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81
DOI: 10.2174/1874285801913010081, 2019, 13, 81-85
The Open Microbiology Journal
Content list available at: https://openmicrobiologyjournal.com
RESEARCH ARTICLE
Antibacterial and Antioxidant Activities of Nasturtium officinale Essential Oil on
Food Borne Bacteria
Saman Mahdavi1,*, Mojtaba Kheyrollahi2, Hossein Sheikhloei2 and Alireza Isazadeh3,4
1Department of Microbiology, Maragheh Branch, Islamic Azad University, Maragheh, Iran
2Department of Chemistry and Food Engineering, Maragheh Branch, Islamic Azad University, Maragheh, Iran
3Immunology Research Center, Tabriz University of Medical Sciences, Tabriz, Iran
4Department of Genetics, Tabriz Branch, Islamic Azad University, Tabriz, Iran
Abstract:
Introduction:
The use of synthetic preservatives has been increasing in the food industry, and this leads to an increased incidence of gastrointestinal diseases and
cancers in humans in the long run.
Aims & Objectives:
The aim of this study was to investigate the antibacterial and antioxidant activities of Nasturtium officinale essential oil on some important food
borne bacteria.
Materials & Methods:
In this study, the antibacterial activity of N. officinale essential oil was evaluated on Staphylococcus aureus, Bacillus cereus, Escherichia coli and
Salmonella enteric by microdilution method. Also, the antioxidant activity of this essential oil was evaluated by inactivating free radicals produced
by 2,2-diphenyl-1-picrylhydrazyl (DPPH). Finally, the chemical compounds of the N. officinale essential oil were evaluated by gas chromato-
graphy- mass spectrometry (GC/MS).
Results:
The results showed that S. enteric and E. coli isolates had the most resistance and B. cereus isolates had the most susceptibility to N. officinale
essential oil. The evaluation of antioxidant properties showed that in the same concentrations, the antioxidant effect of N. officinale was less than
BHT. The obtained results from GC/MS showed that Phytol (30.20%) was the highest proportion and Megastigmatrienone 2 (0.18%) was the
lowest proportion of essential oil.
Conclusion:
In general, the results of this study showed that N. officinale essential oil has an appropriate antibacterial activity against gram positive bacteria and
can be used as a new antibacterial and antioxidant compound in the food industry.
Keywords: Antibacterial, Antioxidant, Nasturtium officinale, Essential oil, Concentrations, Megastigmatrienone.
Article History Received: January 12, 2019 Revised: March 05, 2019 Accepted: March 10, 2019
1. INTRODUCTION
Today, although advances have been made on food
industry hygiene, diseases caused by microbial contamination
of foodstuff have become a major problem [1]. In some count-
* Address correspondence to this author at the Department of Microbiology,
Maragheh Branch, Islamic Azad University, Derakhshi Street, Maragheh, East
Azarbaijan, Iran; Tel: +98-9144150454; E-mail: s.mahdavi@iau-maragheh.ac.ir
ries, even in developed countries, 30% of the population is
affected by diseases caused by the consumption of conta-
minated foods, once a year [2]. Overuse of preservatives and
antibiotics in the food industry and treatment of patients have
greatly expanded drug resistance [3]. Therefore, natural re-
sources, especially medicinal and edible plants have been
considered as ecological reservoirs [4]. Due to the tendency of
people to consume food with natural preservatives, plant
82 The Open Microbiology Journal, 2019, Volume 13 Mahdavi et al.
sources are not only used as flavoring, but are also used as
antimicrobial compounds [5]. Recent studies have shown that
the extract and essential oil of a large number of traditional
medicinal plants have inhibitory and sometimes lethal effects
on various pathogenic microorganisms [7, 8]. Therefore, many
plant species have been used in the food industry due to their
antimicrobial and anti-oxidant properties [4, 6].
Nasturtium officinale belongs to the Cruciferae family. The
main origin of this plant is the Central and Western Europe, but
today it is spread throughout the world, including Asia, Europe
and throughout North America [9]. For many years, N.
officinale has been used to treat high blood glucose, high blood
lipids, high blood pressure, and cardiovascular and pulmonary
diseases [7]. It also contains beta-carotene, ascorbic acid,
calcium, folic acid, iron, phosphorus, iodine and amino acids,
and it is effective in inhibiting the growth of cancer cells [10].
N. officinale has a significant antioxidant capacity due to the
presence of numerous chemical compounds such as flavonoids
quercetin, carotenoids, beta-carotene, lutein, vitamin C and
zeaxanthin [11]. Also, recent studies have shown that the
extract and essential oil of this plant have antimicrobial activity
against different types of human and food pathogens [4, 12].
Since food health is a fundamental issue, and due to the
negative attitude of consumers to the use of food containing
chemical preservatives, identification and use of herbal and
natural ingredients with antimicrobial and antioxidant pro-
perties as preservatives are very important. Therefore, the aim
of this study was to evaluate the antioxidant and antibacterial
activities of N. officinale essential oil on food borne bacteria.
2. MATERIALS AND METHODS
2.1. Preparation of Ethanolic Essential Oil
After collecting N. officinale from Bonab city (Qara Gho-
shun area, April 2016), it was identified and approved by the
Herbarium of the Islamic Azad University, Maragheh Branch.
For isolation of the essential oils, the dried aerial parts of the
plants (50gr) were separately hydrodistilled in a Clevenger-
type apparatus for 3 h. The oils were dried over anhydrous
sodium sulfate and kept at 4°C in sealed brown vials until
required.
2.2. Preparation of Isolates and Bacterial Strains
The isolated bacteria from foods were used to study the
antibacterial activity of N. officinale essential oil. Gram posi-
tive bacteria included Staphylococcus aureus and Bacillus
cereus, and gram negative bacteria included Escherichia coli
and S. enteric. Also, S. aureus (PTCC 1112), B. cereus (ATCC
11778), E. coli (PTCC 1270) and S. enteric (PTCC 1709) were
purchased from the Persian Type Culture Collection (PTCC) as
standard strains.
2.3. Evaluation of Antibacterial Activity by Microdilution
Method
The Minimum Inhibitory Concentration (MIC) and
Minimum Bactericidal Concentration (MBC) methods were
used to determine the antibacterial activity of the essential oil
of N. officinale. 100µl of sterile Brain Heart Infusion (BHI)
(Merck, Germany) was poured into each micropellet (from No.
2-10). Then, 100µl N. officinale essential oil was poured into
the first and second micropellets and 100µl essential oil was
poured from the second well to a third well; this continued to
the 10th well. Therefore, dilutions of 100-0.39% of essential oil
were prepared. 100µl of new bacterial culture (the equivalent
of concentration of 0.5 Mc Farland test) with 1:100 diluted
ratio was added to each well. Then, 30 µl of resazurin index
(Sigma-Aldrich, USA) was added to all of the wells. The well
that showed a color change was the essential oil MIC. The well
had changed its color with two wells, before and after it had
been cultured in BHI agar medium, and was incubated
(Labtech, South Korea) at 37°C for 24 h. The first plate
associated with the well that did not show bacterial colony was
considered as the essential oil MBC. The MBC was defined as
the concentration in which no microorganism growth was
observed.
2.4. Evaluation of Antioxidant Activity by DPPH Method
Total antioxidant activity was measured by inactivating
free radicals produced by 2,2-diphenyl-1-picril-hydrazil
(DPPH) (Sigma-Aldrich, USA) and decolorization of dark
purple solution. A 500μM methanolic solution of DPPH was
prepared. Different concentrations (50ppm, 100ppm, 200ppm,
300ppm, 400ppm, 500ppm, 1000ppm) of synthesized anti-
oxidants of Butylated Hydroxytoluene (BHT) (Sigma-Aldrich,
USA) were prepared as reference antioxidants. Then, 4ml of
each concentration was transferred to the test tubes and mixed
with 1ml of DPPH solution. After 30 minutes, the absorbance
of the solution was measured at 517nm using a spec-
trophotometer (UNICO-SQ2800, USA). This experiment was
also repeated for N. officinale. The percentage of Radical
scavenging activity (RSA%) was calculated using the
following formula: RSA% = (Ac-As)/Ac × 100 (Ac = control
absorption and As = sample absorption).
2.5. Evaluation of Chemical Compounds by GC/MS
The gas chromatograph (Shimadzu-QP2010, Japan) with
ZB-WAX column (length 20m, inner diameter 0.18mm,
thickness 18.1μm) were used to identify the compounds of the
essential oil of N. officinale. The essential oil of N. officinale
was diluted with normal hexane and 1µl was injected into gas
chromatography/mass spectrometry (GC/MS). The initial
temperature of the oven was 50°C, maintained at this
temperature for 5 minutes (thermal gradient: 3°C per minute)
and then the temperature was increased to 240°C. The final
temperature of the oven was 300°C and maintained at this
temperature for 3 minutes (thermal gradient: 3°C per minute).
The temperature of the injector was 300°C and split/split less
(1 to 50). Helium (99.9999%) was used as the carrier gas at a
flow rate of 1ml/min. Then, mass spectrometry (Agilent 5973,
USA) (length 20m, inner diameter 0.25μm, thickness 0.25mm)
was used. The temperature of the ionization chamber was
150°C, the temperature of the detector was 230°C, the
ionization energy was 70eV and the mass analyzer was
Quadrupole. The scan mass range was 40m/z to 550m/z. The
mass spectrometry was used to determine the compounds of
the essential oil of N. officinale. The spectral values were
compared with Kovatz index values in the standard tables and
Antibacterial and Antioxidant Activities The Open Microbiology Journal, 2019, Volume 13 83
the compounds of the essential oil of N. officinale were
identified according to data and information available in the
GC-MS library. The conditions of the compounds identified
from the essential oil of N. officinale using GC/MS method are
shown in Table 1.
Table 1. The conditions of GC/MS to identification
compounds of N. officinale ethanolic extract.
Conditions and Compounds Instrument
Model QP2010,
Shimadzu Co., Japan Instrument model
Gas
chromatograph
ZB-WAX model Column model
Length: 20 m
Inner diameter: 0.18 mm
Thickness: 0.18 μm
Column dimensions
Initial temperature: 50°C
for 5 min
Final temperature: 300°C
for 5 min
Temperature gradient:
3°C per min
Oven temperature
program
1µl Injection volume
Split/split less (ratio
1:50) Split ratio
300°C Injector temperature
Helium (99.9999%) Carrier gas
1ml/min Flow rate of the carrier
gas
Model 5973, Agilent,
USA Instrument model
Mass
spectrometer
Length: 20m
Inner diameter: 0.25μm
Thickness: 0.25mm
Column dimensions
70eV Ionization energy
150°C Ionization chamber
temperature
Quadrupole Mass analyzer
230°C Detector temperature
3. RESULTS
3.1. Antibacterial Activity of N. officinale Essential Oil
S. enteric and E. coli (gram negative) showed the most
resistance (growth of all isolates in ≥25% concentrations), and
B. cereus (gram positive) isolates had the most sensitivity
(growth of all isolates in ≤1.56% concentration) against
N. officinale essential oil (Table 2).
3.2. Antioxidant Activity of Essential oil of N. officinale
The obtained results showed that in the same
concentrations, the antioxidant effect of N. officinale essential
oil was less than BHT. The antioxidant effect of N. officinale
essential oil, such as BHT, increased with increasing
concentrations (Table 3).
3.3. Compounds of Essential Oil of N. officinale
The chemical compounds extracted from the essential oil
of N. officinale using GC/MS method are shown in Table 4.
According to the obtained results, phytol was the most frequent
compound and Megastigmatrienone 2 was the least frequent
compound. However, further studies on the extracts and
essential oil of N. officinale and especially other bacterial
pathogens may be necessary.
Table 2. Antimicrobial effect of N. officinale ethanolic
extract on bacteria isolated from food.
Bacteria Ethanolic extract (%)
1.56 3.12 6.25 12.5 25 50
E. coli PTCC 1270 + + + + + -
E.coli +3 +3 +3 +3 +3 -3
S. enteric PTCC 1709 + + + + + -
S. enteric +3 +3 +3 +3 +3 -3
S. aureus PTCC 1112 + + + + - -
S. aureus +3 +3 +3 +3 -3 -3
B. cereus ATCC 11778 + - - - - -
B. cereus +3 -1 -2 -3 -3 -3
(+) Bacterial growth; (-) Bacterial non-growth; (PTCC) Persian Type Culture
Collection; (ATCC) American Type Culture Collection
Table 3. Comparison of antioxidant effect of N. officinale
ethanolic extract with BHT.
Sample Concentration (ppm)
50 100 200 300 400 500 1000
N. officinale extract (%) 4.18 9.34 16.39 24.37 28.6 32.83 37.99
BHT (%) 77.97 90.41 92.53 92.86 93.24 93.51 93.75
4. DISCUSSION
Recently, secondary metabolites of medicinal plants such
as essential oils and extracts have been investigated for
antimicrobial effects [13], and it has been shown that the most
obtained essential oil from medicinal plants have anti-fungal,
anti-parasitic, anti-bacterial and anti-viral properties [14].
Therefore, essential oil of medicinal plants has been used in
pharmacological fields, herbal pharmacology, clinical
microbiology, phytopathology, and food, fruits and vegetables
preservatives [15]. Traditional medicinal plants have been
recognized for many centuries in many parts of the world for
the treatment of various diseases and use of these antibacterial
agents has revolutionized the treatment of various bacterial
infections [16]. The results of MIC and MBC analysis in the
present study showed that N. officinale ethanolic essential oil
has a bacteriostatic effect on S. aureus, E. coli, B. cereus and
S. enterica which is in agreement with the results of Lanciotti
et al,. 2003 research [17].
Hexanal is an organic alcohol and previous studies on this
alcohol have reported its antimicrobial properties on
Salmonella spp and Listeria spp. Also, 2-E hexanal has a
protective effect against Salmonella spp. The presence of these
two compounds in a higher degree in the phytochemicals of
essential oil and extracts of N. officinale can be a reason for its
inhibitory properties on Salmonella strains [17]. Patrignani
et al. (2008) showed the antimicrobial effects of hexanal and 2-
E hexanal on S. aureus, S. enterica and E. coli strains [18].
84 The Open Microbiology Journal, 2019, Volume 13 Mahdavi et al.
Table 4. The obtained compounds of N. officinale ethanolic extract using GC/MS.
No. Compound Frequency No. Compound Frequency
1 Hexanal 1.06% 17 2-methoxy-4-vinyl phenol 3.12%
2 Normal hexanol 0.42% 18 3-carene-10-acethyl-methyl 9.41%
3 2-pentyl furan 1.32% 19 Neryl asetone 1.53%
4 Normal nontanal 0.91% 20 Megastigma Trianon 0.49%
5 Decanal normal 0.54% 21 Anthracene 0.49%
6 Trimethyl 0.55% 22 Eucusan 1.44%
7 Beta-Dumas Senon 7.42% 23 2-E hexanal 0.96%
8 3-carene-10-acethyl-methyl 9.41% 24 Benzaldehyde 0.25%
9 E-beta-lavonone 7.15% 25 Normal Octanol 0.55%
10 Megastigmatrienone 2 0.18% 26 Safranal 0.74%
11 Phytol 30.20% 27 1-cyclohexene-1-acetaldoyde 0.55%
12 2-E hexanal 0.96% 28 Cyclohexane 1.41%
13 2-heptane 0.28% 29 2-Butanone 4.10%
14 Bnz- E- acetaldehyde 0.74% 30 Alpha Humolin 0.48%
15 2-Nonnal 0.34% 31 Hexadekan 0.25%
16 Naphthalene-2,1-dihydro-6,1,1-trimethyl 1.25% 32 2-Pentadecanone-14,10,6-trimethyl-25/1% -15,12,9-octo-deca tri-acetic
acid 1.20%
Previous studies indicate that the presence of normal hexanol
in essential oils and extracts of medicinal plants refers to the
antimicrobial effect of these plants on S. aureus and E. coli
bacteria [19]. The presence of normal hexanol in medicinal
plant phytochemicals is one of the inhibitory factors for the
mentioned bacteria, which is compatible with the present study
[19]. The presence of 1-cyclohexan acetaldehyde in the extract
and essential oil of some medicinal plants indicates their anti-
microbial ability, which has an inhibitory effect on S. aureus,
E. coli and K. pneumoniae. This inhibitory property can be
involved with this chemical compound. Our results in
phytochemical section indicate the presence of this compound
in the essential oil of N. officinale.
Butnariu and Bostan (2011) reported that the most
antimicrobial activity of N. officinale was found in S. aureus,
E. coli and S. enterica, respectively. Furthermore, it was
reported that the antimicrobial effect of the essential oil of this
plant was more than its extract [20]. Jang et al. (2010) reported
that the inhibitory effect of N. officinale essential oil on gram
positive bacteria (S. aureus, Listeria monocytogenes, B. cereus)
was more than gram negative bacteria (Aeromonas hydrophila
and Shigella sonnei) [21], which is compatible with the results
of the current study.
The measurement of inhibition of DPPH free radicals is
one of the valid, accurate, easy and inexpensive methods with
high repeatability, which is used in the evaluation of
antioxidant activity of medicinal plant essential oil in vitro. In
the present study, it was shown that increasing the
concentration of N. officinale essential oil leads to an increase
in antioxidant activity and consequently, the percentage of
inhibition of free radicals was increased. Previous studies have
also shown that the inhibitory activity of DPPH-free radicals
by medicinal plants essential oil depends on the concentration,
and with increasing concentrations, inhibitory effects increased
[22 - 24]. The compounds of N. officinale essential oil are
capable of releasing electrons to free radicals and thus stop the
free radical chain reaction, which matches the results of the
current study.
CONCLUSION
According to the results obtained in this study,
N. officinale essential oil showed appropriate antibacterial and
antioxidant activity against tested gram-positive bacteria.
Therefore, it can be used as a natural preservative and anti-
bacterial compound in food.
ETHICS APPROVAL AND CONSENT TO PARTI-
CIPATE
Not applicable.
HUMAN AND ANIMAL RIGHTS
No animals/humans were used for studies that are the basis
of this research.
CONSENT FOR PUBLICATION
Not applicable.
CONFLICT OF INTEREST
The authors declare no conflict of interest, financial or
otherwise.
ACKNOWLEDGEMENTS
Declared none.
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© 2019 Mahdavi et al.
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