g/ml concentrations of the oil,

where the final concentration of the solvent was 0.5%

(Leelasuphakul et al. 2008). The samples were inoculated

with spore suspension of each fungal pathogen containing

1.0108spores/ml. From this, aliquots of 10-l spore

suspension from each were placed on separate glass slides

in triplicate. Slides containing the spores were incubated in

a moisture chamber at 28C for 4 h. Each slide was then

fixed in lactophenol cotton blue and observed under the

microscope for spore germination. The spores-generated

germ tubes were enumerated, and percentage of spore

germination was calculated. Dichloromethane (0.5%), as a

control, was tested separately for spore germination of the

fungi.

In vitro growth kinetics assay

T. rubrum KCTC 6375, which appeared to be the more

resistant fungus as compared to T. mentagrophytes KCTC

6085 and M. canis KCTC 6348 to the essential oil in spore

germination assay, was chosen as the test fungus for kinetic

study and evaluation of antidermatophytic potential of

essential oil (Rana et al. 1997). A 10-l spore suspension

(1.0108spores/ml) of this fungal pathogen was inoculated

to different concentrations of essential oil (31.25, 62.5, 125,

and 250 g/ml) in a test tube, and a homogenous

suspension was made by inverting the test tubes three to

four times. After the specific intervals, i.e., 30, 60, 90, 120,

150, and 180 min, the reaction mixture was filtered through

Whatman No. 1 filter paper, and the retained spores were

washed two or three times with sterile distilled water. The

filter was then removed, and spores were washed off into

10 ml of sterile distilled water. From this, 100 l of spore

suspension was taken onto the glass slide and incubated at

282C for 24 h. The spores-generated germ tubes were

enumerated, and percentage of spore germination was

calculated. Control sets were prepared in 0.5% dichloro-

methane with sterile distilled water. All experiments were

conducted in triplicate.

Statistical analysis

The data obtained in this study were evaluated using the

one-way analysis of variance test, followed by Students t

test. Significant levels were considered at P


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Determination of minimum inhibitory concentrations

The MICs, defined as the lowest concentrations of the

essential oil that resulted in complete growth inhibition of

the tested fungi, were found to be 62.5500 g/ml. T.

rubrum KCTC 6352, T. mentagrophytes KCTC 6085, T.

mentagrophytes KCTC 6077, and M. canis KCTC 6348

were found to be the most susceptible fungal pathogens to

the essential oil of N. domestica. Methanol, ethyl acetate,

and chloroform extracts also displayed potential effect of

antidermatophytic activity as MICs against the tested fungal

pathogens, with their respective MIC values ranging from

250 to 1,000, 125 to 1,000, and 500 to 2,000 g/ml

(Table 3). As control, each 5% solvent (dichloromethane, n-

hexane, chloroform, ethyl acetate, and methanol) did not

affect the growth of the sample strains in this study.

However, mild to moderate antidermatophytic effect

(1,000 to 2,000 g/ml) of hexane extract was observed

against the tested fungal pathogens as a MIC.

Spore germination

The results obtained for essential oil from the spore

germination assay of each of the test fungal pathogens are

shown in Fig. 1. Dichloromethane (0.5%, v/v), as a control,

did not inhibit the spore germination of any of the fungal

pathogens tested. The essential oil significantly inhibited

the fungal spore germination at the varied concentrations

(31.251,000 g/ml). A 100% inhibition of fungal spore

germination was observed for T. mentagrophytes KCTC

6085, M. canis KCTC 6348, and T. rubrum KCTC 6375 at

250, 250, and 500 g/ml concentrations of essential oil,

respectively. The oil also exhibited a potent inhibitory

effect on the spore germination of T. rubrum KCTC 6345,

T. rubrum KCTC 6352, T. mentagrophytes KCTC 6316, T.

mentagrophytes KCTC 6077, M. canis KCTC 6591, and M.

canis KCTC 6349 in the range of 40% to 90% at

concentrations ranging from 250 to 1,000 g/ml.

Growth kinetics

The antidermatophytic kinetics of the essential oil againstT.

rubrum KCTC 6375 is shown in Fig. 2. Exposure of T.

rubrum KCTC 6375 spores to different concentrations of

the essential oil for a period of 0 to 180 min caused varying

degree of inhibition of spore germination. An increase in

fungicidal activity was observed with increase in exposure

time and concentration. The essential oil at 31.25 and

62.5 g/ml showed antifungal activity but not rapid killing,

and about 40% to 50% inhibition was observed at exposure

time of 120 min. However, there was a marked increase in

the killing rate at 125 and 250 g/ml after 60 min of

exposure, and 90% to 100% inhibition of spore germination

was observed on 180 min exposure.

Discussion

The increasing health implications caused by human

infectious fungal pathogens means there is a need to

develop safe and new natural antifungal agents that could

be used in the field of medical mycology to cure human

fungal disorders. The estimated lifetime risk of acquiring a

dermatophyte infection is between 10% and 20%. Essential

oils and extracts from plant species have long been used for

treatment of various diseases, including skin conditions,

and there is at least some evidence that natural products

may tend to have less deleterious side effects than

corresponding synthetic drugs (Tavares et al. 2008). In

general, plant-derived essential oils and extracts are

considered as non-phytotoxic compounds and potentially

effective against several microorganisms including fungal

and bacterial pathogens (Pandey et al. 1982; Chung et al.

Table 1 Antidermatophytic activity of essential oil (1,000 g/disc) of

Nandina domestica Thunb. against human infectious fungal pathogens

Fungal pathogen Essential oila MICd

Radial growth

(mm)bRadial growth

inhibition (%)c

Trichophyton rubrum

KCTC 6345

31.03 0.56 31.10 0.15e 500

Trichophyton rubrum

KCTC 6375

21.36 0.57 53.00 0.27e 125

Trichophyton rubrum

KCTC 6352

17.53 0.37 61.10 1.15e 62.5

Trichophyton

mentagrophytes

KCTC 6085

16.26 0.30 63.90 0.25 62.5

Trichophyton

mentagrophytes

KCTC 6077

14.16 0.57 68.60 2.51 62.5

Trichophyton

mentagrophytes

KCTC 6313

21.40 0.20 52.50 2.10e 125

Microsporum canis

KCTC 6591

21.66 0.30 51.90 1.25e 125

Microsporum canis

KCTC 6348

16.86 0.11 62.60 0.15e 62.5

Microsporum canis

KCTC 6349

20.90 0.60 53.60 2.20e 125

Solvent (dichloromethane) as negative control (radial growth diameter

450.0 for each fungal strain) had no antifungal effectaEssential oil (tested volume 1,000 g/disc)b Radial growth of fungal pathogensc Radial growth inhibition percentaged Minimum inhibitory concentration (values in microgram/milliliter)e Values are given as meanSD (n =3) and considered to be

significantly different at P


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2007). Therefore, they can be used as a natural therapy

against superficial human fungal infections caused by

dermatophytes.

Since ancient times, interests have been focused on the

development of safer antifungal agents to control severe

fungal diseases by the essential oils and extracts (Chung et

al. 2007; Prasad et al. 2004). Previously our research group

and other researchers have documented the antifungal

properties of various plant essential oils and extracts

(Bajpai et al. 2009; Tavares et al. 2008; Yousef and Tawil

1980).

In the present study, the hydrodistillated essential oil

isolated from the floral parts of N. domestica consisted of

mono- and sesquiterpenes, and mono- and sesquiterpene

hydrocarbons (Bajpai et al. 2008b). In recent years, several

researchers have reported the mono- and sesquiterpenes,

and mono- and sesquiterpene hydrocarbons as the major

components of essential oils of plant origin, which have

enormous potential to strongly inhibit the microbial

pathogens (Cakir et al. 2004). In general, the active

antimicrobial compounds of essential oils are phenolic

terpenes such as thymol and carvacrol; it would seem

reasonable that their antifungal mode of action might be

related to that of other compounds. Most of the studies on

the mechanism of phenolic compounds have focused on

their effects on cellular membranes. Actually, phenolic

compounds not only attack cell walls and cell membranes,

thereby affecting the permeability and release of intracellu-

lar constituents, but they also interfere with membrane

Table 3 Determination of minimum inhibitory concentration of

various organic extracts of Nandina domestica Thunb. against human

infectious fungal pathogens

Fungal pathogen MIC

HXE CHE ETE MNE

Trichophyton rubrum

KCTC 6345

2,000 2,000 500 1,000

Trichophyton rubrum

KCTC 6375

1,000 500 500 500

Trichophyton rubrum

KCTC 6352

2,000 500 125 500

Trichophyton mentagrophytes

KCTC 6085

2,000 500 250 500


KCTC 6077

1,000 500 250 250


KCTC 6313

2,000 1,000 500 500

Microsporum canis KCTC 6591 2,000 500 500 1,000

Microsporum canis KCTC 6348 1,000 500 250 250

Microsporum canis KCTC 6349 2,000 1,000 1,000 1,000

Solvents (hexane, chloroform, ethyl acetate, and methanol) as negative

controls had no antifungal effect

Values are given as meanSD (n=3)

MIC minimum inhibitory concentration (values in microgram/millili-

ter), HXE hexane extract, CHE chloroform extract, ETE ethyl acetate

extract, MNE methanol extract

Table 2 Antidermatophytic activity of organic extracts (1,500 g/disc) of Nandina domestica Thunb. against human infectious fungal pathogens

Fungal pathogen Radial growth inhibition

HXE CHE ETE MNE

Millimetera Percentb Millimeter Percent Millimeter Percent Millimeter Percent

Trichophyton rubrum KCTC 6345 36.7 1.1 19.2 2.0c 31.81.2 29.42.0c 32.7 0.5 31.41.1c 30.91.0 31.32.1c



Trichophyton mentagrophytes KCTC 6085 30.71.7 33.33.0c 22.41.1 51.22.3 24.1 1.1 47.31.5c 25.51.0 44.01.0c

Trichophyton mentagrophytes KCTC 6077 34.61.3 24.31.3c 30.71.3 32.62.5c 20.2 1.5 55.11.1 26.50.5 42.21.7c

Trichophyton mentagrophytes KCTC 6313 33.21.2 27.31.3c 26.81.5 41.23.2c 24.3 1.5 47.02.1c 32.01.0 29.12.3c

Microsporum canis KCTC 6591 35.8 1.7 22.1 1.5c 27.51.2 39.63.1c 26.3 1.6 42.01.6c 26.31.5 43.12.1c



Solvents (hexane, chloroform, ethyl acetate, and methanol) as negative controls (radial growth diameter 450.0 for each fungal strain) had no

antifungal effect

HXE hexane extract, CHE chloroform extract, ETE ethyl acetate extract, MNE methanol extract

aRadial growth of fungal pathogensb Percentage of radial growth inhibitionc Values are given as meanS.D. (n=3), and considered to be significantly different at P


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function. Thus, active phenolic compounds might have

several invasive targets, which could lead to the inhibition

of human infectious fungal pathogens.

In the present study, the essential oil of N. domestica

showed potential antidermatophytic effect against the tested

human infectious fungal pathogens. This research work also

describes the complex effect of the oil on fungal sporegermination and exhibited a wide range of antidermatophytic

activity. During the kinetic study of T. rubrum KCTC 6375,

it appeared that the exposure time of the oil had a little

effect on the fungicidal activity at lower concentration, but

at the concentration of 125 and 250 g/ml, the fungicidal

action was very rapid and showed 90% to 100% spore

germination inhibition of T. rubrum KCTC 6375. The

activities of the oil could be attributed to the presence of

major components of the oil such as 1-indolizino carbazole,

2-pentanone, monophenol, azridine, methylcarbinol, etha-

none, furfural, 1-hydroxy-4-methylbenzene, 2(5H)-fura-

none, and 3,5-dimethylpyrazole (Bajpai et al., 2008a), andthese findings are in agreement with previous research

literature reported by others (Tavares et al. 2008; Chung et

al. 2007). Also, the results of the antifungal screening

showed that methanol, ethyl acetate, and chloroform

extracts of the plant sample have potential antidermato-

phytic effect against some of the tested fungal pathogens.

This antidermatophytic effect might be exerted due to the

presence of several bioactive compounds in various extracts

of N. domestica as evident by the findings of others (Urzua

and Mendoza 1998; Perry and Foster 1994). Further, as

shown in Table 1, the essential oil showed potential

antidermatophytic effect in case of T. rubrum KCTC

6352, T. mentagrophytes KCTC 6085, T. mentagrophytes

KCTC 6077, and M. canis KCTC 6348, with MIC value of62.5 g/ml for each fungal pathogen. Earlier papers on the

analysis and antifungal properties of the essential oils of

some species have shown that they have a varying degree

of antidermatophytic effects against some of the human

infectious fungal pathogens due to their different chemical

compositions (Tavares et al. 2008; Chung et al. 2007). In

this study, it has become clear that the essential oil and

extracts of N. domestica have great potential to strongly

inhibit the members of the Trichophyton and Microsporum

species causing certain superficial fungal infections of the

skin known as tinea infections such as tinea capitis, tinea

pedis, tinea corporis, and onychomycosis. However, fromsome plant oils such as wintergreen, eucalyptus, clove, and

sage, there has been much research and reporting of toxic

and irritant properties (Lawless 1995; Newall et al. 1996;

Reynolds 1996). In spite of this, most of these oils are

available for purchase as whole oils or as a part of

pharmaceutical or medicinal products, indicating that toxic

properties do not prohibit their use.

Fig. 2 Kinetics of inhibition ofTrichophyton rubrum KCTC 6375 spores by the essential oil of Nandina domestica Thunb. *Values are given as

meanSD (n=3) and considered to be significantly different at P


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In addition, certain plant essential oils, extracts, and

phytochemicals act in many ways on various types of

disease complex and may potentially contribute in the field

of applied microbiology and biotechnology including

medical mycology as the supplement to control human

pathogenic fungi in the future as fast and reliable

alternatives. The development of natural antifungal agents

would also help to decrease the negative impact of synthetic

agents such as residues, resistance, and environmental

pollution. In this respect, natural fungicides may be

effective, selective, biodegradable, and less toxic to the

environment. On the other hand, the use of plant essential

oils in consumer goods is expected to increase in the future

due to the risk of green consumerism, which stimulates

the use and development of products derived from plants,

as both consumers and regulatory agencies are more

comfortable with the use of natural antimicrobials (Tuley

de Silva 1996). The results obtained in this study

potentially suggested that N. domestica can be used as a

leading factor in a wide range of activities. Thus, it can be

concluded that its essential oil and crude extracts could be

used as a potential source of natural antidermatophytic

agents to control dermatophytic fungi, which cause super-

ficial fungal infections in human beings. However, the

effect of external conditions on chemical composition of

plants has been recognized for more than 90 years. The

environment affects the essential oil composition directly

through metabolic processes and indirectly through plant

growth. The total accumulation depends upon the genetic

composition of the plant, and it varies between genera and

species. Within a species itself, altering the environmental

and genetic composition will produce different quantities

and types of essential oil (Bernath and Tetenyi 1978). Thus,

further study would be conducted on the effect of genetic

and environmental factors on the chemical composition

and the toxic or irritant properties of N. domestica

essential oil.

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Anti Fungal Potential of Essential Oil and Various Organic