Food Bioscience 34 (2020) 100510

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Food Bioscience
journal homepage: www.elsevier.com/locate/fbio

Composition, phenolic content, antioxidant and antimicrobial activity of T

Pistacia atlantica subsp. kurdica hulls’ essential oil
Seyedeh-Maryam Hasheminya, Jalal Dehghannya∗
Department of Food Science and Technology, University of Tabriz, Tabriz, 51666-16471, Iran

A R T I C LE I N FO A B S T R A C T

Keywords: Chemical compounds, total phenolic content, antioxidant and antimicrobial activity of Pistacia atlantica subsp.
α-Pinene kurdica hulls’ essential oil (EO) was investigated. The EO was extracted using hydrodistillation and its GC-MS
Bene analysis showed 95 compounds, the most important of which were α-pinene (10.8%), β-citral (7.0%), carvone
Essential oil hydrate (4.4%), myristic acid (4.9%), p-acetyltoluene (3.5%), pinocarveol (3.3%) and palustrol (3.3%). Total
Pistacia atlantica
phenolic compounds in the EO was 178 mg GAE/100 g dry weight (dw). Antioxidant activity of the EO was
Wild pistachio
measured using two methods: The FRAP (ferric reducing antioxidant power) assay and the DPPH free radical
scavenging activity. The FRAP value was 6.24 mg/g, and the IC50 value using the DPPH method was 25.2 mg/
mL. In addition, using broth microdilution and disc diffusion techniques, the antimicrobial activity of the EO
against Escherichia coli, Pseudomonas aeruginosa, Salmonella Typhimurium, Streptococcus faecalis, Bacillus cereus,
Staphylococcus aureus and Candida albicans was investigated. The minimum inhibitory concentration of the EO
was between 0.13 mg/mL (C. albicans) and 0.42 mg/mL (E. coli). Moreover, the lowest minimum microbicidal
concentration of the EO (0.16 mg/mL) was with C. albicans and the highest of 0.52 mg/mL was with E. coli.
Furthermore, the highest inhibition zone of 24.2 mm was with C. albicans and the lowest inhibition zone of
20.8 mm was with E. coli.

1. Introduction diabetes, cancer and cardiovascular disease (Rezaie et al., 2015a,

One of the ways to control the growth of food pathogenic micro-
organisms is to use antimicrobial preservatives and chemical com-
pounds (Hasheminya et al., 2019a). There are some concerns about the
effects of chemical preservatives, so some consumers are interested in
replacing chemical antimicrobials with natural compounds (Houicher,
Hamdi, Hechachna, & Özogul, 2018). Herbal essential oils are natural
antimicrobials (Hasheminya et al., 2019b). Essential oils are secondary
metabolites of medicinal plants that are found in different parts of the
plants such as skins, roots, leaves, stems, fruits, seeds and plant flowers.
Environmental factors have an important role in the production and
accumulation of secondary metabolites of medicinal plants. Factors
such as temperature, rainfall, light intensity and altitude, which de-
termine the climate of an area, are among the environmental factors
affecting the accumulation of secondary metabolites (Burt, 2004;
Rezaie, Farhoosh, Ali Sharif, Asili, & Iranshahi, 2015a; Taghizadeh
et al., 2018a).
Essential oils (EO) are prepared from the raw material using hy-
drodistillation, steam distillation, “dry” distillation or mechanical pro-
cesses (Council of Europe, 2011). EO reduce the risk of diseases such as
2015b). Along with the antibacterial properties of EO, antiviral, anti-
fungal, antitoxigenic, antiparasitic and insecticidal effects have also
been reported (Burt, 2004).
Pistacia atlantica named Bene (regardless of subspecies) in Iran is a
high-altitude tree with a height of 2–7 m and is one of the species of
wild pistachios from the Anacardiaceae family. The plant has been
naturally spread to the Canary Islands, Mediterranean countries, Syria,
the Caucasus, Iran, Afghanistan and Pakistan (Gourine, Yousfi,
Bombarda, Nadjemi, & Gaydou, 2010a). P. atlantica has 4 subspecies
including kurdica, cabulica, atlantica and mutica. P. atlantica subsp.
kurdica (PAK) is a tree which grows wild in the Zagros region of Iran at
altitudes of 600–3000 m above sea level. P. atlantica subsp. atlantica
grows in North Africa. The covered area of the three subspecies (kur-
dica, cabulica and mutica rootstocks) in Iran is over 1.2 million hectares
(Hatamnia, Abbaspour, & Darvishzadeh, 2014). P. atlantica fruit con-
sists of three parts including the kernel (25%), a rigid wooden shell
(51%) and a soft outer hull (24%). The outer hull is green, has about
30% oil that can be observed by squeezing the hull between two fingers.
The oil is easily removed from the green hull. Native people of Iran use
the oil obtained from the kernel and hull of the fruit to fry food. It is

∗
Corresponding author.
E-mail address: J_dehghannya@tabrizu.ac.ir (J. Dehghannya).

https://doi.org/10.1016/j.fbio.2019.100510
Received 17 December 2018; Received in revised form 14 December 2019; Accepted 20 December 2019
Available online 26 December 2019
2212-4292/ © 2019 Elsevier Ltd. All rights reserved.
S.-M. Hasheminya and J. Dehghannya
also used in traditional medicine for the treatment of eczema, throat
infection, kidney stones and asthma, as well as having styptic, anti-
inflammatory, antipyretic, antibacterial and antiviral activities (Rezaie
et al., 2015b).
Salimi, Shafaghat, Sahebalzamani, and Alizadeh (2011) reported α-
pinene (87.9%) as the main component from PAK. The other major
components were β-pinene (7.4%), camphene (2.7%) and verbenone
(2.5%). Sharifi and Hazell (2011) did GC-MS analysis and investigated
antimicrobial activity of the EO of the trunk exudates from PAK. α-
Pinene (97.2%) was the main constituent of the essential oil with an-
timicrobial property. Hesami, Bahramian, Fatemi, and Hesami (2014)
studied the effect of PAK's EO on Botrytis cinerea mold growth in culture
media and on strawberry fruits. The EO showed antifungal activity
against B. cinerea and was recommended as a natural inhibitor to
control the growth of molds on fruits such as strawberries. Minaiyan,
Karimi, and Ghannadi (2015) measured the anti-inflammatory effect of
PAK volatile oil and gum on acetic acid-induced acute colitis in rat. α-
Pinene was the main component of the volatile EO (41.2%). The oral
gum and volatile oil decreased all indices of colitis and myeloperox-
idase activity. Shahghobadi, Shabanian, Shafie Rahmani, and Khadivi
(2018) reported genetic characterization of PAK from the northern
Zagros forests in Iran. Although some studies have been done to in-
vestigate the chemical and antioxidant compounds of the EO of P.
atlantica subsp. mutica and P. khinjuk (Rezaie et al., 2015a; Taghizadeh
et al., 2018a), no information is available on chemical compositions,
antimicrobial and antioxidant properties of PAK fruit's hull (PAKH).
The purpose of this study was to measure the chemical compounds of
the EO, to measure its antioxidant activity based on the FRAP (ferric
reducing antioxidant power) assay and DPPH radical scavenging ac-
tivity, to measure its total phenolic compounds and antimicrobial ac-
tivity using broth microdilution and disc diffusion methods on Gram-
negative (Escherichia coli, Pseudomonas aeruginosa, Salmonella Typhi-
murium) and Gram-positive (Streptococcus faecalis, Bacillus cereus, Sta-
phylococcus aureus) bacterial strains and one fungi strain (Candida al-
bicans).
2. Material and methods
2.1. Materials
Ripe Bene fruits from 10 wild trees (2–7 m height) were collected at
all tree levels in October 2017 from Ilam city in Iran (latitude 33°38′ N,
longitude 46°25′ E). A specimen of the fruit was validated by the her-
barium staff of the Faculty of Pharmacy, Tabriz University of Medical
Sciences, Tabriz, Iran. The fruits were dried at room temperature
(25 ± 1 °C) for 72 h and their hulls were manually removed from the
fruits and then ground for 1 min (Model Pulverisette 14, Fritsch
Industries, Idar-Oberstein, Germany) and passed through a 40 mesh
size. Microbial strains of E. coli (ATCC 25922), P. aeruginosa (ATCC
27853), S. Typhimurium (ATCC 14028), S. faecalis (PTCC 1237), B.
cereus (ATCC 11778), S. aureus (ATCC 25923), and C. albicans (ATCC
1677) were obtained from the Iranian Research Organization for
Science and Technology (IROST, Tehran, Iran). Ferric chloride hex-
ahydrate, 2,4,6-Tris(2-pyridyl)-s-triazine (TPTZ, purity > 99%), me-
thanol (purity > 99.8%), Folin-Ciocalteu reagent, sodium carbonate,
gallic acid (GA), butylated hydroxytoluene (BHT, purity > 99.0%), 2,2-
diphenyl-1-picyrylhydrazyl (DPPH, purity > 98%), sodium acetate tri-
hydrate, hydrochloric acid and ascorbic acid (AA) (Sigma Aldrich Co.,
St. Louis, Missouri, USA), anhydrous sodium sulfate, dimethyl sulfoxide
(DMSO, purity > 99.8%), Muller-Hinton agar, Muller-Hinton broth and
Sabouraud dextrose agar (Merck, Darmstadt, Germany), streptomycin
and ketoconazole antibiotics (Mast Laboratories Ltd., Liverpool, UK)
were used.
2
Food Bioscience 34 (2020) 100510
2.2. Extraction and measurement of EO compounds from the hulls
The ground hulls (200 g) were immersed in 500 mL distilled water
and the EO of the fruits’ hulls was obtained using hydrodistillation for
5 h using a Clevenger-type apparatus (Schott Duran, Mainz, Germany).
The extracted EO was transferred to a glass vial and purified by se-
paration of the remnant water by freezing at −20 °C, and the EO, which
remain liquid, was drained from the vial. Afterwards, the EO was de-
hydrated using anhydrous sodium sulfate and after filtering through a
0.22 μm PVDF syringe filter (Millipore Iberica SA, Madrid, Spain) was
kept in dark glass containers in the refrigerator at 4 °C for 48 h
(Mirahmadi & Norouzi, 2017).
Measurement of EO extracts was done using a gas chromatograph
(GC) (Model GC-17A, Version 3, Shimadzu Inc., Shimadzu, Japan)
connected to a mass spectrometer (Model QP-5050A) equipped with a
DB-5 column (polydimethylsiloxane, dimensions: 60 m × 0.25 mm,
film thickness 0.25 μm) (J&W Scientific, Folsom, California, USA) and a
flame ionization detector which was operated in the EI (electron ioni-
zation) mode at 70 eV. Helium was used as the carrier gas for the GC at
a flow rate of 1.2 mL/min. The oven temperature was kept at 50 °C for
3 min. Then, the temperature was increased by 3 °C/min up to 240 °C
and kept at this temperature for 8 min. The injector and detector
temperatures were 230 and 270 °C, respectively. The split ratio was
adjusted to 1:10 and the injected volume was 1 μL of 10% EO in n-
hexane. To calculate retention indices, injection of n-alkanes (C8–C30)
(Sigma-Aldrich, Steinheim, Germany) was done with similar tempera-
ture conditions. Then, the Kovats retention indices of the compounds
were calculated (Adams, 2007; Rezaie et al., 2015a):
I= 100× [ n+ ( N− n) (log t unknown − log t n)/(log tN − log t n )]
where I is the Kovats retention index, n represents the number of carbon
atoms in the smaller n-alkane, N is the number of carbon atoms in the
larger n-alkane, and t represents the retention time of the related
compounds. Identification of compounds was done by comparing mass
spectra and retention indices using authentic samples (α-pinene, β-ci-
tral and limonene, Sigma Aldrich Co., USA) and available data in the
literature (Adams, 2007) as well as by computer matching using the
NIST 21 and NIST 107 (https://chemdata.nist.gov/) and WILEY229
(https://www.sisweb.com/software/wiley-registry.htm) libraries
(Babahmad et al., 2018; NIST Chemistry WebBook, 2013). Xcalibur
software (version 2.1, Thermo Fisher Scientific, San Jose, California,
USA) was used for data analysis.
2.3. Measurement of EO yield
The yield of EO (REO, %) was calculated as follows:
mEO
REO (%) = × 100
ms
where mEO and ms represent the mass of EO (g) and dried hulls (g),
respectively (Boutekedjiret, Bentahar, Belabbes, & Bessiere, 2003).
2.4. Measurement of total phenolic compounds (TPC)
The Folin-Ciocalteu method with some modifications was used to
determine the TPC of the EO (Chrysargyris, Xylia, Botsaris, &
Tzortzakis, 2017; Muanda, Soulimani, Diop, & Dicko, 2011). The Folin-
Ciocalteu reagent (25 μL) was mixed with 10 μL EO and then, the
mixture was incubated at 25 °C for 5 min. Afterwards, 25 μL 20% (w/v)
sodium carbonate solution and 140 μL distilled water were added. After
30 min, the absorbance of samples was measured at 760 nm using a
Synergy H4 Microplate Reader (BioTek Instruments Inc., Winooski,
Vermont, USA). Standard curves were prepared using GA (0–250 μg/
mL) and the results was expressed in mg GA equivalence (GAE)/100 g
dw. The GAE was obtained using the following linear equation for the
standard curve:
S.-M. Hasheminya and J. Dehghannya
y = 0.0747x + 0.0325 (R2 = 0.9935)
where y and x represent the absorbance and concentration (μg/mL) of
GA, respectively.
2.5. Measurement of antioxidant activity using the DPPH method
The antioxidant capacity of the EO was measured using the DPPH
free radical scavenging activity. Fifty μL of EO at different concentra-
tions (100, 50, 25, 12.5 and 6.25 μg/mL) was mixed with 2 mL of the
60 μM DPPH methanol solution. The samples were shaken in the dark at
room temperature (25 ± 1 °C) for 30 min using a shaker incubator
(Model G25 & R25, New Brunswick Scientific, Edison, New Jersey,
USA). The absorbance of samples was read at 517 nm using a spec-
trophotometer (Model 8453, Agilent Technologies, Santa Clara,
California, USA). BHT was used as a positive control. The percentage of
free radical inhibition was calculated using (Babahmad et al., 2018;
Hasheminya & Dehghannya, 2019):
A − AS ⎞
DPPH inhibition percentage (%) = ⎛ DPPH
⎜ × 100
⎟
⎝ ADPPH ⎠
where, ADPPH is the absorbance of the DPPH solution with EO, and AS is
the absorbance of the DPPH solution without EO. After measuring the
DPPH scavenging activity, IC50 was calculated, which represents a
concentration of EO that can inhibit 50% of the free radicals.
2.6. Measurement of antioxidant activity using the FRAP assay
The FRAP reagent was prepared by mixing 10 mL 300 mM acetate
buffer at pH = 3.6 (3.1 g sodium acetate trihydrate), 1 mL 10 mM TPTZ
solution (dissolved in 40 mM hydrochloric acid) and 1 mL 20 mM ferric
chloride hexahydrate (dissolved in distilled water). Then, 10 μL of
different concentrations of EO (100, 50, 25, 12.5 and 6.25 mg/mL)
were added to 190 μL of the FRAP solution. After 30 min at 37 °C, the
absorbance was read at 593 nm using the microplate reader. The
standard curve was prepared using AA (0–250 μg/mL) and the results
were expressed in mg AA/g dw. The antioxidant power of the EO was
compared with BHT as the reference antioxidant (Hatamnia et al.,
2014; Rezaie et al., 2015a).
2.7. Measurement of antimicrobial properties
2.7.1. Broth microdilution method
Assessment of minimum inhibitory concentration (MIC) and
minimum microbicidal concentration (MMC) of the EO was done using
a broth microdilution method using a 96-well plate. The EO at 4 mg/mL
(highest concentration) was prepared by diluting it in 5% DMSO (di-
methyl sulfoxide). In the first well of each column, only 200 μL of the
EO was added at 4 mg/mL. Then, in all the other wells, 90 μl of the
Muller-Hinton broth culture medium for bacteria and 90 μL of the
Sabouraud dextrose agar culture medium for the fungus were added.
Then, 100 μL in the wells located in the first column containing the EO
was transferred to all the wells located in the second column containing
the culture medium and after mixing the EO and the medium, 100 μL of
the mixture was transferred to all the wells located in the third column,
and this procedure was continued until the last dilution of the EO.
Afterwards, 100 μL from all the wells in the last column was removed
and discarded. Then, 10 μL of bacterial suspensions (having a 0.5
McFarland value (Hasheminya et al., 2019a)), equivalent to
5 × 106 CFU/mL and 10 μL of fungal suspension equivalent to
5 × 103 CFU/mL were added to the wells of the culture medium
containing different concentrations of EO, so that the final volume in
each well became 100 μL. The plates were then covered with sterile
plastic caps and incubated at 37 °C for 24 h for bacterial specimens and
at 25 °C for 48 h for fungal samples. The lowest concentration in which
no microorganism growth was observed was determined as the MIC
3
Food Bioscience 34 (2020) 100510
(Babahmad et al., 2018; Chrysargyris et al., 2017). Afterwards, 100 μL
of the contents of the first set of wells where the growth of each mi-
croorganism was not observed were transferred to the Muller-Hinton
agar for bacterial samples and the Sabouraud dextrose agar for the
fungus sample, and were incubated at 37 °C for 24 h and at 25 °C for
48 h, respectively. The lowest concentration of the EO without growth
was the MMC. Streptomycin and ketoconazole antibiotics were sepa-
rately used as positive controls (Table 3) (Babahmad et al., 2018).
2.7.2. Disc diffusion method
All bacteria were cultured in a Muller-Hinton agar medium at 37 °C
and the fungal specimen was cultured in a Sabouraud dextrose agar
medium at 25 °C overnight. Then, 100 μL of microbial suspensions
equivalent to 108 CFU/mL were inoculated onto the surface of the
plates containing Muller-Hinton agar for bacteria and Sabouraud dex-
trose agar for the fungal sample. Then, sterile filter paper disks (Padtan
Teb, Tehran, Iran) with a diameter of 6 mm were first impregnated with
10 μL of the EO and placed on the plates containing the culture med-
iums inoculated with microorganisms. The plates containing bacteria
were incubated at 37 °C for 24 h and the plates containing the fungal
specimen at 25 °C for 48 h. Finally, the diameter of the growth in-
hibition zones was measured using a digital caliper (accuracy: ± 0.001
inch or ± 0.0254 mm) (Model 500-196-30, Mitutoyo Co., Mitutoyo,
Japan). Streptomycin (10 μg/disc) and ketoconazole (25 μg/disc) an-
tibiotic discs were used as positive controls (Chrysargyris et al., 2017).
2.8. Statistical analysis
Statistical analysis was carried out on the measured characteristics
of the EO of Bene fruit's hull for the TPC, antioxidant and antimicrobial
activities in a completely randomized design (CRD) framework. All tests
were done with 3 replications. The mean comparison was based on
Duncan's multiple range test at the 5% probability level. Analysis and
evaluation of ANOVA (one-way) was done using the Statistical Analysis
System (SAS) software (version 9.4) (SAS Institute Inc., Cary, North
Carolina, USA).
3. Results and discussion
3.1. Chemical composition of the EO
The chemical compounds of the EO are shown in Table 1. In total,
95 chemical compounds were measured. The most prevalent com-
pounds included α-pinene, β-citral and myristic acid. In general, the
highest amounts of the EO compounds were monoterpene hydro-
carbons, oxygenated monoterpenes, sesquiterpene hydrocarbons, oxy-
genated sesquiterpenes, alcohols, aldehydes and fatty acids. In a similar
study, the major chemical compounds of the EO obtained from P.
atlantica subsp. mutica's hull were α-pinene (20.8%), camphene (8.4%),
β-myrcene (8.2%), and limonene (8%) (Rezaie et al., 2015a). In addi-
tion, Taghizadeh et al. (2018a) measured 56 compounds in the EO
obtained from P. khinjuk's hulls, and the major compounds were β-
caryophyllene (25.3%), β-myrcene (16.5%), α-pinene (15.0%) and α-
humulene (5.7%).
Chemical compounds of the EO obtained from the Pistacia leaf
species such as P. lentiscus (Aissi, Boussaid, & Chokri, 2016; Benyoussef,
Charchari, Nacer-Bey, & Yahiaoui, 2005; Boelens and Jimenez, 1991;
Gardeli, Papageorgiou, Mallouchos, Theodosis, & Komaitis, 2008; Yosr,
Imen, Rym, hokri, & Mohamed, 2018), P. khinjuk (Pooter, Schamp,
Aboutabl, Tohamy, & Doss, 1991), P. palaestina (Flamini, Bader, Cioni,
Katbeh-Bader, & Morelli, 2004), P. atlantica (Barrero et al., 2005;
Labed-Zouad et al., 2017; Sadeghi, Pourya, & Smagghe, 2016; Tzakou,
Bazos, & Yannitsaros, 2007; Zerey-Belaskri & Benhassaini, 2016), P.
terebinthus (Duru et al., 2003) and P. chinensis (Pooter et al., 1991) have
also been reported. For example, the main components of the EO ob-
tained from the P. lentiscus leaf were α-pinene (Greece and France)
S.-M. Hasheminya and J. Dehghannya Food Bioscience 34 (2020) 100510

Table 1 Table 1 (continued)

Chemical composition of Pistacia atlantica subsp. kurdica essential oil (in per-
cent) with Kovats indices (KI). No Compounds Percentage KIaa KIbb

No Compounds Percentage KIaa KIbb 74 β-Bisabolene 0.2 1510 1509

75 γ-Cadinene 3.0 1514 1513
1 1-Hexanal 0.2 798 802 76 Elemol 0.6 1548 1550
2 1-Heptanal 0.3 876 876 77 Germacrene B 2.2 1561 1561
3 α-Thujene 0.4 924 925 78 Palustrol 3.3 1568 1568
4 α-Tricyclene 0.2 926 927 79 Spathulenol 0.6 1578 1578
5 α-Pinene 10.9 939 940 80 Caryophyllene oxide 0.2 1588 1583
6 Camphene 1.0 946 946 81 Viridiflorol 0.5 1595 1587
7 Verbenene 0.2 951 951 82 1-Epi-cubenol 1.7 1628 1629
8 β-Pinene 1.3 973 975 83 Isospathulenol 2.7 1634 1639
9 β-Myrcene 0.2 991 992 84 epi-α-Cadinol 1.0 1640 1642
10 n-Octanal 1.1 1001 1001 85 α-Muurolol 0.8 1645 1646
11 α-Fellandrene 0.1 1005 1006 86 β-Eudesmol 0.2 1649 1650
12 3-Carene 0.1 1013 1011 87 α-Eudesmol 0.7 1652 1654
13 p-Cymene 0.1 1025 1026 88 α-Cadinol 0.2 1654 1662
14 β-Ocimene 0.1 1031 1031 89 α-Sinensal 1.1 1758 1756
15 Eucalyptol 0.4 1034 1035 90 Myristic acid 4.9 1768 1771
16 Limonene 0.2 1036 1039 91 Palmitic acid 0.2 1958 1972
17 Octanol 0.5 1063 1063 92 Palmitic acid, ethyl ester 0.3 1968 1975
18 γ-Terpinene 0.3 1067 1069 93 Elaidic acid 0.7 2123 –
19 Linalool oxide 0.8 1073 1073 94 Phytol 0.4 2128 2114
20 Terpinolene 0.3 1088 1089 95 Oleic Acid 0.3 2147 –
21 Nonanal 1.6 1101 1102 Total identified 100
22 Linalool 1.1 1110 1109 Classification of the constituents
23 Perillen 0.7 1114 1114 1 Monoterpene hydrocarbon 21.5
24 α-Campholenal 0.4 1127 1125 2 Oxygenated monoterpenes 20.3
25 trans-Mentha-2,8-dien-1-ol 1.8 1128 1128 3 Sesquiterpene hydrocarbon 14.1
26 Camphor 3.0 1131 1139 4 Oxygenated sesquiterpenes 3.7
27 Pinocarveol 3.4 1141 1141 5 Alcohol 12.0
28 cis-Verbenol 0.7 1143 1142 6 Aldehyde 10.9
29 Camphene hydrate 0.3 1148 1150 7 Fatty acid 6.6
30 Pinocarvone 1.0 1160 1162 8 Others 11.0
31 α-Phellandren-8-ol 0.4 1164 1166 Total identified 100c
32 Borneol 0.9 1165 1171
a
33 p-Acetyltoluene 3.5 1178 1179 KIa: Experimental Kovats indices on a DB-5 column calculated from the GC-
34 2-Methylisoborneol 1.2 1180 1180 MS chromatograms.
35 Cryptone 0.8 1185 1188 b
KIb: Published literature (NIST) Kovats indices on a DB-5 column, where
36 p-Cymen-8-ol 1.0 1189 1196
available.
37 2-Methyl-2-hexanol 1.6 1196 1196 c
38 Myrtenal 2.7 1197 1204
The relative percentage of the essential oil constituents were expressed as
39 α-Terpineol 0.6 1207 1207 percentages using peak area normalization (i.e., the total area of the peaks was
40 Nopol 0.6 1212 – used as the denominator and the individual peak as the numerator assuming all
41 Verbenone 0.3 1217 1218 peaks were proportional to the number of moles of that material).
42 trans-Carveol 0.2 1219 1229
43 Octanol acetate 0.2 1222 –
(Castola, Bighelli, & Casanova, 2000; Papageorgiou & Mellides, 1991),
44 trans-Crysanthenyl acetate 1.3 1231 1235
45 Carvone 0.2 1240 1242 d-carene (Egypt) (Pooter et al., 1991) and terpinen-4-ol, α-pinene, li-
46 Piperitone oxide 0.4 1241 – monen and β-myrcene (Corsica) (Castola et al., 2000). In addition, α-
47 Ascaridole 0.2 1248 1247 pinene has been reported as the main compound in the EO obtained
48 Geraniol 0.4 1253 1255 from P. khinjuk leaves (Pooter et al., 1991), P. atlantica leaves (Gourine
49 β-Citral 7.0 1256 1256
et al., 2010a) and P. palaestina leaves (Flamini et al., 2004). Moreover,
50 Carvenone oxide 0.2 1261 1272
51 Nonanoic acid 0.7 1267 1273 the major component in the EO obtained from the leaves of P. atlantica
52 2-Decenal 0.6 1271 1274 (Barrero et al., 2005; Tzakou et al., 2007) and P. terebinthus (Duru et al.,
53 Bornyl acetate 0.3 1286 1285 2003) was terpinen-4-ol. In addition to the above, the main compound
54 Menthyl acetate 0.4 1287 1287
of the EO from P. chinensis was trans-β-ocimene (Pooter et al., 1991).
55 Sabinyl acetate 0.7 1290 1291
56 Limonene dioxide 0.3 1294 1294 Labed-Zouad et al. (2017) reported that the main components of the
57 Pinanediol 0.4 1319 – EO extracted from P. atlantica's leaves were α-pinene, spathulenol, γ-
58 Limonene-diol 0.4 1321 1321 gurjunene and α-phellandrene. However, the main components of the
59 Citronellyl acetate 0.3 1376 1357 EO extracted from P. atlantica's flower were reported as α-pinene, α-
60 trans-Sobrerol 0.4 1386 1386
terpinene, β-phellandrene and α-phellandrene. Sadeghi et al. (2016)
61 Longifolene 0.7 1402 1408
62 Carvone hydrate 4.5 1424 1424 also reported that α-pinene was the main component of the EO ob-
63 Coumarin 0.4 1432 1432 tained from fruit, gum and leaves of PAK. Yosr et al. (2018) reported
64 γ-Elemene 1.4 1434 1437 the main components of the EO extracted from the leaves, stems,
65 Aromadendrene 1.4 1436 1438
flowers and fruit of Tunisian P. lentiscus were α-pinene, β-myrcene, α-
66 β-Humulene 0.3 1454 1454
67 α-Humulene 0.6 1455 1455
limonene and germacrene-D. Plant age, cultivation conditions, geo-
68 allo-Aromadendrene 1.6 1462 1462 graphy, temperature, day length, harvest time, plant organ where EO is
69 Ledene 0.4 1487 1490 extracted, EO extraction methods, and climatic conditions have im-
70 Guaiene 0.6 1490 1490 portant roles in EO composition. The aforementioned factors affect the
71 Epizonarene 0.3 1500 1501
biosynthesis of plant pathways and consequently the amounts of the
72 Bicyclogermacrene 0.2 1502 1502
73 Cuparene 1.5 1505 1505 major compounds, which leads to the formation of various chemotypes
(Babahmad et al., 2018; Chryssavgi, Vassiliki, Athanasios, Kibouris, &

4
S.-M. Hasheminya and J. Dehghannya
Table 2
Yield of essential oil, total phenolic compounds (TPC), DPPH free radical scavenging activity and FRAP assay of Pistacia atlantica subsp. kurdica essential oil and BHT.
Yield (% w/w, dry weight) TPC (mg GAE/100 g dry weight)
Essential oil 0.21 ± 0.05 178 ± 0.4
BHT – –
Michael, 2008; Petretto et al., 2018; Zerey-Belaskri & Benhassaini,
2016).
3.2. Evaluation of the EO yield
The yield of the EO obtained from PAKH was 0.21% (w/w, dw)
(Table 2). Chahed et al. (2007) reported the yield of the EO extracted
from P. vera L. from different Tunisian localities (Grobalia, Kairouan
and Sfax regions) at 0.14, 0.37 and 0.53%, respectively. In another
study, the yield of the EO of Tunisian pistachio fruit was studied. The
yield of the EO during fruit formation and ripening varied and was in
the range of 0.1–0.4% based on dw (Chahed et al., 2008).
3.3. Evaluation of TPC
The TPC of the EO extracted from PAKH was 178 mg GAE/100 g dw
(Table 2). Although information on the TPC of the aqueous, methanolic,
ethanolic, acetonic and hexanoic extract of various parts of PAK, P.
atlantica subsp. mutica, P. vera var. sarakhs and P. lentiscus L. have been
reported (Chryssavgi et al., 2008; Hatamnia et al., 2014, 2016; Rezaie
et al., 2015b; Taghizadeh et al., 2018b), the TPC of the EO obtained
from PAK has not yet been reported. However, there are some reports
about the TPC of the EO extracted from other plants. For example,
Muanda et al. (2011) reported that the TPC of the EO obtained from
Stevia rebaudiana bertoni's leaves was 115 mg GAE/100 g dw. In an-
other study, Mohamed et al. (2013) reported that the TPC of the EO
extracted from Syzygium cumini was 128 mg GAE/100 g dw. Khanavi
et al. (2009) reported that the TPC of the EO obtained from 7 different
Stachys species was in the range of 430–4450 mg GAE/100 g dw.
Overall, medicinal plants have high natural antioxidants, and phenolic
compounds are secondary metabolites of these plants and their amounts
depend on genetic and environmental factors (Wong, Li, Cheng, &
Chen, 2006).
3.4. Evaluation of antioxidant activity
The IC50 value of the EO obtained from PAKH derived from the
DPPH method was 25.2 mg/mL, indicating a significantly (P < 0.05)
lower antioxidant activity than BHT (0.01 mg/mL) (Table 2). Few
studies have been done regarding the evaluation of the antioxidant
properties of EO obtained from Pistacia species (Aissi et al., 2016;
Gourine et al., 2010a, 2010b; Labed-Zouad et al., 2017; Rezaie et al.,
2015a). Generally, results of the DPPH test represented a weak poten-
tial of the EO to scavenge free radicals present in organic solution. Si-
milar results have been reported by Gourine et al. (2010a) and Gourine
et al. (2010b). Gourine et al. (2010a) studied the antioxidant properties
of male and female EO of P. atlantica Desf. during June, July, August,
September and October and observed that their IC50 values were in the
range of 8.5–27.9 mg/mL. In general, the male compared EO had
stronger antioxidant activity. The IC50 values of BHT, BHA and AA were
6.29, 7.12 and 4.48 μg/mL, respectively. In another study, Gourine
et al. (2010b) measured the antioxidant properties of the EO extracted
from P. atlantica's leaves from 4 different geographical regions in Al-
geria (Laghouat, South of Laghouat, Hassi R'mel and Aïn-Oussera) and
reported the IC50 values in the range of 8.8–27.5 mg/mL. The IC50
values of BHT, BHA and AA were 0.01, 0.01 and 0.004 mg/mL, re-
spectively. Rezaie et al. (2015a) also referred to a mild antioxidant
activity of mutica subspecies fruit hulls' EO compared to BHT. EC50
5
Food Bioscience 34 (2020) 100510
DPPH IC50 (mg/mL) FRAP assay (mg/g)
a
25.2 ± 0.03 6.2 ± 0.1a
0.01 ± 0.00001b 0.58 ± 0.01b
values of the EO and BHT were 23.0 and 8.3 μg/mL, respectively. Aissi
et al. (2016) also investigated the antioxidant activity of the EO ex-
tracted from 14 Tunisian P. lentiscus populations using the DPPH
method and reported their antioxidant activities in the range of
299–993 μg/g. The IC50 value of BHT was 29.4 μg/mL. Labed-Zouad
et al. (2017) studied the antioxidant activity of the EO obtained from P.
atlantica's leaves and fruits using the DPPH method and reported the
IC50 values of 23.9, 28.5 μg/mL, respectively. The IC50 value of BHA
was 7.3 μg/mL.
The antioxidant activity of the PAKH's EO using the FRAP assay was
6.24 mg/g, which was significantly (P < 0.05) higher than the BHT
(0.58 mg/g) (Table 2), indicating a strong antioxidant capacity of the
EO. Similar results have been reported by Aissi et al. (2016), Gourine
et al. (2010a), Gourine et al. (2010b) and Rezaie et al. (2015a). Gourine
et al. (2010a) reported the antioxidant activity of the EO obtained from
P. atlantica Desf.‘s leaves during June, July, August, September and
October using the FRAP method were in the range of 4.95–11.8 mg/mL,
which were higher than BHA (0.42 mg/mL) and BHT (0.37 mg/mL).
Gourine et al. (2010b) reported the antioxidant activities of the EO
extracted from P. atlantica from 4 different geographical regions in
Algeria (Laghouat, South of Laghouat, Hassi R'mel and Aïn-Oussera)
using the FRAP method in the range of 2.8–11.1 mg/mL, which were
higher than BHA (0.42 mg/mL) and BHT (0.37 mg/mL). Rezaie et al.
(2015a) showed a higher antioxidant potency of mutica subsp. EO using
the FRAP assay (5.29 mmol/g) than BHT (0.45 mmol/g), AA
(1.34 mmol/g) and alpha-tocopherol (2.51 mmol/g). Aissi et al. (2016)
measured the antioxidant activity of the EO obtained from 14 Tunisian
P. lentiscus populations using the FARP method and reported their an-
tioxidant activities in the range of 6.2–13.8 mmol/g.
Various studies suggested that the ability of EO to inhibit the free
radicals is related to the overall contribution of their active ingredient
components such as phenolic acid and flavonoids (Chryssavgi et al.,
2008). Phenolic compounds have high antioxidant potency and are
effective in eliminating and preventing the formation of free radicals;
such that an important role of phenolic compounds as free radical in-
hibitors in several investigations has been emphasized (Chryssavgi
et al., 2008; Rezaie et al., 2015a). For example, Rezaie et al. (2015a)
attributed the antioxidant activity of the EO to their monoterpenes and
sesquiterpenes compounds and Aissi et al. (2016) ascribed the anti-
oxidant activity to oxygenated monoterpenes and oxygenated sesqui-
terpenes. In another study, the antioxidant activity of P. atlantica was
attributed to the synergistic effects of monoterpenes and sesquiterpenes
such as limonene, α-pinene, β-elemene, γ-gurjunene, germacrene-B and
spathulenol (Labed-Zouad et al., 2017). The antioxidant properties of
phenols are mostly due to their oxidation and redox properties, which
allows them to function as a reducing agent and a hydrogen donor.
Moreover, high molecular weight phenolic compounds such as sesqui-
terpene hydrocarbon and oxygenated sesquiterpenes (Table 1) have
more potential to inhibit free radicals, and this ability is more depen-
dent on the number of aromatic rings and the nature of the hydroxyl
groups. The difference between the results obtained from the phenolic
content of different varieties of EO obtained from different parts of the
various species of Pistacia can be attributed to genetic and environ-
mental factors in various investigations (Wong et al., 2006).
3.5. Evaluation of antimicrobial properties
The results of antimicrobial tests using two techniques of broth
S.-M. Hasheminya and J. Dehghannya Food Bioscience 34 (2020) 100510

Table 3
Minimum inhibitory concentration (MIC) and minimum microbicidal concentration (MMC) of Pistacia atlantica subsp. kurdica essential oil and positive controls
(streptomycin and ketoconazole antibiotics) for different bacteria strains and the fungus based on broth microdilution method.
Microbial strain Essential oil (mg/mL) Antibiotics (mg/mL)

Streptomycin Ketoconazole

MIC MMC MIC MMC MIC MMC

a a b a
Gram-negative Escherichia coli 0.42 ± 0.14 0.52 ± 0.14 0.07 ± 0.03 0.10 ± 0.02 NT NT
Pseudomonas aeruginosa 0.31 ± 0.00b 0.31 ± 0.00c 0.08 ± 0.02a 0.12 ± 0.00b NT NT
Salmonella typhimurium 0.26 ± 0.07c 0.42 ± 0.14b 0.07 ± 0.03b 0.10 ± 0.02a NT NT
Gram-positive Streptococcus faecalis 0.21 ± 0.07d 0.21 ± 0.07e 0.05 ± 0.01c 0.08 ± 0.02b NT NT
Bacillus cereus 0.21 ± 0.07d 0.26 ± 0.07dd 0.05 ± 0.15c 0.10 ± 0.02a NT NT
Staphylococcus aureus 0.16 ± 0.00e 0.21 ± 0.07e 0.08 ± 0.02a 0.17 ± 0.05c NT NT
Fungus Candida albicans 0.13 ± 0.03f 0.16 ± 0.00f NT NT 0.03 ± 0.02 0.04 ± 0.01

NT. Not tested.

Table 4
Growth inhibition zones (mm) obtained for different bacteria strains and fungus based on disc diffusion method in the presence of Pistacia atlantica subsp. kurdica
essential oil and positive controls (Streptomycin and ketoconazole antibiotics).
Microbial strain Zone of growth inhibition (mm)

Essential oil Streptomycin (10 μg/disc) Ketoconazole (25 μg/disc)

d c
Gram-negative Escherichia coli 20.8 ± 0.1 19.8 ± 0.03 NT
Pseudomonas aeruginosa 21.8 ± 0.04bc 20.5 ± 0.1b NT
Salmonella typhimurium 21.5 ± 0.1c 18.3 ± 0.1d NT
Gram-positive Streptococcus faecalis 22.3 ± 0.1c 20.6 ± 0.1b NT
Bacillus cereus 22.5 ± 0.02b 21.1 ± 0.2a NT
Staphylococcus aureus 23.8 ± 0.2b 21.2 ± 0.1a NT
Fungus Candida albicans 24.2 ± 0.1a NT 21.6 ± 0.02

Diameter of the disks for positive controls and samples were 6 mm.
NT: Not tested.

microdilution and disc diffusion are shown in Tables 3 and 4, respec-
tively. PAKH’ EO in both methods were effective on all tested microbial
strains. The MIC and MMC of the EO in all microbial strains were less
than the positive control (Table 3). The results of disc diffusion showed
that the diameter of the inhibition zone of microbial strains were, in
general, higher than the positive control (Table 4). The highest dia-
meter of the inhibition zone of 24.2 mm was with C. albicans and the
lowest diameter of the inhibition zone of 20.8 mm was with E. coli. In
general, the results showed that the diameter of the inhibition zone of
all microbial strains was higher than the positive control.
Rezaie et al. (2015a) reported a MIC of P. atlantica subsp. mutica's
EO against E. coli and S. aureus, respectively, as 6 and 12.5 μg/mL.
Taghizadeh et al. (2018a) measured the MIC and MMC of P. khinjuk EO
for the microbial strains of P. aeruginosa, B. cereus, Micrococcus luteus, S.
aureus and S. Typhimurium in the range of 16–150 and 16–150 μg/mL,
respectively.
Antibacterial activity of EO is associated with the presence of active
components, including isoprenes such as monoterpenes, sesquiterpenes
and their alcohols. Some researchers have reported the relationship
between the chemical structures of some of the dominant components
in the EO with their antibacterial activity (Burt, 2004). The main
components of the EO in this study using GC-MS were α-pinene and β-
citral (Table 1). The hydrophobic nature of the hydrocarbon skeleton
and the hydrophobicity of their functional groups are the main reasons
for the antibacterial activity of the EO (Taghizadeh et al., 2018a).
According to different investigations, the sensitivity of Gram-posi-
tive bacteria to EO is higher than Gram-negative ones. The difference in
antimicrobial actions of EO against Gram-positive and Gram-negative
bacteria is based on their different cellular structure (Hasheminya,
Mokarram, Ghanbarzadeh, Hamishekar, & Kafil, 2018). Due to the
presence of outer membranes surrounding the cell wall in Gram-nega-
tive bacteria, it seems that these bacteria are less susceptible to the
antibacterial effect of the EO. One of the important properties of EO and
their constituent elements is their hydrophobic property, which enables
them to partition into the lipids of bacterial cell membranes and mi-
tochondria, and disrupt their structures and increases their perme-
ability. This leads to the leakage of ions and other cellular contents.
Although the release of limited amounts of these materials is tolerable
to the bacteria, the extensive loss of cellular contents or the release of
important ions and molecules can lead to cell death (Burt, 2004).
4. Conclusions
The main components of the EO obtained from the kurdica sub-
species of P. atlantica (Bene) fruit's hull were α-pinene, β-citral, carvone
hydrate, myristic acid, pinocarveol, p-acetyltoluene and palustrol. The
EO of Bene fruit's hull had more inhibitory effects on the growth of
Gram-positive bacteria than Gram-negative ones. The fungal sample (C.
albicans) had less resistance compared to bacteria strains. In sum, to
further assess the antioxidant activity of the EO obtained from PAKH, it
can be tested with different foods, for example, edible oil production, to
study its potential for use as a natural preservative. To better evaluate
the antimicrobial properties of the EO, an in vivo study is needed.
Finally, toxicological and regulatory investigations are also necessary
before using these natural products as a biologic agent.
CRediT authorship contribution statement
Seyedeh-Maryam Hasheminya: Methodology, Software, Formal
analysis, Investigation, Resources, Data curation, Writing - original
draft, Visualization. Jalal Dehghannya: Conceptualization, Validation,
Writing - review & editing, Supervision, Project administration,
Funding acquisition.

6
S.-M. Hasheminya and J. Dehghannya Food Bioscience 34 (2020) 100510

Declaration of competing interest Dehghannya, J. (2019a). Development and characterization of biocomposite films
made from kefiran, carboxymethyl cellulose and Satureja khuzestanica essential oil.
Food Chemistry, 289, 443–452.
The authors confirm that they have no conflicts of interest with Hasheminya, S.-M., Mokarram, R. R., Ghanbarzadeh, B., Hamishekar, H., Samadi Kafil,
respect to the study described in this manuscript. H., & Dehghannya, J. (2019b). Influence of simultaneous application of copper oxide
nanoparticles and Satureja Khuzestanica essential oil on properties of kefir-
an–carboxymethyl cellulose films. Polymer Testing, 73, 377–388.
Acknowledgement Hatamnia, A. A., 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.
This research was supported by a research grant from the University Hatamnia, A. A., Rostamzad, A., Hosseini, M., Abbaspour, N., Darvishzadeh, R.,
of Tabriz (Number: 2706). Malekzadeh, P., et al. (2016). Antioxidant capacity and phenolic composition of
leaves from 10 Bene (Pistacia atlantica subsp. kurdica) genotypes. Natural Product
Research, 30(5), 600–604.
Appendix A. Supplementary data Hesami, G., Bahramian, S., Fatemi, A., & Hesami, S. (2014). Effect of Pistacia atlantica
subsp. kurdica essential oil and acetic acid on Botrytis cinerea growth in culture media
and strawberry fruits. Bulletin of Environment, Pharmacology and Life Sciences, 3(2),
Supplementary data to this article can be found online at https:// 100–106.
doi.org/10.1016/j.fbio.2019.100510. Houicher, A., Hamdi, M., Hechachna, H., & Özogul, F. (2018). Chemical composition and
antifungal activity of Anacyclus valentinus essential oil from Algeria. Food Bioscience,
25, 28–31.
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