The Open Microbiology Journal




ISSN: 1874-2858 ― Volume 13, 2019
RESEARCH ARTICLE

Antibacterial and Antioxidant Activities of Nasturtium officinale Essential Oil on Food Borne Bacteria



Saman Mahdavi1, *, Mojtaba Kheyrollahi2, Hossein Sheikhloei2, Alireza Isazadeh3, 4
1 Department of Microbiology, Maragheh Branch, Islamic Azad University, Maragheh, Iran
2 Department of Chemistry and Food Engineering, Maragheh Branch, Islamic Azad University, Maragheh, Iran
3 Immunology Research Center, Tabriz University of Medical Sciences, Tabriz, Iran
4 Department 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 chromatography- 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 Information


Identifiers and Pagination:

Year: 2019
Volume: 13
First Page: 81
Last Page: 85
Publisher Id: TOMICROJ-13-81
DOI: 10.2174/1874285801913010081

Article History:

Received Date: 12/01/2019
Revision Received Date: 05/03/2019
Acceptance Date: 10/03/2019
Electronic publication date: 28/03/2019
Collection year: 2019

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© 2019 Mahdavi et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: (https://creativecommons.org/licenses/by/4.0/legalcode). This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* 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




1. INTRODUCTION

Today, although advances have been made on food industry hygiene, diseases caused by microbial contamination of foodstuff have become a major problem [1Mahdavi S, Azizi Dehbokri M, Isazadeh A. Contamination of chicken meat with Salmonella spp distributed in mahabad city, Iran. Int J Enteric Pathog 2018; 6(3): 65-8.[http://dx.doi.org/10.15171/ijep.2018.18] ]. In some countries, even in developed countries, 30% of the population is affected by diseases caused by the consumption of contaminated foods, once a year [2Al-Mustafa AH, Al-Thunibat OY. Antioxidant activity of some Jordanian medicinal plants used traditionally for treatment of diabetes. Pak J Biol Sci 2008; 11(3): 351-8.[http://dx.doi.org/10.3923/pjbs.2008.351.358] [PMID: 18817155] ]. Overuse of preservatives and antibiotics in the food industry and treatment of patients have greatly expanded drug resistance [3Mahdavi S, Tanhaeivash E, Isazadeh A. Investigating the presence and expression of stx1 gene in Escherichia coli isolated from women with urinary tract infection using real-time PCR in tabriz, Iran. Int J Enteric Pathog 2018; 6(4): 104-7.[http://dx.doi.org/10.15171/ijep.2018.26] ]. Therefore, natural resources, especially medicinal and edible plants have been considered as ecological reservoirs [4Farshbaf Derhami S, Ghiami Rad M, Mahmoudi R, Asadi Nadari MR. Comparaitive studies of antibacterial activity of extracts Nasturtium Officinale and Coriandrum Sativum against some of pathogenic bacteria. J Vet Microbiol 2017; 13(2): 47-55.]. Due to the tendency of people to consume food with natural preservatives, plant sources are not only used as flavoring, but are also used as antimicrobial compounds [5Meng F, Zuo G, Hao X, et al. Antifungal activity of the benzo[c]phenanthridine alkaloids from Chelidonium majus Linn against resistant clinical yeast isolates. J Ethnopharmacol 2009; 125(3): 494-6.[http://dx.doi.org/10.1016/j.jep.2009.07.029] [PMID: 19647059] ]. 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 [7Zargari F, Ghorbanihaghjo A, Babaei H, Farajnia S, Roodbari NH. The effect of hydroalcoholic extract of Nasturtium officinale R. Br on antioxidant status and DNA damage in liver and kidney rats exposed to arsenic. Med J Tabriz Univ Med Sci 2014; 36(3): 44-9., 8Mahdavi S, Haj Azimian S, Isazadeh A, Babashpour M, Shishehgar R. Study of the antioxidant and antimicrobial effects of the ethanolic extract of Eucalyptus camaldulensis Dehnh against infectious bacteria isolated from clinical and animal sources. J Comp Pathobiol 2017; 13(4): 2063-70.]. Therefore, many plant species have been used in the food industry due to their antimicrobial and anti-oxidant properties [4Farshbaf Derhami S, Ghiami Rad M, Mahmoudi R, Asadi Nadari MR. Comparaitive studies of antibacterial activity of extracts Nasturtium Officinale and Coriandrum Sativum against some of pathogenic bacteria. J Vet Microbiol 2017; 13(2): 47-55., 6Rahman S, Parvez AK, Islam R, Khan MH. Antibacterial activity of natural spices on multiple drug resistant Escherichia coli isolated from drinking water, Bangladesh. Ann Clin Microbiol Antimicrob 2011; 10(1): 10-5.[http://dx.doi.org/10.1186/1476-0711-10-10] [PMID: 21406097] ].

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 [9Zaki AA, Elbarawy AM, Darwish AS. Biochemical studies on the effect of Nasturtium Officinalis plant extract in chickens fed raw soya bean meals. Aust J Basic Appl Sci 2011; 5: 755-61.]. For many years, N. officinale has been used to treat high blood glucose, high blood lipids, high blood pressure, and cardiovascular and pulmonary diseases [7Zargari F, Ghorbanihaghjo A, Babaei H, Farajnia S, Roodbari NH. The effect of hydroalcoholic extract of Nasturtium officinale R. Br on antioxidant status and DNA damage in liver and kidney rats exposed to arsenic. Med J Tabriz Univ Med Sci 2014; 36(3): 44-9.]. 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 [10Mohammadi J, Safari F, Rad P, Delaviz H. The effect of Hydroalcoholic extract of Nasturtium officinalis on ovarian hormonal and histological changes after toxicity by doxorubicin in rats. Majallah-i Ilmi-i Danishgah-i Ulum-i Pizishki-i Rafsanjan 2016; 14(11): 953-64.]. 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 [11Gill CI, Haldar S, Boyd LA, et al. Watercress supplementation in diet reduces lymphocyte DNA damage and alters blood antioxidant status in healthy adults. Am J Clin Nutr 2007; 85(2): 504-10.[http://dx.doi.org/10.1093/ajcn/85.2.504] [PMID: 17284750] ]. 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 [4Farshbaf Derhami S, Ghiami Rad M, Mahmoudi R, Asadi Nadari MR. Comparaitive studies of antibacterial activity of extracts Nasturtium Officinale and Coriandrum Sativum against some of pathogenic bacteria. J Vet Microbiol 2017; 13(2): 47-55., 12Omidi A, Sharifi A. Effect of methanolic extract of Nasturtium officinale on growth and biofilm formation of Pseudomonas aeruginosa. Majallah-i Danishgah-i Ulum-i Pizishki-i Gurgan 2018; 20(2): 102-8.].

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 properties 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 Ghoshun 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 positive 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 antioxidants 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 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.


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.


Table 3
Comparison of antioxidant effect of N. officinale ethanolic extract with BHT.


4. DISCUSSION

Recently, secondary metabolites of medicinal plants such as essential oils and extracts have been investigated for antimicrobial effects [13Tepe B, Donmez E, Unlu M, et al. Antimicrobial and antioxidative activities of the essential oils and methanol extracts of Salvia cryptantha (Montbret et Aucher ex Benth.) and Salvia multicaulis (Vahl). Food Chem 2004; 84(4): 519-25.[http://dx.doi.org/10.1016/S0308-8146(03)00267-X] ], 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 [14Kordali S, Kotan R, Mavi A, Cakir A, Ala A, Yildirim A. Determination of the chemical composition and antioxidant activity of the essential oil of Artemisia dracunculus and of the antifungal and antibacterial activities of Turkish Artemisia absinthium, A. dracunculus, Artemisia santonicum, and Artemisia spicigera essential oils. J Agric Food Chem 2005; 53(24): 9452-8.[http://dx.doi.org/10.1021/jf0516538] [PMID: 16302761] ]. Therefore, essential oil of medicinal plants has been used in pharmacological fields, herbal pharmacology, clinical microbiology, phytopathology, and food, fruits and vegetables preservatives [15Daferera DJ, Ziogas BN, Polissiou MG. GC-MS analysis of essential oils from some Greek aromatic plants and their fungitoxicity on Penicillium digitatum. J Agric Food Chem 2000; 48(6): 2576-81.[http://dx.doi.org/10.1021/jf990835x] [PMID: 10888587] ]. 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 [16Banerjee S, Banerjee RP, Pradhan NK. A comparative study on antimicrobial activity of leaf extract of five medicinal plants and commonly used antibiotics. Am J Phytomed Clin Ther 2014; 2(6): 788-95.]. 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 [17Lanciotti R, Belletti N, Patrignani F, Gianotti A, Gardini F, Guerzoni ME. Application of hexanal, E-2-hexenal, and hexyl acetate to improve the safety of fresh-sliced apples. J Agric Food Chem 2003; 51(10): 2958-63.[http://dx.doi.org/10.1021/jf026143h] [PMID: 12720377] ].

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 [17Lanciotti R, Belletti N, Patrignani F, Gianotti A, Gardini F, Guerzoni ME. Application of hexanal, E-2-hexenal, and hexyl acetate to improve the safety of fresh-sliced apples. J Agric Food Chem 2003; 51(10): 2958-63.[http://dx.doi.org/10.1021/jf026143h] [PMID: 12720377] ]. Patrignani et al. (2008) showed the antimicrobial effects of hexanal and 2-E hexanal on S. aureus, S. enterica and E. coli strains [18Patrignani F, Iucci L, Belletti N, Gardini F, Guerzoni ME, Lanciotti R. Effects of sub-lethal concentrations of hexanal and 2-(E)-hexenal on membrane fatty acid composition and volatile compounds of Listeria monocytogenes, Staphylococcus aureus, Salmonella enteritidis and Escherichia coli. Int J Food Microbiol 2008; 123(1-2): 1-8.[http://dx.doi.org/10.1016/j.ijfoodmicro.2007.09.009] [PMID: 180550 50] ]. 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 [19Cha JD, Jeong MR, Jeong SI, et al. Chemical composition and antimicrobial activity of the essential oils of Artemisia scoparia and A. capillaris. Planta Med 2005; 71(2): 186-90.[http://dx.doi.org/10.1055/s-2005-837790] [PMID: 15729631] ]. 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 [19Cha JD, Jeong MR, Jeong SI, et al. Chemical composition and antimicrobial activity of the essential oils of Artemisia scoparia and A. capillaris. Planta Med 2005; 71(2): 186-90.[http://dx.doi.org/10.1055/s-2005-837790] [PMID: 15729631] ]. 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.

Table 4
The obtained compounds of N. officinale ethanolic extract using GC/MS.


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 [20Butnariu M, Bostan C. Antimicrobial and anti-inflammatory activities of the volatile oil compounds from Tropaeolum majus L.(Nasturtium). Afr J Biotechnol 2011; 10(31): 5900-9.]. 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) [21Jang M, Hong E, Kim GH. Evaluation of antibacterial activity of 3-butenyl, 4-pentenyl, 2-phenylethyl, and benzyl isothiocyanate in Brassica vegetables. J Food Sci 2010; 75(7): M412-6.[http://dx.doi.org/10.1111/j.1750-3841.2010.01725.x] [PMID: 215355 49] ], 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 [22Kil HY, Seong ES, Ghimire BK, et al. Antioxidant and antimicrobial activities of crude sorghum extract. Food Chem 2009; 115(4): 1234-9.[http://dx.doi.org/10.1016/j.foodchem.2009.01.032] -24Sun L, Zhang J, Lu X, Zhang L, Zhang Y. Evaluation to the antioxidant activity of total flavonoids extract from persimmon (Diospyros kaki L.) leaves. Food Chem Toxicol 2011; 49(10): 2689-96.[http://dx.doi.org/10.1016/j.fct.2011.07.042] [PMID: 21802475] ]. 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 antibacterial compound in food.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

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.

REFERENCES

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[2] Al-Mustafa AH, Al-Thunibat OY. Antioxidant activity of some Jordanian medicinal plants used traditionally for treatment of diabetes. Pak J Biol Sci 2008; 11(3): 351-8.[http://dx.doi.org/10.3923/pjbs.2008.351.358] [PMID: 18817155]
[3] Mahdavi S, Tanhaeivash E, Isazadeh A. Investigating the presence and expression of stx1 gene in Escherichia coli isolated from women with urinary tract infection using real-time PCR in tabriz, Iran. Int J Enteric Pathog 2018; 6(4): 104-7.[http://dx.doi.org/10.15171/ijep.2018.26]
[4] Farshbaf Derhami S, Ghiami Rad M, Mahmoudi R, Asadi Nadari MR. Comparaitive studies of antibacterial activity of extracts Nasturtium Officinale and Coriandrum Sativum against some of pathogenic bacteria. J Vet Microbiol 2017; 13(2): 47-55.
[5] Meng F, Zuo G, Hao X, et al. Antifungal activity of the benzo[c]phenanthridine alkaloids from Chelidonium majus Linn against resistant clinical yeast isolates. J Ethnopharmacol 2009; 125(3): 494-6.[http://dx.doi.org/10.1016/j.jep.2009.07.029] [PMID: 19647059]
[6] Rahman S, Parvez AK, Islam R, Khan MH. Antibacterial activity of natural spices on multiple drug resistant Escherichia coli isolated from drinking water, Bangladesh. Ann Clin Microbiol Antimicrob 2011; 10(1): 10-5.[http://dx.doi.org/10.1186/1476-0711-10-10] [PMID: 21406097]
[7] Zargari F, Ghorbanihaghjo A, Babaei H, Farajnia S, Roodbari NH. The effect of hydroalcoholic extract of Nasturtium officinale R. Br on antioxidant status and DNA damage in liver and kidney rats exposed to arsenic. Med J Tabriz Univ Med Sci 2014; 36(3): 44-9.
[8] Mahdavi S, Haj Azimian S, Isazadeh A, Babashpour M, Shishehgar R. Study of the antioxidant and antimicrobial effects of the ethanolic extract of Eucalyptus camaldulensis Dehnh against infectious bacteria isolated from clinical and animal sources. J Comp Pathobiol 2017; 13(4): 2063-70.
[9] Zaki AA, Elbarawy AM, Darwish AS. Biochemical studies on the effect of Nasturtium Officinalis plant extract in chickens fed raw soya bean meals. Aust J Basic Appl Sci 2011; 5: 755-61.
[10] Mohammadi J, Safari F, Rad P, Delaviz H. The effect of Hydroalcoholic extract of Nasturtium officinalis on ovarian hormonal and histological changes after toxicity by doxorubicin in rats. Majallah-i Ilmi-i Danishgah-i Ulum-i Pizishki-i Rafsanjan 2016; 14(11): 953-64.
[11] Gill CI, Haldar S, Boyd LA, et al. Watercress supplementation in diet reduces lymphocyte DNA damage and alters blood antioxidant status in healthy adults. Am J Clin Nutr 2007; 85(2): 504-10.[http://dx.doi.org/10.1093/ajcn/85.2.504] [PMID: 17284750]
[12] Omidi A, Sharifi A. Effect of methanolic extract of Nasturtium officinale on growth and biofilm formation of Pseudomonas aeruginosa. Majallah-i Danishgah-i Ulum-i Pizishki-i Gurgan 2018; 20(2): 102-8.
[13] Tepe B, Donmez E, Unlu M, et al. Antimicrobial and antioxidative activities of the essential oils and methanol extracts of Salvia cryptantha (Montbret et Aucher ex Benth.) and Salvia multicaulis (Vahl). Food Chem 2004; 84(4): 519-25.[http://dx.doi.org/10.1016/S0308-8146(03)00267-X]
[14] Kordali S, Kotan R, Mavi A, Cakir A, Ala A, Yildirim A. Determination of the chemical composition and antioxidant activity of the essential oil of Artemisia dracunculus and of the antifungal and antibacterial activities of Turkish Artemisia absinthium, A. dracunculus, Artemisia santonicum, and Artemisia spicigera essential oils. J Agric Food Chem 2005; 53(24): 9452-8.[http://dx.doi.org/10.1021/jf0516538] [PMID: 16302761]
[15] Daferera DJ, Ziogas BN, Polissiou MG. GC-MS analysis of essential oils from some Greek aromatic plants and their fungitoxicity on Penicillium digitatum. J Agric Food Chem 2000; 48(6): 2576-81.[http://dx.doi.org/10.1021/jf990835x] [PMID: 10888587]
[16] Banerjee S, Banerjee RP, Pradhan NK. A comparative study on antimicrobial activity of leaf extract of five medicinal plants and commonly used antibiotics. Am J Phytomed Clin Ther 2014; 2(6): 788-95.
[17] Lanciotti R, Belletti N, Patrignani F, Gianotti A, Gardini F, Guerzoni ME. Application of hexanal, E-2-hexenal, and hexyl acetate to improve the safety of fresh-sliced apples. J Agric Food Chem 2003; 51(10): 2958-63.[http://dx.doi.org/10.1021/jf026143h] [PMID: 12720377]
[18] Patrignani F, Iucci L, Belletti N, Gardini F, Guerzoni ME, Lanciotti R. Effects of sub-lethal concentrations of hexanal and 2-(E)-hexenal on membrane fatty acid composition and volatile compounds of Listeria monocytogenes, Staphylococcus aureus, Salmonella enteritidis and Escherichia coli. Int J Food Microbiol 2008; 123(1-2): 1-8.[http://dx.doi.org/10.1016/j.ijfoodmicro.2007.09.009] [PMID: 180550 50]
[19] Cha JD, Jeong MR, Jeong SI, et al. Chemical composition and antimicrobial activity of the essential oils of Artemisia scoparia and A. capillaris. Planta Med 2005; 71(2): 186-90.[http://dx.doi.org/10.1055/s-2005-837790] [PMID: 15729631]
[20] Butnariu M, Bostan C. Antimicrobial and anti-inflammatory activities of the volatile oil compounds from Tropaeolum majus L.(Nasturtium). Afr J Biotechnol 2011; 10(31): 5900-9.
[21] Jang M, Hong E, Kim GH. Evaluation of antibacterial activity of 3-butenyl, 4-pentenyl, 2-phenylethyl, and benzyl isothiocyanate in Brassica vegetables. J Food Sci 2010; 75(7): M412-6.[http://dx.doi.org/10.1111/j.1750-3841.2010.01725.x] [PMID: 215355 49]
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Endorsements



"Open access will revolutionize 21st century knowledge work and accelerate the diffusion of ideas and evidence that support just in time learning and the evolution of thinking in a number of disciplines."


Daniel Pesut
(Indiana University School of Nursing, USA)

"It is important that students and researchers from all over the world can have easy access to relevant, high-standard and timely scientific information. This is exactly what Open Access Journals provide and this is the reason why I support this endeavor."


Jacques Descotes
(Centre Antipoison-Centre de Pharmacovigilance, France)

"Publishing research articles is the key for future scientific progress. Open Access publishing is therefore of utmost importance for wider dissemination of information, and will help serving the best interest of the scientific community."


Patrice Talaga
(UCB S.A., Belgium)

"Open access journals are a novel concept in the medical literature. They offer accessible information to a wide variety of individuals, including physicians, medical students, clinical investigators, and the general public. They are an outstanding source of medical and scientific information."


Jeffrey M. Weinberg
(St. Luke's-Roosevelt Hospital Center, USA)

"Open access journals are extremely useful for graduate students, investigators and all other interested persons to read important scientific articles and subscribe scientific journals. Indeed, the research articles span a wide range of area and of high quality. This is specially a must for researchers belonging to institutions with limited library facility and funding to subscribe scientific journals."


Debomoy K. Lahiri
(Indiana University School of Medicine, USA)

"Open access journals represent a major break-through in publishing. They provide easy access to the latest research on a wide variety of issues. Relevant and timely articles are made available in a fraction of the time taken by more conventional publishers. Articles are of uniformly high quality and written by the world's leading authorities."


Robert Looney
(Naval Postgraduate School, USA)

"Open access journals have transformed the way scientific data is published and disseminated: particularly, whilst ensuring a high quality standard and transparency in the editorial process, they have increased the access to the scientific literature by those researchers that have limited library support or that are working on small budgets."


Richard Reithinger
(Westat, USA)

"Not only do open access journals greatly improve the access to high quality information for scientists in the developing world, it also provides extra exposure for our papers."


J. Ferwerda
(University of Oxford, UK)

"Open Access 'Chemistry' Journals allow the dissemination of knowledge at your finger tips without paying for the scientific content."


Sean L. Kitson
(Almac Sciences, Northern Ireland)

"In principle, all scientific journals should have open access, as should be science itself. Open access journals are very helpful for students, researchers and the general public including people from institutions which do not have library or cannot afford to subscribe scientific journals. The articles are high standard and cover a wide area."


Hubert Wolterbeek
(Delft University of Technology, The Netherlands)

"The widest possible diffusion of information is critical for the advancement of science. In this perspective, open access journals are instrumental in fostering researches and achievements."


Alessandro Laviano
(Sapienza - University of Rome, Italy)

"Open access journals are very useful for all scientists as they can have quick information in the different fields of science."


Philippe Hernigou
(Paris University, France)

"There are many scientists who can not afford the rather expensive subscriptions to scientific journals. Open access journals offer a good alternative for free access to good quality scientific information."


Fidel Toldrá
(Instituto de Agroquimica y Tecnologia de Alimentos, Spain)

"Open access journals have become a fundamental tool for students, researchers, patients and the general public. Many people from institutions which do not have library or cannot afford to subscribe scientific journals benefit of them on a daily basis. The articles are among the best and cover most scientific areas."


M. Bendandi
(University Clinic of Navarre, Spain)

"These journals provide researchers with a platform for rapid, open access scientific communication. The articles are of high quality and broad scope."


Peter Chiba
(University of Vienna, Austria)

"Open access journals are probably one of the most important contributions to promote and diffuse science worldwide."


Jaime Sampaio
(University of Trás-os-Montes e Alto Douro, Portugal)

"Open access journals make up a new and rather revolutionary way to scientific publication. This option opens several quite interesting possibilities to disseminate openly and freely new knowledge and even to facilitate interpersonal communication among scientists."


Eduardo A. Castro
(INIFTA, Argentina)

"Open access journals are freely available online throughout the world, for you to read, download, copy, distribute, and use. The articles published in the open access journals are high quality and cover a wide range of fields."


Kenji Hashimoto
(Chiba University, Japan)

"Open Access journals offer an innovative and efficient way of publication for academics and professionals in a wide range of disciplines. The papers published are of high quality after rigorous peer review and they are Indexed in: major international databases. I read Open Access journals to keep abreast of the recent development in my field of study."


Daniel Shek
(Chinese University of Hong Kong, Hong Kong)

"It is a modern trend for publishers to establish open access journals. Researchers, faculty members, and students will be greatly benefited by the new journals of Bentham Science Publishers Ltd. in this category."


Jih Ru Hwu
(National Central University, Taiwan)


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