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Antibacterial activity and composition of essential oils from Origanum, Thymbra and Satureja species with commercial importance in Turkey

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The antibacterial activity of essential oils and their derivatives has been recognized for a long time. In the present study, the chemical composition and the antibacterial properties of the essential oils obtained from the aerial parts of the four Lamiaceae species, wild oregano (Origanum minutiflorum) (endemic in Turkey), oregano (Origanum onites), black thyme (Thymbra spicata) and wild savory (Satureja cuneifolia), with commercial importance in Turkey, were evaluated.The major constituent of the oils determined by GC was cavracrol (86.9% in O. onites, 84.6% in O. minutiflorum, 75.5% in T. spicata and 53.3% in S. cuneifolia). Four essential oils were investigated for activity against Aeromonas hydrophila, Bacillus amyloliquefaciens, B. brevis, B. cereus, B. subtilis, Corynebacterium xerosis, Enterococcus faecalis, Escherichia coli, Klebsiella pneumoniae, Listeria monocytogenes, Micrococcus luteus, Mycobacterium smegmatis, Proteus vulgaris, Staphylococcus aureus and Yersinia enterocolitica, using a paper disc diffusion method. All essential oils inhibited all bacteria at concentrations of <1/100 (v/v). The essential oil of T. spicata was the most active. B. amyloliquefaciens was the most sensitive. The results of this study confirmed the possibility of using these four essential oils in food systems to prevent the growth of foodborne bacteria and extend the shelf life of processed foods.
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Antibacterial activity and composition of essential oils from
Origanum,Thymbra and Satureja species with
commercial importance in Turkey
Hasan Baydar
a
, Osman Sa
ggdic
ß
b,*
,G
uulcan
OOzkan
c
, Tahsin Karado
ggan
a
a
Agricultural Faculty, Department of Field Crops, University of Suleyman Demirel, 32260 Isparta, Turkey
b
Agricultural Faculty, Department of Food Engineering, University of Suleyman Demirel, 32260 Isparta, Turkey
c
Agricultural Faculty, University of Suleyman Demirel, 32260 Isparta, Turkey
Received 23 November 2002; received in revised form 15 February 2003; accepted 18 February 2003
Abstract
The antibacterial activity of essential oils and their derivatives has been recognized for a long time. In the present study, the
chemical composition and the antibacterial properties of the essential oils obtained from the aerial parts of the four Lamiaceae
species, wild oregano (Origanum minutiflorum) (endemic in Turkey), oregano (Origanum onites), black thyme (Thymbra spicata) and
wild savory (Satureja cuneifolia), with commercial importance in Turkey, were evaluated.
The major constituent of the oils determined by GC was cavracrol (86.9% in O. onites, 84.6% in O. minutiflorum, 75.5% in T.
spicata and 53.3% in S. cuneifolia). Four essential oils were investigated for activity against Aeromonas hydrophila,Bacillus amy-
loliquefaciens,B. brevis,B. cereus,B. subtilis,Corynebacterium xerosis,Enterococcus faecalis,Escherichia coli,Klebsiella pneumoniae,
Listeria monocytogenes,Micrococcus luteus,Mycobacterium smegmatis,Proteus vulgaris,Staphylococcus aureus and Yersinia
enterocolitica, using a paper disc diffusion method. All essential oils inhibited all bacteria at concentrations of <1/100 (v/v). The
essential oil of T. spicata was the most active. B. amyloliquefaciens was the most sensitive. The results of this study confirmed
the possibility of using these four essential oils in food systems to prevent the growth of foodborne bacteria and extend the shelf
life of processed foods.
Ó2003 Elsevier Ltd. All rights reserved.
Keywords: Lamiaceae; Antibacterial activity; Essential oils
1. Introduction
From antiquity, in addition to spices and their de-
rivatives being used for flavouring foods and beverages
and for medication, they have also been highly valued
for their use as antimicrobials (
OOzcan, 1998). The leafy
part of plants such as oregano, thyme and savory be-
longing to the Lamiaceae family have been added to
meat, fish and food products for many years (Sa
ggdıc
ß&
OOzcan, 2003).
Turkey is regarded as an important gene-center for
the family Lamiaceae (Labiatae). The family is repre-
sented by 45 genera, 546 species and 730 taxa in Turkey.
The rate of endemism in the family is 44.2% (Baser,
1993). The members of the Lamiaceae are common
mainly in the mountainous areas of the Mediterranean
parts of Turkey and the composition of their essential
oils is detailed by Baser (1994).
The flora of Turkey has 23 species of Origanum (15
endemic), 2 species of Thymbra and 14 species of Sat-
ureja (4 endemic). They are regarded as oil-rich (>2%)
on the basis of their essential oil contents (Baser, 1993).
They are known and used as thyme or ‘‘kekik’’ which is
the name given those species with a thymol/carvacrol
type odor in Turkey. Origanum minutiflorum O. Schwarz
and P.H. Davis, Origanum onites L., Thymbra spicata L.
and Satureja cuneifolia Ten. are largely collected wild
from the Isparta region, in the south-western part of
Turkey, and then exported to the world markets at al-
most 1000 tonnes per year.
The chemical composition of essential oils depends
on climatic, seasonal, and geographic conditions, har-
vest period, and distillation technique. In addition, their
*
Corresponding author. Tel.: +90-246-2111542; fax: +90-246-
2370437.
E-mail address: osagdic@ziraat.sdu.edu.tr (O. Sa
ggdic
ß).
0956-7135/$ - see front matter Ó2003 Elsevier Ltd. All rights reserved.
doi:10.1016/S0956-7135(03)00028-8
Food Control 15 (2004) 169–172
www.elsevier.com/locate/foodcont
antibacterial activity depends on the type, composition
and concentration of the spice or the essential oils, the
type and concentration of the target microorganism,
the composition of the substrate, the processing and the
storage conditions (Marino, Bersani, & Comi, 2001;
OOzcan & Erkmen, 2001; Pandit & Shelef, 1994; Panizi,
Flamini, Cioni, & Morelli, 1993).
The antibacterial activities of spices and essential oils
have been known for a long time, and a number of re-
search projects on the antimicrobial effect of oregano,
thyme and savory plants, essential oils and their deriv-
atives have been reported (Aligiannis, Kalpoutzakis,
Mitaku, & Chinou, 2001; Cosentino et al., 1999; Dor-
man & Deans, 2000; Hammer, Carson, & Riley, 1999;
Marino et al., 2001;
OOzcan, 1998; Panizi et al., 1993;
Sa
ggdıc
ß,Kus
ßc
ßu,
OOzcan, &
OOzc
ßelik, 2002; Sa
ggdıc
ß&
OOzcan, 2003). Research reports on the essential oil
composition of black thyme (T. spicata) and oregano
(O. onites) are limited (Akg
uul & Kıvanc
ß, 1988; Kıvanc
ß&
Akg
uul, 1986), whereas the oils of wild oregano (O. mi-
nutiflorum) and wild savory (S. cuneifolia) have never
been studied before. Especially wild oregano is endemic
in Turkey, and so it has a special importance for the
study.
In the present work, a wide range of potentially
pathogenic and other bacteria was used to evaluate
antibacterial activity and to relate it to the chemical
composition of essential oils extracted from plants be-
longing to the Lamiaceae, including wild oregano,
oregano, black thyme and wild savory.
2. Materials and methods
2.1. Plant materials
The aerial parts of wild oregano (O. minutiflorum O.
Schwarz and P.H. Davis) (endemic in Turkey), oregano
(O. onites L.), black thyme (T. spicata L.) and wild sa-
vory (S. cuneifolia Ten.) were collected wild during the
flowering stage from Isparta, the south western part of
Turkey in June to July in 2001 at altitudes of 250–1900
m. The plants were identified by Dr. H.
OOzc
ßelik, Di-
rector of the Herbarium Section, Isparta. Herbarium
specimens were deposited at the Department of Biology,
Faculty of Science and Education, University of Suley-
man Demirel, Isparta, Turkey.
2.2. Isolation of essential oils
The essential oils of the species were produced by the
Clevenger hydrodistillation method. Plant materials
(100 g), cut into small pieces, were placed in a distillation
apparatus with 2 l of double distilled water and hydro-
distilled for 3 h. After the oils were dried over anhydrous
sodium sulphate, they were stored at 4 °C until used for
GC analyses (Deans & Svoboda, 1990).
2.3. Determination of chemical composition of essential
oils by GC
The gas chromatographic analysis of the essential oils
was performed with a Hewlett-Packard 6890 series gas
chromatograph (Perkin Elmer (PE) Auto System XL,
USA), fitted with a flame ionisation detector (FID). The
PE Auto System XL gas chromatograph was employed
under the following conditions: capillary column, CP-
Wax52CB(50m0.32 mm; film thickness ¼0.25 lm);
oven temperature program, 60 °C raised to 220 °Cata
rate of 5 °C/min and than held at 220 °C for 20 min;
injector and detector temperatures, 240 °C; carrier gas,
helium at flow rate of 40 ml/min; split ratio, 1/20 ml/min.
Relative percentage amounts were calculated from
chromatograms by the Turbo Crom. Navigator com-
puter program.
2.4. Reference bacteria
The 15 bacteria used as test organisms were as fol-
lows: Aeromonas hydrophila ATCC 7965, Bacillus amy-
loliquefaciens ATCC 3842, B. brevis FMC 3, B. cereus
FMC 19, B. subtilis IMG 22, Corynebacterium xerosis
UC 9165, Enterococcus faecalis ATCC 15753, Escheri-
chia coli DM, Klebsiella pneumoniae FMC 5, Listeria
monocytogenes Scott A, Micrococcus luteus LA 2971,
Mycobacterium smegmatis RUT, Proteus vulgaris FMC
1, Staphylococcus aureus Cowan 1, Yersinia enterocoli-
tica EU.
B. amyloliquefaciens,B. brevis,P. vulgaris and Y.
enterocolitica were grown in nutrient broth (Acumedia
Manufacturers, Inc., Maryland) at 25 °C for 22 h. The
other bacteria were grown in the same medium at 35 °C
for 22 h. (Marshall, 1992). The bacteria were obtained
by Dr. M. Dıgrak from the Biology Department, Fac-
ulty of Science and Education, University of Sutcu
Imam, Kahramanmaras
ß, Turkey.
2.5. Determination of antibacterial activity by the paper
disc diffusion method
The spice essential oils were tested for antibacterial
activity by the paper disc diffusion method. The bacteria
were maintained on Nutrient agar at 4 °C. Molten (45
°C) sterile nutrient agar (10 ml) in a flask was inoculated
with a broth culture (1%, containing 106–107cfu/ml) of
the respective bacterial strains and poured over base
plates containing 10 ml Nutrient agar in sterile 9 cm
Petri dishes. Fifty microliters of dilution of the essential
oils were pipetted on sterile filter paper discs (Whatman
No.1. 5 mm in diameter), which were allowed to dry in
an open sterile Petri dish in a biological safety cabinet
170 H. Baydar et al. / Food Control 15 (2004) 169–172
with vertical laminar flow (Nuaire Laminar Flow
Products, USA). 1/50, 1/100, 1/200 and 1/300 solutions
of the essential oils in absolute ethanol were applied to
the discs. Discs were placed on the surface of the inocul-
ated plates and incubated for 18 h. Diameters (mm) of
the zones of bacterial inhibition minus the disc diameter
were recorded (Aureli, Costantini, & Zolea, 1992;
_
IIlc
ßim,
ggrak, & Ba
ggcı, 1998). Control assay discs impreg-
nated with absolute ethanol and then allowed to dry
were also used. All analyses were applied in duplicate.
3. Results and discussion
3.1. Chemical composition of the essential oils
The essential oil components identified are given in
Table 1. Eight major constituents were determined
representing 97.4% in wild oregano, 97.1% in oregano,
99.0% in black thyme and 93.1% in wild savory.
The essential oils were characterised by high contents
of cavracrol, c-terpinene and p-cymene, respectively
(Table 1). The essential oil components of O. onites have
been determined by researchers (e.g. Sokovic, Tzakou,
Pitarokili, & Couladis, 2002), but studies on the chem-
ical compositions of the other essential oils were lacking.
3.2. Determination of antibacterial activity of the essen-
tial oils by paper disc diffusion method
The essential oils from the four spices were inhibitory
to the growth of all the bacteria under test, and these
finding are summarised in Table 2. B. amyloliquefaciens
and P. vulgaris were the most susceptible. The essential
oil of black thyme on B. amyloliquefaciens and P. vulg-
aris had inhibition zones with diameters in excess of 39.5
and 56.5 mm, respectively. Control treatment (absolute
alcohol) did not show an inhibitory effect on any of the
bacteria.
The oil of wild oregano was inhibitory to all of the
bacteria at a concentration of 1/50 and at the 1/100
concentration against A. hydrophila,B. amyloliquefac-
iens,C. xerosis,E. faecalis,M. luteus and P. vulgaris.
Whereas the 1/200 concentration inhibited B. amyloliq-
uefaciens and C. xerosis, the 1/300 concentration of the
oil was only active on B. amyloliquefaciens. Studies on
the antimicrobial effect of wild oregano are lacking in
literature.
The essential oil of oregano at 1/50 concentration was
active against all of the bacteria. Also, 1/100 concen-
tration of the oil inhibited the bacteria except A. hy-
drophila,B. cereus and E. coli. While the oil at 1/200
concentration was only inhibitory to B. amyloliquefac-
iens and P. vulgaris, 1/300 concentration of the oil had
Table 1
Chemical composition of the essential oils (% total peak area)
Essential oil components (%)
Wild
oreganoa
Oregano Black
thyme
Wild
savory
Myrcene 1.5 1.3 1.3 2.1
a-terpinene 0.8 0.9 1.1 2.1
c-terpinene 3.3 3.9 11.6 27.4
p-cymene 4.2 2.9 9.2 7.3
Bornylacetate 0.8 0.4 0.1 0.1
Borneol 0.5 0.6 0.1 0.7
Thymol 1.7 0.2 0.1 0.1
Cavracrol 84.6 86.9 75.5 53.3
a
Endemic in Turkey.
Table 2
Inhibition by essential oils of Turkish spices (zone size, mm)
Test bacteria Different concentrations of the essential oils
Wild oreganoaOregano Black thyme Wild savory
1/50 1/100 1/200 1/300 1/50 1/100 1/200 1/300 1/50 1/100 1/200 1/300 1/50 1/100 1/200 1/300
A. hydrophila 35.5 34.0 – – 38.5 – – – 36.0 28.5 – – 30.5 27.0
B. amyloliquefac-
iens
39.0 35.5 36.0 36.0 41.5 35.5 33.5 39.5 36.0 34.5 34.0 36.0 34.5
B. brevis 33.5 – – – 55.0 50.5 – – 45.0 38.5 – – 42.0 36.5
B. cereus 40.0 – – – 34.0 – – – 36.5 – – – 36.5 31.0
B. subtilis 41.0 – – – 46.5 34.5 – – 44.0 30.5 – – 26.5 23.0
C. xerosis 39.5 38.5 35.0 – 38.5 35.0 – 40.0 37.5 35.0 34.0
E. faecalis 40.5 36.0 49.0 31.5 – 34.5 32.0 33.0 33.5
E. coli 35.5 – – – 32.5 – – – 36.5 – – – 37.5 36.5
K. pneumonias 38.0 – – – 38.0 29.5 – – 39.0 33.5 – – 35.0 13.5
L. monocytogenes 25.5 – – – 31.0 24.5 – – 33.5 28.0 – – 12.5 – –
M. luteus 38.5 31.5 34.5 32.0 – 35.5 31.0 44.5 33.0
M. smegmatis 39.5 44.0 37.5 – 50.5 42.5 42.0 33.0 29.0 –
P. vulgaris 51.0 33.5 53.5 41.0 20.0 56.5 41.5 21.5 39.0 38.0 29.5
S. aureus 31.5 – – – 36.0 26.5 – – 35.0 29.0 – – 34.0 28.5
Y. enterocolitica 37.0 – – – 45.0 40.0 – – 36.0 32.5 – – 32.0 – –
–: not determined.
a
Endemic in Turkey.
H. Baydar et al. / Food Control 15 (2004) 169–172 171
no inhibitory effect against any of the bacteria. Several
researchers reported that O. onites inhibited yeasts and
moulds (Kıvanc
ß& Akg
uul, 1989; Sokovic et al., 2002).
The essential oil of black thyme (containing mainly
cavracrol 75.5%) was the most active. The 1/50 con-
centration was inhibitory against all strains, and the
1/100 concentration inhibited all except B. cereus and
E. coli. Only, B. amyloliquefaciens and P. vulgaris were
sensitive to the 1/200 concentration, and B. amylolique-
faciens was affected by the 1/300 concentration. The
black thyme oil on P. vulgaris produced the largest in
the study (56.5 mm). It was previously determined that
the decoction, extract and hydrosol of black thyme in-
hibited moulds, yeasts and bacteria (Kıvanc
ß& Akg
uul,
1988;
OOzcan, 1998;
OOzcan & Boyraz, 2000; Sa
ggdıc
ßet al.,
2002; Sa
ggdıc
ß&
OOzcan, 2003).
Report at the antimicrobial activity of wild savory are
lacking. The concentration of 1/50 and 1/100 of the oil
was effective against all of the bacteria, but not against
L. monocytogenes and Y. enterocolitica at 1/100 con-
centration. The 1/200 concentration only inhibited M.
smegmatis and P. vulgaris, whilst the 1/300 concentra-
tion of the oil did not inhibited on any of the bacteria.
The results showed that the activity of the oils can be
attributed, to a considerable degree, to the existence
mostly of cavracrol, p-cymene and c-terpinene. Essential
oils rich in phenolic compounds such as cavracrol are
widely reported to possess high levels of antimicrobial
activity (Aligiannis et al., 2001; Panizi et al., 1993;
Sivropoulou et al., 1996), which has been confirmed and
extended in the present studies.
4. Conclusion
The results of this study suggest the possibility of
using the four essential oils or some of their components
as natural food preservatives, because the oils possess
strong antibacterial activity. The antibacterial properties
of the essences of the wild oregano (O. minutiflorum),
oregano (O. onites), black thyme (T. spicata) and wild
savory (S. cuneifolia) are mostly attributable to the
phenolic compound cavracrol and to the hydrocarbons
c-terpinene and p-cymene. The essential oils were nat-
ural products preventing the growth of foodborne
pathogens or spoilage organisms in the test systems.
Further work is necessary to explore the efficacy, and
palatability, of suitable concentrations of these essential
oils in foods.
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... Gedikoğlu and coauthors [32] reported that carvacrol (68.20%), γ-terpinene (13.25%), p-cymene (5.37%), βcaryophyllene (2.59%), and thymol (1.19%) were major components of T. spicata. Barakat and coauthors [33], Hancı and coauthors [34], Baydar and coauthors [35] and Markovic and coauthors [36] reported that carvacrol, γ-terpinene and p-cymene were the major components of the essential oils of T. Spicata and their amounts varied according to the different growth seasons. ...
... mm) against S. aureus (Table 2, 3). In studies investigating the antimicrobial activity of T. spicata essential oil in various bacterial and fungal strains by disk diffusion methods; It has been determined that the essential oil of the plant has an antimicrobial effect against the tested bacteria and fungi [35,45,46]. Bioactivity of essential oil might be attributed to a single major constituent or to the synergistic/ additive behaviours of minor components [47]. ...
... In this study, the essential oils were characterised by high contents of carvacrol. Similar results having been reported in other studies, Baydar and coauthors [35] stated that the essential oil of T. spicata (containing mainly carvacrol 75.5%) was the inhibitory against E. coli and S. aureus. It is thought that carvacrol interacts with the cytoplasmic membrane and causes passive transport of ions across the membrane [48]. ...
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... In addition, their antibacterial potency may change based on the content or concentration of the plant or its essential oil, and also the type and density of the bacteria. 47 The essential oils of Origanum species, obtained at the right time, from the right place, and in the right way, can be applied to the leather, which is a soft and breathable material for diabetic foot patients. This application may be done after the fatliquoring process via microencapsulation or during finishing process by spraying method of nano/microencapsules. ...
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... Essential oils are natural compounds produced by aromatic plants as secondary metabolites that have antioxidant, antiradical, and antimicrobial properties [7]. Antibacterial activities of some essential oils have been reported [8]. ...
Conference Paper
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In the present study, we synthesised Origanum vulgare essential oil/Ag nanoparticles nanoemulsion with a spontaneous emulsification method. First, Ag nanoparticles (AgNPs) were synthesised via a green method and these particles were then used as the aqueous phase of the nanoemulsions. Origanum vulgare essential oil (EO) exhibits a broad-spectrum antimicrobial activity against foodborne microorganisms like Escherichia coli O157:H7 so, it was used to preparing the nanoemulsion. Scanning electron microscopy (SEM), X-ray diffraction spectroscopy (XRD), UV-Vis spectroscopy confirmed the formation of AgNP and dynamic light scattering (DLS) was used to measuring the particle size and nanoemulsion droplet size. Finally, we investigated the antibacterial activity of AgNPs, Origanum vulgare EO and Origanum vulgare EO/AgNPs nanoemulsion against E. coli O157:H7 via inhibition zone method. Our results showed that bacterial inhibition zones of AgNPs were increased in a dose-dependent manner and Origanum vulgare EO (100%) had a great antibacterial activity against E. coli O157:H7 but its antibacterial activity was drastically decreased at 12.5% which was the concentration that used in the emulsion. As expected, nanoemulsion showed greater inhibition zones than AgNPs and EO(12.5%). The antibacterial activity of nanoemulsion is higher than its active components AgNPs and Origanum vulgare EO (12.5%) in which produced the largest E. coli O157:H7 inhibition zones (19.67 mm) within all the compounds (P<0.05).
... Some plants contain a variety of active ingredients such as saponins, polysaccharides, and essential oils, which play important roles in inhibiting the growth of pathogens, improving immunity, and promoting intestinal health without toxic and side effects (9). Plant extracts are secondary metabolites of plants (10), which have the functions of antimicrobial (11), and antiinflammatory (12), and have been proposed as substitutes for chemical feed additives with the banning of some ionophore feed additives in many countries (13). ...
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The study aimed to screen the antibacterial activity of seven types of essential oils against 5 bacteria and 4 strains of E. coli using disk diffusion and MIC method. The essential oils were more effective against Gram-positive bacteria as compared to Gram-negative species. Thyme and cinnamon essential oils showed strong antimicrobial activity against all microorganisms tested. Especially, the tested essential oils inhibited the growth of multi-antibiotics resistant bacteria isolated from food processing chains, indicating the possibility of their potential use in reality. The MIC values of cinnamon and thyme essential oils against E. coli ATCC 25922, S. typhimurium, S. aureus, L. monocytogenes and P. aeruginosa were 512-1024 µg/mL and 1024-4096 µg/mL, respectively. The present study provided useful information and showed the potential use of cinnamon and thyme essential oils in food storage as natural antimicrobial preservatives.
Chapter
Medicinal traditional plants are a source of inspiration for the discovery of new bioactive substances. Plant infusions, extracts, and essential oils are known for their diverse biological activity since they are rich in secondary metabolites. The Mediterranean area in general and Lebanon in particular is known for its plant diversity due to its climate and geographical location. This chapter will provide an overview of Lebanese plants with antimicrobial activity. Many of these plants are known for their culinary and traditional medicinal uses for the treatment of different ailments. The main plant families discussed here include Amaryllidaceae, Anacardiaceae, Apiaceae, Asteraceae, Berberidaceae, Cannabaceae, Cistaceae, Lamiaceae, Myrtaceae, Pinaceae, Portulacaceae, Ranunculaceae, Rutaceae, Rosaceae, and others.
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The antimicrobial activities of the extracts of seven spices (cumin, Helichrysum compactum Boiss (HC), laurel myrtle, oregano, sage and thyme) were examined in their capacity to inhibit the growth of Escherichia coli O157-H7 Spices were fractionated by the extraction method to obtain a methanolic fraction. Of the spices tested thyme showed promising results by inhibiting growth both in paper disc assay and agitated liquid culture assay Antibacterial effects of tested spices extracts vary related to concentrations. Thyme and oregano showed higher activity than the others. It was also found that laurel and HC markedly stimulated the growth of E. coli O157-H7 Statistically, important variations were found among the inhibitory effects of spice extracts. This study has shown that E. coli O157-H7 inhibition by spice extracts may be of use in the field of food preservation.
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Steam distilled volatile oil from marjoram (Origanum majorana L.) was evaluated for its antibacterial and antifungal activities. A range of 25 bacterial and five fungal species was used in this study, and included animal and plant pathogens, food poisoning bacteria and mycotoxigenic fungi. The oil exerted considerable inhibitory powers against several of the bacteria, with the food-poisoning bacterium Staphylococcus aureus being least affected. The most susceptible organisms were Beneckea natriegens, Erwinia carotovora and Moraxella sp. Of the fungi tested, Aspergillus niger proved the most susceptible to marjoram oil.