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Ellahi H, Khalili Sadrabad E, Hekmatimoghaddam S H, Jebali A, Sadeghizadeh-yazdi J, Rastiani F et al . Antimicrobial Activity and Chemical Composition of Pistachia Atlantica Gum Sub Sp. Kurdica. Essential Oil. JNFS. 2019; 4 (3) :186-190
URL: http://jnfs.ssu.ac.ir/article-1-277-en.html
Zoonotic Diseases Research Center, Department of Food Hygiene and Safety, School of Public Health, Shahid Sadoughi University of Medical Sciences, Yazd, Iran.
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Antimicrobial Activity and Chemical Composition of Pistachia Atlantica Gum Sub Sp. Kurdica. Essential Oil
 
Hasan Ellahi; MSc1, Elham Khalili Sadrabad; PhD1, Seyed Hossein Hekmatimoghaddam; MD2, Ali Jebali; PhD3, Jalal Sadeghizadeh-yazdi4; PhD, Fatemeh Rastiani; MSc1 & Fateme Akrami Mohajeri; PhD*1
 
1Zoonotic Diseases Research Center, Department of Food Hygiene and Safety, School of Public Health, Shahid Sadoughi University of Medical Sciences, Yazd, Iran.
2Department of Advanced Medical Sciences and Technologies, School of Paramedicine, Shahid Sadoughi University of Medical Sciences, Yazd, Iran.
3Department of Laboratory Sciences, School of Paramedicine, Shahid Sadoughi University of Medical Sciences, Yazd, Iran.
4Departmeny of Food Sciences and Technology, School of Public Health, Shahid Sadoughi University of Medical Sciences, Yazd, Iran.
 
ARTICLE INFO   ABSTRACT
ORIGINAL ARTICLE
 
Background: Staphylococcus aureus, Salmonella enterica, Escherichia Coli (E. Coli) and Listeria monocytogenes are considered as important foodborne pathogens. Pistachia atlantica sub sp. Kurdica, called wild pistachio, has been known as an antimicrobial compound. The aim of this study was to determine the antimicrobial activity and chemical composition of this essential oil (EO) on some of foodborne pathogens. Methods: The EO of Pistachia atlantica was obtained by hydro-distillation and analyzed by GC-MASS. The antibacterial effects of Pistachia atlantica were evaluated at two concentrations of 10 and 15 µL against Staphylococcus aureus, E. Coli, Salmonella enterica, and Listeria monocytogenes using disk diffusion method. The analysis was done by SPSS. Results: In the current study, α-pinene (92.5%) and ß-pinene (1.62%) were the main components of Pistachia atlantica EO. The EO was most effective on Salmonella enterica, whereas, its effect on Listeria monocytogenes was the weakest. The results showed a significant difference in reducing Salmonella enterica in comparison to others (P < 0.05). Conclusion: The EO has inhibitory effects on the studied bacteria. Therefore, this EO can be used as a natural preservative to extend the shelf life of foods.
 
Keywords: Pistachia atlantica; antimicrobial; Listeria monocytogenes; Staphylococcus aureus; Escherichia Coli; Listeria monocytogenes
Article history:
Received: 30 Dec 2017
Revised: 3 Mar 2018
Accepted: 26 May 2018
 
*Corresponding author:
Fateme.akrami@gmail.com
Zoonotic Diseases Research Center, Department of Food Hygiene and Safety, School of Public Health, Shahid Sadoughi University of Medical Sciences, Yazd, Iran.
 
 
Postal code: 1981619573
Tel: +989136517764
 
Introduction
Food can be contaminated by pathogenic bacteria including Salmonella enterica, Staphylococcus aureus, Escherichia Coli (E. Coli), and Listeria monocytogenes, which can cause several problems in gastro intestinal tract. During the last decades, extensive use of antimicrobial drugs has led to bacterial resistance in human beings (Moshafi et al., 2004). Essential oils (EO) are aromatic oils extracted from plants by different methods (Burt, 2004). Essential oils have been recognized as natural and harmless antimicrobial agents for the environment and Generally Recognized As Safe (GRAS) in food application (Nawel et al., 2013). The antibacterial effects of EOs depend on the type of plant, meteorological conditions, place of growth, as well as drying and processing methods. The use of oil plants in Iran as an antioxidant or antibiotic was traced back to ancient times (Akrami et al., 2015). Pistachio atlantica subsp. Kurdica, called Baneh, is one of the wild pistachio species (grows in Zagros forests), which belongs to the Anacardiacea family (Karimi et al., 2009). Three subspecies of cabulica, kurdica, and mutica grow in Iran. Over 1,200,000 hectares of western, central, and eastern parts of Iran are covered by kurdica and mutica subspecies (Farhoosh et al., 2008). Pistacia atlantica tree grows in the western (mainly), central, and eastern part of Iran. The local people use this tree to produce ingredients in some food, jams, and gum (Hatamnia et al., 2014). The gum obtained from this tree consists of oleoresin. This essential oil contains α-Thujene, α-Pinene, Camphorene, Sabinene, β-Pinene, Δ3-Carene Limonene, as well as alpha-tropineol, armanderen, and caprylic acid (Sharifi and Hazell, 2011). The results of previous studies show that the presence of resin in Pistachio has an inhibitory effect on the growth of clostridium botulinum, Staphylococcus aureus, E. Coli, and Streptococcus (Aksoy et al., 2006, Daifas et al., 2004). In another study, the antimicrobial activity of Pistachio atlantica Subsp., i.e., kurdica species were found to have positive results on helicobacter pylori (Sharifi and Hazell, 2011).The aim of the current study was to investigate the inhibition effect of Pistachio atlantica Subsp. Kurdica gum essential oil on staphylococcus aureus, Salmonella, E. Coli, and Listeria monocytogenes.
Materials and Methods
Preparation of the essential oil of Pistachia atlantica gum Subsp. Kurdica: Pistachia atlantica sub sp. Kurdica gum was collected from Kordestan province in Iran. The herbarium approval of the plant was confirmed by the Institute of Medicinal Plants, Medical University of Tehran, Iran. The gum was placed inside the Clevenger along with distilled water and the extraction was carried out by steam distillation method. The ratio of the achieved essence to gum weight was also calculated. The oil was kept at low temperature for further analysis (Mohajeri et al., 2018, Rahimi et al., 2019).
GC-MASS analysis of essential oil: The components of gum EO were isolated by Gas Chromatography/Mass Spectrometry (GC model 9-A, Shimadzu, Japan, and GC/MS model Varian 3400, USA) using a DB-5 column with a length of 30 m and an inner diameter of 0.25 mm. Later, these components were identified by comparing their mass spectrum with the range of combinations found in the computer database and valid compositions. The oven temperature was increased from 60 to 250 °C with an increment rate of 5 °C per minute. At the end, it was kept for 10 minutes at 250 °C. Helium carrier gas with a flow rate of 1.1 mL/min and ionization energy of 70 electron volts was used. The separation ratio was 1 to 50 and the injection volume was 100 μ (Rahimi et al., 2019, Sharifi and Hazell, 2011).
Determination of antimicrobial properties of Pistacia atlantica gum EO by disk diffusion method: In this study, four standard bacterial strains were used including Listeria monocytogenes (PTCC 1298), Escherichia coli (ATCC 2592), Staphylococcus aureus (ATCC 25923), and Salmonella enterica (PTCC 14028). At first, a microbial suspension equivalent to 0.5 McFarland turbidity standards (approximate density of 1.5×108 CFU/mL) was prepared from each strain. Then, 100 µL of each bacterial suspension with a density of 106 CFU/mL was cultured by spreading on the surface of the Mueller-Hinton agar medium. A 5-mm diameter sterile paper disk was placed on the medium and 15 µL of pure EO was injected into the disk. Plates were incubated for 24 hours at 37° C. Then, the diameter of the inhibition zone was measured. All treatments were carried out in triplicate (Akrami et al., 2015).
Data analysis: The experimental data were


 
Results
Chemical composition of Pistacia atlantica gum EO
The oil yield of the Pistacia atlantica gum EO was evaluated as 10% (w/w). About 97.02% of the components of gum EO were identified (approximately 13 compounds); of which α-pinene (92.08%) and β-pinene (1.61 %) were predominant (Table 1). Given that α-pinene was the main ingredient of Pistacia atlantica gum EO, the antimicrobial effects may be due to the presence of this component.
Antibacterial activity in disk diffusion method
The growth rates of Staphylococcus aureus, Salmonella enterica, Escherichia coli, and Listeria monocytogenes at concentration of 106 CFU/mL after 24 hours of exposure with Pistacia atlantica gum EO are shown in Figure 1. The maximum inhibition zone diameter was related to S. enterica, while the minimum value was attributed to L. monocytogenes. The results showed a significant difference in reduction of Salmonella enterica in comparison to others (P < 0.05). This result indicated that by increasing the concentration, the diameter of inhibition zone increased significantly (P < 0.05).
Discussion
Nevertheless, making definite conclusion in this regard is difficult, since other compounds such as ß-pinene, sabinene, and camphene exist in Pistacia atlantica  gum  EO, which may have  contributed to the inhibitory effect (Delazar et al., 2003, Mecherara-Idjeri et al., 2008). Minaiyan et al. reported 38 compounds in the Pistacia atlantica tree's EO, among which α-pinene (41.23%), β-pinene (6.85), and trans-verbenol (5.39%) had the highest concentrations (Minaiyan et al., 2015). In a similar study on the Pistacia atlantica composition in Marven region, Iran, α-pinene comprised about 70% of the EO (Delazar et al., 2003). This difference in amount may be due to the different species or geographic regions (Benhammou et al., 2008, Ghalem and Mohamed, 2009).
The agar diffusion test showed that Salmonella enterica had the highest sensitivity to the EO, while Listeria monocytogenes had the least sensitivity. So, it can be concluded that
the Pistacia atlantica gum EO had an inhibitory effect on both gram positive and gram negative bacteria. In a similar study, the antimicrobial
effect of Pistacia lentiscus leaf EO against gram-negative bacteria (such as pseudomonas and salmonella) and gram-positive bacteria (such
as Staphylococcus aureus, Bacillus and Enterococcus) was investigated by disk diffusion method. Salmonella and Enterobacter had a higher sensitivity to the EO (Derwich et al., 2010). The results of our study are in agreement with those reported by Gholem and Mohamed research. Their findings indicated that α-pinene had an antibacterial agent in the Pistacia atlantica's gum (Ghalem and Mohamed, 2009). The effect of EO on different bacteria may vary according to the laboratory conditions, the gum harvesting season, the gum's freshness or being processed, as well as the equipment and method of the extraction. Benhammou et al. studied the effect of Pistacia atlantica's gum on eight bacteria (E coli, Klebsiella pneumoneae, Pseudomonas aeruginosa, Salmonella typhi, Enterobacter cloacea, Proteus mirabilis, Listeria monocytogenes, and Staphylococcus aureus) using disk diffusion method. They showed that S. typhi and S. aureus had the most sensitivity, while K. pneumoneae and L. monocytogenes were the most resistant bacteria (Benhammou et al., 2008). A study on the effect of Pistacia atlantica's gum EO on Streptococcus mutans by disc diffusion method showed that by increasing the concentration from 20 to 50 mg/mL, the inhibition zone diameter increased (Delazar et al., 2003).
Conclusion
The results of this study indicated that Pistachia atlantica subsp. kurdica had inhibitory effects on Staphylococcus aureus, Salmonella enterica, Escherichia coli, and Listeria monocytogenes. Thus, by studying the organoleptic effects of Pistachia atlantica, this compound can be used as a natural preservative for increasing the shelf life of food products.
Authors’ contribution
Akrami, Hekmati moghaddam, Jebali, Sadeghizadeh Yazdi, and Khalili conceived and designed the experiments. Ellahi and Rastiani carried out the experiment. All authors contributed to the final version of the manuscript.
Acknowledgement
This manuscript is part of a MSc. thesis in food hygiene and safety department at Public Health School at Shahid Sadoughi University of Medical Sciences, Yazd, Iran.
Conflict of interests
The authors declare no conflict of interests regarding the publication of this paper.
References
Akrami F, et al. 2015. Antioxidant and antimicrobial active paper based on Zataria (Zataria multiflora) and two cumin cultivars (Cuminum cyminum). LWT-Food Science and Technology. 60 (2): 929-933.
Aksoy A, Duran N & Koksal F 2006. In vitro and in vivo antimicrobial effects of mastic chewing gum against Streptococcus mutans and mutans streptococci. Archives of Oral Biology. 51 (6): 476-481.
Benhammou N, Bekkara FA & Panovska TK 2008. Antioxidant and antimicrobial activities of the Pistacia lentiscus and Pistacia atlantica extracts. African Journal of Pharmacy and Pharmacology. 2 (2): 022-028.
Burt S 2004. Essential oils: their antibacterial properties and potential applications in foods—a review. International Journal of Food Microbiology. 94 (3): 223-253.
Daifas DP, et al. 2004. Effects of mastic resin and its essential oil on the growth of proteolytic Clostridium botulinum. International Journal of Food Microbiology. 94 (3): 313-322.
Delazar A, Nazemieh H, Modaresi M & Afshar J 2003. Study on essential oil obtained from oleoresin of Pistacia atlantica var. mutica.
Derwich E, Manar A, Benziane Z & Boukir A 2010. GC/MS analysis and in vitro antibacterial activity of the essential oil isolated from leaf of Pistacia lentiscus growing in Morocoo. World Applied Sciences Journal. 8 (10): 1267-1276.
Farhoosh R, Tavakoli J & Khodaparast MHH 2008. Chemical composition and oxidative stability of kernel oils from two current subspecies of Pistacia atlantica in Iran. Journal of the American Oil Chemists' Society. 85 (8): 723.
Ghalem B & Mohamed B 2009. Antimicrobial activity evaluation of the oleoresin oil of Pistacia vera L. African Journal of Pharmacy and Pharmacology. 3 (3): 092-096.
Hatamnia AA, Abbaspour N & Darvishzadeh R 2014. Antioxidant activity and phenolic profile of different parts of Bene (Pistacia atlantica subsp. kurdica) fruits. Food Chemistry. 145: 306-311.
Karimi H, Zamani Z, Ebadi A & Fatahi M 2009. Morphological diversity of Pistacia species in Iran. Genetic Resources and Crop Evolution. 56 (4): 561-571.
Mecherara-Idjeri S, Hassani A, Castola V & Casanova J 2008. Composition of leaf, fruit and gall essential oils of Algerian Pistacia atlantica Desf. Journal of Essential Oil Research. 20 (3): 215-219.
Minaiyan M, Karimi F & Ghannadi A 2015. Anti-inflammatory effect of Pistacia atlantica subsp. kurdica volatile oil and gum on acetic acid-induced acute colitis in rat. Research Journal of Pharmacognosy. 2 (2): 1-12.
Mohajeri FA, et al. 2018. The effect of Zataria multiflora Boiss Essential oil on the growth and citrinin production of Penicillium citrinum in culture media and cheese. Food and Chemical Toxicology.
Moshafi MH, Mehrabani M & Zolhasab H 2004. Antibacterial activity studies of Salvia Mirzayanii and Salvia Atropatana against six standard gram-positive and gram-negative bacteria. Journal of Kerman University of Medical Sciences. 11 (2).
Nawel M, ElAmine D, Hocine A & Boufeldja T 2013. Comparative analysis of essential oil components of two Daucus species from algeria and their antimicrobial activity. International Research Journal of Biological Sciences. 2 (1): 22-29.
Rahimi V, et al. 2019. Chemical Composition and Antifungal Activity of Essential Oil of Zataria Multiflora. Journal of Nutrition and Food Security. 4 (1): 1-6.
Sharifi MS & Hazell SL 2011. GC-MS Analysis and Antimicrobial activity of the essential oil of the trunk exudates from Pistacia atlantica kurdica. Journal of Pharmaceutical Sciences and Research. 3 (8): 1364.

 
Type of article: orginal article | Subject: public specific
Received: 2017/12/30 | Accepted: 2018/05/26 | Published: 2019/08/1

References
1. Akrami F, et al. 2015. Antioxidant and antimicrobial active paper based on Zataria (Zataria multiflora) and two cumin cultivars (Cuminum cyminum). LWT-Food Science and Technology. 60 (2): 929-933.
2. Aksoy A, Duran N & Koksal F 2006. In vitro and in vivo antimicrobial effects of mastic chewing gum against Streptococcus mutans and mutans streptococci. Archives of Oral Biology. 51 (6): 476-481.
3. Benhammou N, Bekkara FA & Panovska TK 2008. Antioxidant and antimicrobial activities of the Pistacia lentiscus and Pistacia atlantica extracts. African Journal of Pharmacy and Pharmacology. 2 (2): 022-028.
4. Burt S 2004. Essential oils: their antibacterial properties and potential applications in foods—a review. International Journal of Food Microbiology. 94 (3): 223-253.
5. Daifas DP, et al. 2004. Effects of mastic resin and its essential oil on the growth of proteolytic Clostridium botulinum. International Journal of Food Microbiology. 94 (3): 313-322.
6. Delazar A, Nazemieh H, Modaresi M & Afshar J 2003. Study on essential oil obtained from oleoresin of Pistacia atlantica var. mutica.
7. Derwich E, Manar A, Benziane Z & Boukir A 2010. GC/MS analysis and in vitro antibacterial activity of the essential oil isolated from leaf of Pistacia lentiscus growing in Morocoo. World Applied Sciences Journal. 8 (10): 1267-1276.
8. Farhoosh R, Tavakoli J & Khodaparast MHH 2008. Chemical composition and oxidative stability of kernel oils from two current subspecies of Pistacia atlantica in Iran. Journal of the American Oil Chemists' Society. 85 (8): 723.
9. Ghalem B & Mohamed B 2009. Antimicrobial activity evaluation of the oleoresin oil of Pistacia vera L. African Journal of Pharmacy and Pharmacology. 3 (3): 092-096.
10. Hatamnia AA, Abbaspour N & Darvishzadeh R 2014. Antioxidant activity and phenolic profile of different parts of Bene (Pistacia atlantica subsp. kurdica) fruits. Food Chemistry. 145: 306-311.
11. Karimi H, Zamani Z, Ebadi A & Fatahi M 2009. Morphological diversity of Pistacia species in Iran. Genetic Resources and Crop Evolution. 56 (4): 561-571.
12. Mecherara-Idjeri S, Hassani A, Castola V & Casanova J 2008. Composition of leaf, fruit and gall essential oils of Algerian Pistacia atlantica Desf. Journal of Essential Oil Research. 20 (3): 215-219.
13. Minaiyan M, Karimi F & Ghannadi A 2015. Anti-inflammatory effect of Pistacia atlantica subsp. kurdica volatile oil and gum on acetic acid-induced acute colitis in rat. Research Journal of Pharmacognosy. 2 (2): 1-12.
14. Mohajeri FA, et al. 2018. The effect of Zataria multiflora Boiss Essential oil on the growth and citrinin production of Penicillium citrinum in culture media and cheese. Food and Chemical Toxicology.
15. Moshafi MH, Mehrabani M & Zolhasab H 2004. Antibacterial activity studies of Salvia Mirzayanii and Salvia Atropatana against six standard gram-positive and gram-negative bacteria. Journal of Kerman University of Medical Sciences. 11 (2).
16. Nawel M, ElAmine D, Hocine A & Boufeldja T 2013. Comparative analysis of essential oil components of two Daucus species from algeria and their antimicrobial activity. International Research Journal of Biological Sciences. 2 (1): 22-29.
17. Rahimi V, et al. 2019. Chemical Composition and Antifungal Activity of Essential Oil of Zataria Multiflora. Journal of Nutrition and Food Security. 4 (1): 1-6.
18. Sharifi MS & Hazell SL 2011. GC-MS Analysis and Antimicrobial activity of the essential oil of the trunk exudates from Pistacia atlantica kurdica. Journal of Pharmaceutical Sciences and Research. 3 (8): 1364.

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