Journal of Food Processing and Preservation ISSN 1745-4549

CHEMICAL CONSTITUENTS, ANTIMICROBIAL AND

ANTIOXIDATIVE EFFECTS OF TRACHYSPERMUM AMMI
ESSENTIAL OIL
HASSAN GANDOMI1, SEPIDEH ABBASZADEH2,5, ASHKAN JEBELLIJAVAN3 and AGHIL SHARIFZADEH4
1
Department of Food Hygiene, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
2
Nutrition and Food Hygiene, Baqiyatallah University of Medical Sciences, Tehran, Iran
3
Department of Food Hygiene, Faculty of Veterinary, University of Semnan, Semnan, Iran
4
Mycology Research Center, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran

5
Corresponding author. ABSTRACT
TEL: +98-21-6111-7074;
FAX: +98-21-6693-3222; The chemical composition of Trachyspermum ammi essential oil (EO) was ana-
EMAIL: abbaszadehs@bmsu.ac.ir lyzed by gas chromatography–mass spectrometry, and thymol (63.4%), p-cymene
(19%) and g-terpinene (16.9%) were found as the major components. The anti-
Received for Publication February 17, 2013
microbial properties of the EO were investigated against 10 important foodborne
Accepted for Publication May 3, 2013
pathogenic bacteria and spoilage fungi by disk diffusion and by determining the
doi:10.1111/jfpp.12131 minimum inhibitory concentration (MIC). The EO exhibited strong activity
against both bacteria and fungi, with greater inhibition of bacterial growth com-
pared with fungi; MIC value of EO against all bacteria was evaluated at 500 ppm,
whereas the fungal species were inhibited at concentrations of 1000–2000 ppm.
The EO also showed antioxidant activity assessed by 2,2-diphenyl-1-
picrylhydrazyl, with IC50 (concentration providing 50% inhibition) of 34 mg/mL.
Similarly, in b-carotene/linoleic acid assay, the EO was effectively able to inhibit
the linoleic acid oxidation, exhibiting 82.16% inhibition that was similar to buty-
lated hydroxytoluene. Overall, the EO exhibit potent antimicrobial and antioxi-
dant activity, which supports its potential use for perishable and high fatty foods.

PRACTICAL APPLICATIONS
This study is the first report of the chemical composition of Iranian Trachysper-
mum ammi essential oil and its antimicrobial and antioxidant activities. In conclu-
sion, the obtained data indicate that the essential oil exhibits potent antibacterial
and antifungal activity, which supports its use in traditional medicine for its anti-
septic properties. The results clearly show that the oil of T. ammi presents antioxi-
dant activity and might be useful for high fatty foods.

Antioxidants are known as molecules capable of inhibiting

INTRODUCTION
oxidation process in food and body (Sikorski 2001). Appli-
It has been estimated that as many as 30% of people in cation of some synthetic antioxidants, such as butylated
industrialized countries suffer from a foodborne disease hydroxytoluene (BHT) and butylated hydroxyanisole
each year, and in 2000, at least two million people died from (BHA), is known to be associated with some malignancies,
diarrheal disease worldwide (WHO 2002). Some bacteria hepatic damages and toxicities in laboratory animals
and molds grow and release their own enzymes into the (Al-Reza et al. 2009; Hwang et al. 2001).
liquid surrounding them, and absorb the products of exter- In recent years, development of antibiotic resistance and
nal digestion. This is the main basis of microbial food spoil- negative consumer perception about possible toxicity and
age, which lowers its nutritional value and causes financial other side effects of chemical preservatives shift attentions
losses in food industry. Oxidative rancidity is the major toward natural alternatives. Many researchers have shown
cause of food quality deterioration, leading to the formation that secondary plant metabolites, such as essential oils
of undesirable off-flavors as well as unhealthful compounds. (EOs), can exhibit antimicrobial and antioxidant effects

1690 Journal of Food Processing and Preservation 38 (2014) 1690–1695 © 2013 Wiley Periodicals, Inc.
H. GANDOMI ET AL. AJWAN EO’S ANTIMICROBIAL AND ANTIOXIDATIVE EFFECTS

(Carmo and Souza 2010; Gandomi et al. 2009; Khosravi and held for 20 min. Helium was used as the carrier gas at a
et al. 2011; Pires et al. 2011). These properties are due to the flow rate 1.0 mL/min. The compounds of the oil were iden-
many active phytochemicals including flavonoids, terpe- tified by comparing their retention indices (RIs) and mass
noids, carotenoids, coumarins and curcumines (Koleva and spectra fragmentation with those on the stored Wiley 7 n.1
Vanbeek 2001, Singh et al. 2004). Moreover, the potential Mass Computer Library.
use of EOs as additives to improve food preservation has
been researched in several studies (Bei et al. 2011; Gandomi
Antimicrobial Activity
et al. 2009; Lima 2006; Mahboubi and Kazempour 2011;
Saei-Dehkordi et al. 2010). Trachyspermum ammi, com- Microbial Strains. The activity of the EO was tested
monly known as Ajowan, is one of the aromatic seed spices toward 10 different foodborne pathogens: bacterial species
that originated in the Middle East, India, Iran, Afghanistan including Bacillus cereus (ATCC 11778), Staphylococcus
and Egypt. In these countries, it is traditionally used as a aureus (ATCC 6538), Listeria monocytogenes (ATCC 19118),
medicinal plant for its antiseptic, appetizer and carminative Salmonella typhimurium phagetype II and Escherichia coli
properties (Zargari 1989). Thymol, the major phenolic O157H7; and fungal species including Penicillium citrinum
compound present in Ajowan, has been reported to (PTCC 5304), Penicillium chrysogenum (PTCC 5033),
be a germicide, antispasmodic and antifungal agent Aspergillus flavus (ATCC 15546), Aspergillus niger (ATCC
(Nagalakshmi et al. 2000). 16404) and Aspergillus parasiticus (PTCC 5286). Bacterial
The purpose of this study was to assess the chemical and fungal strains were maintained on brain–heart infusion
composition and antimicrobial effects of Ajowan EO (BHI) agar and potato dextrose agar (PDA) slants, respec-
against important foodborne pathogenic bacteria and food tively, and stored at 4C.
spoilage fungi, as well as its antioxidative properties for its
potential use as a natural food additive. Preparation of Inocula. Bacterial inocula were prepared by
inoculating a loopful from slant culture in BHI broth which
was incubated for 18 h at 35C. Second subcultures were
MATERIALS AND METHODS prepared in the same condition. Bacterial suspension was
adjusted to an optical density of 0.1 at 600 nm, using a
Plant Material Spectronic 20 spectrophotometer (Milton Roy Company,
Seeds of T. ammi were collected in July 2011 from Isfahan, Warminster, PA) and enumerated by duplicate plating from
Iran. Plants were taxonomically identified at the Pharma- tenfold serial dilutions on BHI agar and counting the colo-
cognosy Department, Faculty of Pharmacy, University of nies after 24 h of incubation at 35C. Fungal strains were
Tehran, Iran. The seeds were thoroughly washed and dried grown on PDA slants at 30C for 7–10 days until sporulate.
in the shade at room temperature for 24 h. Spores were harvested by adding 10 mL of sterile distilled
water containing 0.05% Tween 20 and scraping the surface
of the culture to free the spores. The spore suspension was
Isolation of the Essential Oil counted with a hemocytometer and further diluted to give a
concentration of (1–5) ¥ 106 spores/mL.
The dried T. ammi seeds were submitted to hydrodistillation
in a Clevenger-type apparatus at 100C for 5 h. The EO was
isolated and dried over anhydrous sodium sulfate and then Determination of Microbial Susceptibility with
stored in a dark glass bottle at 4C until required. Disk Diffusion Method. The antimicrobial activity was
carried out using the disk diffusion method. T. ammi EO
(10 mL) was inoculated to 6-mm-diameter disks and placed
Chemical Composition Analysis of the on BHI agar or PDA plates inoculated with bacterial sus-
Essential Oil pension or fungal spore and incubated at 37C for 24 h and
30C for 48 h, respectively. At the end of the incubation
Gas chromatography–mass spectrometry (GC-MS) method
period, the susceptibility of the test organisms was deter-
was used for chemical composition analysis of the EO, using
mined by measuring the diagonal of the zone of inhibition
an AGILENT 6890 (Santa Clara, CA) gas chromatography
around the disk. The results given are as an average of
equipped with an AGILENT 5973 series mass selective
duplicated experiments.
detector (length, 30 m; inner diameter, 250 mm; film thick-
ness, 25 mm). The injector and selective mass detector tem-
peratures were maintained at 250 and 230C, respectively. Determination of Minimum Inhibitory Concentra-
The oven temperature program was initiated at 40C, held tion (MIC). MICs were determined using the broth
for 1 min and then raised up to 250C at a rate of 3C/min microdilution method recommended by the CLSI, with

Journal of Food Processing and Preservation 38 (2014) 1690–1695 © 2013 Wiley Periodicals, Inc. 1691
AJWAN EO’S ANTIMICROBIAL AND ANTIOXIDATIVE EFFECTS H. GANDOMI ET AL.

some modifications (Schwalbe et al. 2007). Stock solution of TABLE 1. CHEMICAL COMPONENT (%) OF THE TRACHYSPERMUM
the tested EO in sterile broth medium (RPMI 1640 for fungi AMMI ESSENTIAL OIL ANALYZED BY GAS CHROMATOGRAPHY–MASS
SPECTROMETRY
and BHI broth for bacterial pathogens) with 10% dimethyl
sulfoxide (DMSO) was prepared. Serial dilutions of the Components Rt RIa %
stock solutions in broth medium were prepared (200 mL/ Thymol 27.64 1235 63.42
well) in a 96-well microtiter plate. Then, all wells were a-Thujene 9.41 852 0.07
inoculated by 20 mL of fungal spore suspension or bacterial a-Pinene 9.64 857 0.06
culture (final fungal spore and bacterial concentration was Sabinene 11.34 899 0.44
p-Cymene 14.06 956 19.01
104 spores/mL and 5 ¥ 105 cfu/mL, respectively), and incu-
b-Ocimene X 14.12 958 0.10
bated at 37C for 24 h and 30C for 48 h, respectively. The
g-Terpinene 15.85 993 16.89
MIC was defined as the lowest concentration of the EO at Total 99.99
which the microorganism does not demonstrate visible a
The retention indices (RIs) were calculated for all volatile constituents
growth. A positive control containing the bacterial culture
using a homologous series of n-alkanes C8–C16.
and DMSO without the EO and a negative control contain- Rt, retention time.
ing only the medium were performed as well.
then 25 mL of linoleic acid (L1376-500MG, Sigma, St. Louis,
Antioxidant Activity MO) and 200 mg Tween 40 (822185, Merck) were added.
2,2-Diphenyl-1-Picrylhydrazyl (DPPH) Assay. The After the evaporation of chloroform, 100 mL of oxygen
hydrogen atom or electron donation abilities of the corre- saturated distilled water was added with vigorous shaking.
sponding EO were measured through the bleaching of the Then, 2500 mL of aliquots was dispensed into the test tubes,
purple-colored methanol solution of DPPH. This spectro- 350 mL of the EO (2 g/L) was added and the emulsion
photometric assay was carried out using the stable radical system was incubated for 48 h at room temperature. The
DPPH as a reagent according to the method of Burits same procedure was performed for both BHT (as positive
(2000). Briefly, 50 mL of various concentrations of the EO control) and blank. After this incubation period, absorbance
was added to 5 mL of the DPPH solution (0.004% metha- of the mixtures was obtained at 490 nm. Afterward, the
nol solution). After 30 min of incubation at room tempera- antioxidative capacity of the EO was compared with those
ture, the absorbance was read against pure methanol at of BHT and blank. Further, all inhibition percentages were
517 nm. The radical-scavenging activities of the samples compared using one-way analysis of variance.
were calculated as percentage of inhibition according to the
following equation: RESULTS AND DISCUSSION
I (%) = ( Ablank − Asample Ablank ) × 100 The results of the GC-MS analysis of T. ammi volatile oil are
given in Table 1. The oil was shown to contain a mixture of
where Ablank is the absorbance of the control (containing all components, mainly thymol together with a small amount
reagents except the test compound) and Asample is the absor- of other volatile compounds. Seven components were iden-
bance of the test compound. EO concentration providing tified, which represented 99.99% of the total oils. As
50% inhibition (IC50) was calculated from the linear regres- shown in Table 1, thymol (63.4%), p-cymene (19%) and
sion algorithm of the graph plotted inhibition percentage g-terpinene (16.9%) were found as the major components.
against the EO concentration using PHARM/PCS Version Some previous studies have already reported that thymol is
4 (Springer-Verlag New York Inc., New York). Values the major component of this oil. Although in our study
(mean ⫾ SD) of the EO were compared with those of BHT (Iranian species) thymol represents 63.4% of the total oil, in
using Student’s t-test. Indian species (Singh et al. 2004), it appears to represent
39%, which may reflect variations due to time of plant
growing, preparation process, cultivar differences and geo-
b-Carotene–Linoleic Acid Assay
graphical location from which the plants were collected
In this assay, the antioxidant capacity was determined by (Saei-Dehkordi et al. 2010).
measuring the inhibition of volatile organic compounds The oil was tested against 10 important food spoilage
and the conjugated diene hydroperoxides arose from microorganisms, including five pathogenic bacteria and five
linoleic acid oxidation according to the method of foodborne fungi, by a qualitative and quantitative evalua-
Dapkevicius et al. (1998). In this regard, stock solution of tion expressed in growth inhibition zone diameters and
b-carotene–linoleic acid mixture was prepared as follows: MIC values, respectively. The results of the inhibitory activi-
0.5 mg b-carotene (K15555836, Merck, Whitehouse Station, ties of EOs on the growth of bacterial species are presented
NJ) was dissolved in 1 mL of chloroform (HPLC grade)and in Table 2. As shown in the disk diffusion results, the oil was

1692 Journal of Food Processing and Preservation 38 (2014) 1690–1695 © 2013 Wiley Periodicals, Inc.
H. GANDOMI ET AL. AJWAN EO’S ANTIMICROBIAL AND ANTIOXIDATIVE EFFECTS

TABLE 2. AVERAGE INHIBITION ZONE (MM) AND MINIMUM In addition, the antioxidant activity of the EO and the
INHIBITORY CONCENTRATIONS (MIC) (PPM) OF TRACHYSPERMUM amount of EO which induced 50% inhibition (IC50) was
AMMI ESSENTIAL OIL AGAINST FIVE IMPORTANT FOODBORNE
estimated and shown in Table 4. The results indicated that
BACTERIA
an increase in T. ammi EO concentration resulted in an
Diameter of increase of the free radical-scavenging activity. In this
inhibition MIC
regard, the antiradical activity of the EO was less than that
zone (mm) (ppm)
of BHT (P < 0.05); however, T. ammi EO showed good anti-
Bacillus cereus 35 500 radical activity in DPPH assay. In the present study, the
Staphylococcus aureus 33.5 500
decrease in DPPH due to the EO (IC50: 34 mg/mL) of
Listeria monocytogenes 36 500
T. ammi was higher than that reported by Khanum et al.
Salmonella typhimurium 34 500
Escherichia coli 39 500 (2011) for the alcohol extract (around 37 mg/mL) of
T. ammi and also lower than its water extract (around
TABLE 3. AVERAGE INHIBITION ZONE (MM) AND MINIMUM
29 mg/mL) in the work mentioned.
INHIBITORY CONCENTRATION (MIC) (PPM) OF TRACHYSPERMUM It seems that the high percentage of oxygenated monoter-
AMMI ESSENTIAL OIL AGAINST FIVE IMPORTANT FOOD penes, particularly thymol, and the high level of g-terpinene
SPOILAGE FUNGI and p-cymene of T. ammi EO might be related to its high
Diameter of antiradical activity (Cao et al. 2009).
inhibition MIC The antioxidant activity of T. ammi EO determined in
zone (mm) (ppm) terms of percent inhibition in b-carotene–linoleic acid
Penicillium citrinum >80 2000 system is presented in Fig. 1. As can be seen, the EO effec-
Penicillium chrysogenum >80 2000 tively inhibited the linoleic acid oxidation as much as
Aspergillus flavus >80 2000 82.16%. In this regard, with the same concentration, the EO
Aspergillus niger >80 1000 showed higher inhibition compared with the control
Aspergillus parasiticus >80 3000 (5.83%) and similar to BHT by as much as 86.53%.
The results of this test were in good agreement with
found to be effective at a 10-mL dose and based on broth Khanum et al. (2011) on T. ammi extracts. These character-
microdilution method, the MIC of the volatile oil was istics of the T. ammi EO can be attributed to its main com-
500 ppm against all the tested bacteria (Table 2). ponents. In this regard, Cao et al. (2009) presented the
Table 3 shows the antifungal activity of T. ammi EO on oxygenated monoterpenes and monoterpene hydrocarbons
food spoilage fungi. All assayed fungi were sensitive to the
EO presenting large growth inhibition zones with a diam-
TABLE 4. IN VITRO ANTIOXIDANT ACTIVITIES OF TRACHYSPERMUM
eter of more than 80 mm using direct contact disk diffusion AMMI ESSENTIAL OIL AND BUTYLATED HYDROXYTOLUENE (BHT) IN
method at 10-mL dose (Table 3), which could be due to DPPH (2,2-DIPHENYL-1-PICRYLHYDRAZYL) ASSAY
fungi static activity of its vapor phase. The researchers
Sample IC50 (mg/mL)
believe that the antifungal activity of the vapor phase of
EOs is the result of their indirect effects on mycelium, and Essential oil 34 ⫾ 0.45
BHT 11 ⫾ 0.2
lipophilic properties of the EOs provide the opportunity to
be absorbed by mycelium (Vesaltalab and Zafari 2012). MIC Values (mean ⫾ SD) were expressed as IC50.
values were between 1000 and 3000 ppm for fungal strains.
Fungal MIC levels for T. ammi were more than that of bac-
terial strains, which may be related to different outer mem-
brane structures.
A few studies have reported that T. ammi is among the
most potent medicinal plant because of its antimicrobial
properties (Hajare and Sharma 2005; Murthy et al. 2009;
Singh et al. 2004), which have been confirmed and extended
in this study. Murthy et al. (2009) reported the inhibitory
effects of T. ammi ethanolic extract on the mycelial growth
and spore germination of toxigenic fungi Aspergillus ochra-
ceus, showing the immense antitoxigenic potential of this oil FIG. 1. ANTIOXIDANT ACTIVITY OF TRACHYSPERMUM AMMI
(Murthy et al. 2009). Previous studies showed that thymol ESSENTIAL OIL IN TERMS OF INHIBITION OF PEROXIDATION IN
has a high microbicidal and anti-aflatoxigenic effects due to LINOLEIC ACID SYSTEM
the presence of a phenolic –OH group (Farag et al. 1989). BHT, butylated hydroxytoluene.

Journal of Food Processing and Preservation 38 (2014) 1690–1695 © 2013 Wiley Periodicals, Inc. 1693
AJWAN EO’S ANTIMICROBIAL AND ANTIOXIDATIVE EFFECTS H. GANDOMI ET AL.

as the principal antioxidant compounds in the plants, and Zataria multifora Boiss. essential oil on growth and Aflatoxin
thymol, carvacrol, g-terpinene and p-cymene as the main formation by Aspergillus flavus in culture media and cheese.
antioxidant compounds have been reported (Matkowski Food Chem. Toxicol. 47, 2397–2400.
2008; Cao et al. 2009; Conforti et al. 2009; Loizzo et al. HAJARE, S. and SHARMA, A. 2005. Aflatoxin inactivation using
2009). The antioxidant activity of these phenolic com- aqueous extract of Ajowan (Trachyspermum ammi) seeds.
pounds could be due to their proton-donating effects. In J. Food Sci. 70, 29–34.
this regard, they can retard or stop the oxidation of other HWANG, J.Y., SHUE, Y.S. and CHANG, H.M. 2001.
molecules by inhibiting the chain reaction of oxidation Antioxidative activity of roasted and defatted peanut kernels.
Food Res. Int. 34, 639–647.
(Sepici-Dincel et al. 2007).
KHANUM, H., RAMALAKSHMI, K., SRINIVAS, P. and
This study is the first report of the chemical composition
BORSE, B.B. 2011. Synergistic antioxidant action of
of Iranian T. ammi EO and its antimicrobial and antioxi-
Oregano, Ajowan and Borage extracts. J. Food Nutr. Sci. 2,
dant activities. In conclusion, the obtained data indicate
387–392.
that the EO exhibits potent antibacterial and antifungal
KHOSRAVI, A.R., SHOKRI, H., EMAMI, S.A., ALAVI, S.M. and
activity, which supports its use in traditional medicine for ASILI, J. 2011. The potential inhibitory effect of Cuminum
its antiseptic properties. The results clearly show that the oil cyminum, Ziziphora clinopodioides and Nigella sativa essential
of T. ammi presents antioxidant activity and might be useful oils on the growth of Aspergillus fumigatus and Aspergillus
for high fatty foods. flavus. Braz. J. Microbiol. 42, 216–224.
KOLEVA, I.I. and VANBEEK, T.A. 2001. Application of ABTS
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