You are on page 1of 5

Industrial Crops & Products 128 (2019) 162–166

Contents lists available at ScienceDirect

Industrial Crops & Products


journal homepage: www.elsevier.com/locate/indcrop

Calamintha incana: Essential oil composition and biological activity T


a,⁎ b,⁎ c d
Jelena Popović-Djordjević , Mustafa Cengiz , Mehmet Sabih Ozer , Cengiz Sarikurkcu
a
University of Belgrade, Faculty of Agriculture, Belgrade, Serbia
b
Süleyman Demirel University, Faculty of Science and Literature, Department of Chemistry, Isparta, Turkey
c
Manisa Celal Bayar University, Faculty of Science and Literature, Department of Chemistry, Manisa, Turkey
d
Süleyman Demirel University, Faculty of Pharmacy, Department of Analytical Chemistry, Isparta, Turkey

ARTICLE INFO ABSTRACT

Keywords: The chemical composition of the essential oils (EO) isolated aerial parts of Calamintha incana (Sm.) Boiss. from
Calamintha incana Turkey was characterized by GC-FID and GC–MS analysis. The oxygenated monoterpenes trans-piperitone oxide
Essential oil (41.37%), piperitenone oxide (34.47%), piperitenone (6.67%), and monoterpene phenol thymol (3.37%) were
trans-Piperitone oxide found to be the major constituents of the essential oils of C. incana. The results of the antioxidant activity in
Antioxidant activity
phosphomolybdenum, radical scavenging (DPPH and ABTS) and reducing power activity (CUPRAC and FRAP) as
GC/MS analysis
well as metal chelating effects (ferrous ion chelating) showed that EO was the most potent in ABTS
(129.58 ± 2.21 mg TEs/g oil) and CUPRAC and FRAP (51.14 ± 0.05 and 53.63 ± 0.10 mg TEs/g, respec-
tively) assays. In enzymes inhibitory activity assays of EO, the best result was achieved for tyrosinase
(2.10 ± 0.30 mg KAEs/g oil). The results suggest that EO might be considered as a potential source of bioactive
agents to be used in food and pharmacological industries.

1. Introduction Lamiaceae, is perennial aromatic plants distributed in Central Asia,


Europe, North Africa and Americas (Bonnier, 1959; Bown, 1995). In the
From the ancient days, medicinal plants have been a valuable source Flora of Turkey, the genus Calamintha is represented by nine species,
of various therapeutics, and still represent an essential fund of new five being endemic to Turkey, and 12 taxa (Davis et al., 1982; Güner
plant-derived natural products or their derivatives with significant et al., 2000). Calamintha species, known as “Miskotu, Dağ Nanesi, Ya-
biological activities (Abu Khalaf, 2016; Atanasov et al., 2015). Enzyme bani Oğulotu etc”, are used for strengthening central nervous system
inhibitory activity of plant extracts and essential oils (EO) has been a and as diaphoretic, emmenagogue, stimulant, expectorant, anti-
subject of many researches. Various classes of available drugs have spasmodic, antiseptic, and digestive (Alan et al., 2009; Alan and Ocak,
certain limitations, which impose the need for the development of a 2009; Baytop, 1999; Bown, 1995; Viney, 1994). In addition, some
new one. Besides the existing compounds, scaffolds and templates of species are reported to display strong antimicrobial activities (Mimica-
naturally occurring compounds have always presented key structures in Dukić et al., 2004). The noticeable mint-like smell of Calamintha plants
the process of new drug discovery (Popovic-Djordjevic et al., 2018). contributed to their use in the traditional medicine of several Medi-
Essential oils are progressively studied for the industrial use pur- terranean countries as a mint alternative (Karousou et al., 2012). In the
poses (chemical, cosmetic, food, fragrance and pharmaceutical) owing Calamintha genus great variations in oil composition occur, both intra
to their potential bioactivities; antioxidant, repellent, antibacterial, and inter species. The most commonly represented components in the
antifungal, analgesic, anti-inflammatory, antihypertensive and AChE oils of various Calamintha species are C(3)-oxygenated p-menthane
inhibitory (Abdelli et al., 2016; Ayvaz et al., 2010; Balkan et al., 2018; compounds (piperitone, piperitone oxide, piperitenone, piperitenone
Bouchra et al., 2003; Bozovic and Ragno, 2017; Marin et al., 2018; oxide, pulegone, menthone and isomenthone) (Demirci et al., 2011;
Sarikurkcu et al., 2018).The origin of the species may have impact on Hanlidou et al., 1991; Karousou et al., 2012; Kitic et al., 2002;
the chemical variability of the EOs (Marongiu et al., 2010). On the Marongiu et al., 2010; Mimica-Dukić et al., 2004; Tümen et al., 1995).
other hand, biological activities of EO depend on the chemical com- Due to the potential market value and chemical diversity of
position, and are influenced by factors such as plant genotype and en- Calamintha plants many researches have been done in recent years.
vironmental conditions (Marin et al., 2018). Composition and biological activity of the essential oil of Calamintha
The genus Calamintha Miller species, which belong to the family incana (Sm.) Boiss. from the area of Kestel, Bursa-Turkey were


Corresponding authors.
E-mail addresses: jelenadj@agrif.bg.ac.rs (J. Popović-Djordjević), cengizmustafa32@gmail.com (M.S. Ozer).

https://doi.org/10.1016/j.indcrop.2018.11.003
Received 30 August 2018; Received in revised form 30 October 2018; Accepted 1 November 2018
Available online 13 November 2018
0926-6690/ © 2018 Elsevier B.V. All rights reserved.
J. Popović-Djordjević et al. Industrial Crops & Products 128 (2019) 162–166

examined in this study. Phosphomolybdenum, ferrous ion chelating, Table 1


reducing power, and free radical scavenging assays were employed for Chemical composition of the essential oil from C. incana.
antioxidant activity. Essential oil of C. incana was tested for inhibition No RRIExpx RRILity RRILitz Compounds (%)w Identificationt
activity against acetylcholinesterase, butyrylcholinesterase, tyrosinase,
α-glucosidase, and α-amylase enzymes. To the best of our knowledge, 1 1201 1203a 1030 Limonene 0.14 1,2,3
2 1276 1280a 1024 p-Cymene 0.18 1,2,3
no data about antioxidant and enzyme inhibition activities of C. incana
3 1391 1393a 992 3-Octanol 0.37 1,2
essential oil have been reported up to date. 4 1501 1497b 1377 α-Copaene 0.11 1,2
5 1531 1535b 1385 β-Bourbonene 0.17 1,2
2. Materials and methods 6 1548 1553a 1097 Linalool 0.53 1,2,3
7 1612 1611a 1174 Terpinen-4-ol 1.46 1,2
8 1715 1719a 1167 Borneol 0.18 1,2,3
2.1. Plant material
9 1733 1733a 1262 cis-Piperitone oxide 0.71 1,2
10 1757 1754a – trans-Piperitone oxide 41.37 1,2
The aerial parts of Calamintha incana (Sm.) Boiss. were randomly 11 1830 – 1303 2-Hydroxypiperitone 0.95 1,2
collected under the forest area from Kestel, Bursa-Turkey on 29 March, 12 1948 1949a 1329 Piperitenone 6.67 1,2
13 1990 1983a 1363 Piperitenone oxide 34.47 1,2
2010 (40° 09' 14.3"N 29° 12' 01.6"E, 540–580 m). The plant was de-
14 2017 2008b 1579 Caryophyllene oxide 1.76 1,2,3
posited and identified by Prof. Dr. Hasan Ozcelik from the Department 15 2196 2198b 1293 Thymol 3.73 1,2,3
of Biology, Süleyman Demirel University, Isparta-Turkey. Total 92.80
Yield (ml/100 g dry 1.30
2.2. Isolation and analysis of the essential oil weight)

x
RRIExp; Relative retention indices calculated against n-alkanes on HP-in-
A British-type Clevenger apparatus (Ildam Ltd., Ankara-Turkey) was
nowax column.
used to obtain essential oil (EO) from the aerial parts of C. incana by y
RRILit; Relative retention indices on given in the literature for the com-
hydro-distillation. The EO was dried over sodium sulphate, filtrated, pound in similar columns (HP-innowax) and analysis conditions from the lit-
and then stored + 4 °C until tested and analyzed. Chemical character- erature [aSource: Demirci et al. (2011); bSource: Formisano et al. (2014)].
ization of the EO was carried out by GC-FID and GC–MS by using the z
RRILit; Relative retention indices on an HP-5MS column from the literature
analytical conditions reported previously (Sarikurkcu et al., 2015). (Adams, 2007).
w
Please see the supplementary file for the details. % calculated from FID data.
t
1: Relative retention index, 2:mass spectrum, 3:co-injection with authentic
2.3. Biological activity compound.

The biological activities of the EO were determined using anti-


oxidant and enzyme inhibition assays. Phosphomolybdenum (Zengin piperitenone oxide (34.47%) and piperitenone (6.67%) as the main
et al., 2015a), ferrous ion chelating (Tepe et al., 2011), reducing power constituents, and monoterpene phenol thymol (3.37%). Other detected
[cupric ion reducing (CUPRAC) and ferric reducing antioxidant power compounds were present in concentrations less than 2% (Table 1).
(FRAP)] (Apak et al., 2006; Kocak et al., 2016), and free radical Available data about the composition of the oil of C. incana are very
scavenging [on 1,1-diphenyl-2-picrylhydrazyl (DPPH·) radical and 2,2- limited. Tümen et al. (1995) reported that piperitenone oxide, limonene
azino-bis (3-ethylbenzothiazloine-6-sulphonic acid) radical cation and piperitone oxide (as a mixture of isomers) were the predominant
(ABTS·+)] (Zengin et al., 2015b) tests were used for antioxidant ac- components of the EO of this species, with 66.60, 6.22 and 5.91%,
tivity. Inhibition effects of the EO against acetylcholinesterase (AChE), respectively.
butyrylcholinesterase (BChE), tyrosinase, α-glucosidase, and α-amylase It could be noticed that trans-piperitone oxide was found only in C.
were also investigated for enzyme inhibition assays (Zengin et al., nepeta subsp. glandulosa (Demirci et al., 2011), whereas its stereoisomer
2015a). Please see the supplementary file for the details. cis-piperitone oxide was reported in various Calamintha species such as
The activity is expressed as both IC50 value (the sample con- in C. sylvatica subsp. sylvatica (Kitic et al., 2001), C. sylvatica (Mimica-
centration providing 50% of radical scavenging/ferrous ion chelating/ Dukić et al., 2004), and C. vardarensis (Kitic et al., 2002). Hanlidou
enzyme inhibition or 0.500 absorbance for the reducing power/phos- et al. (1991) reported that piperitone oxide was found in high con-
phomolybdenum assays, respectively) and standard equivalents (μg/g centrations (62.9 and 67.6%) in EO of two C. menthifolia populations.
extract). Trolox and EDTA were used as positive controls for anti- Piperitone is a natural monoterpene ketone with fresh peppermint
oxidant assays, and galanthamine, kojic acid, and acarbose were used odor, which occurs in essential oils from various leaves. Mentha and
for enzymatic assays. Eucalyptus genera comprise a large number of species rich in piperitone
(Ravid et al., 1994).
2.4. Statistical analysis Piperitenone oxide isolated from essential oil of a new genotype,
Mentha spicata var. viridis, has proved to be very efficient for larvicidal,
All of the experiments of biological activity were repeated in tri- ovicidal, oviposition-deterrent, developmental toxicity, and repellent
plicate and the results were given as the mean value and the standard properties against Anopheles stephensi a well-known malarial disease
deviation (mean ± SD). The results with IC50 values were analyzed agent (Tripathi et al., 2004). Antibacterial activity of this compound
statistically with Student’s t-test (α = 0.01) by using the SPSS v22.0 against various pathogens is also reported (Bozovic et al., 2015).
software Thymol has been identified as a molecule with antioxidative prop-
erties (Deighton et al., 1993). Natural products which are a source of
3. Results and discussion antioxidant molecules such as thymol, may be of particular interest in
food production and storage processes which require the use of effec-
3.1. Chemical composition of the EO tive antioxidants.

In the C. incana EO from the forest area of Kestel (Bursa) only fifteen 3.2. Antioxidant activity
compounds were detected, which accounted for 92.80% of the total
composition. The EO was characterized by a high percentage of the The application of different antioxidant assays is necessary as it is
oxygenated monoterpenes, namely trans-piperitone oxide (41.37%), difficult to assess the antioxidant activity of a product based on a single

163
J. Popović-Djordjević et al. Industrial Crops & Products 128 (2019) 162–166

Table 2 Table 4
Antioxidant activities of the essential oil from C. incana by different assays.x Inhibitory effect of the essential oil from C. incana by different assays.x
Assays Antioxidant activity Assays Inhibitory activity

Phosphomolybdenum (mmol TEs/g oil) 5.52 ± 0.26 AChE (mg GALAEs/g oil) na
Ferrous ion chelating (mg EDTAEs/g oil) 1.94 ± 0.14 BChE (mg GALAEs/g oil) na
DPPH radical scavenging (mg TEs/g oil) 19.28 ± 0.74 Tyrosinase (mg KAEs/g oil) 2.10 ± 0.30
ABTS radical cation scavenging (mg TEs/g oil) 129.58 ± 2.21 α-Amylase (mmol ACEs/g oil) 0.34 ± 0.10
CUPRAC reducing power (mg TEs/g oil) 51.14 ± 0.05 α-Glucosidase (mmol ACEs/g oil) 0.10 ± 0.01
FRAP reducing power (mg TEs/g oil) 53.63 ± 0.10
x
GALAEs, KAEs, and ACEs; galanthamine, kojic acid, and acarbose
x
TEs and EDTAEs; trolox and ethylenediaminetetraacetic acid (disodium equivalents, respectively. na, not active.
salt) equivalents, respectively.

method. In order to obtain a more comprehensive picture about anti- 3.3. Enzyme inhibitory activity
oxidant potential of C. incana EO, several methods were employed and
the results are given in Table 2. The radical scavenging ability of ex- In this work we examined inhibitory potential of C. incana against
amined EO was six-fold higher in ABTS assay (129.58 ± 0.74) than in acetylcholinesterase (AChE), butyrylcholinesterase (BuChE, tyrosinase,
DPPH radical (19.28 ± 0.74) assay, expressed as trolox equivalents per α-amylase and α-glucosidase enzymes using in vitro models (Table 4).
gram of oil. The result obtained for C. incana EO in DPPH assay were Essential oil of C. incana did not exert inhibitory activity against acetyl-
comparable to the activity of Chenopodium bortys EO (12.37–20.72 mg cholinesterase (AChE) and butyrylcholinesterase (BChE), enzymes as-
TEs/g oil) (Ozer et al., 2017). On the other hand, its activity (ABTS sociated with Alzheimer’s (the most common form of dementia) and
assay) was substantially higher than C. bortys EOs (4.95–9.89 mg TEs/g Parkinson’s disease (Sarikurkcu et al., 2014).
oil) (Ozer et al., 2017) and Origanum vulgare subsp. hirtum EO (9.63 mg The highest inhibitory activity was observed against tyrosinase
TEs/g oil) (Sarikurkcu et al., 2015). 2.10 ± 0.30 (expressed as mg of kojic acid equivalents per gram of
Reducing power assays FRAP and CUPRAC may provide important EO). This result indicated its higher activity than reported for C. bortys
information about EO antioxidant power. The antioxidant activity of C. EO (Ozer et al., 2017). Tyrosinase (polyphenol oxidase) is a multi-
incana EO was 51.14 and 53.63 mg TEs/g oil in FRAP and CUPRAC, functional copper-containing oxidase which catalyzes the formation of
respectively (Table 2), which is higher reducing power when compared melanin from tyrosine. Besides, this enzyme is associated with neuro-
to C. bortys EO (9.89–18.45 mg TEs/g oil for FRAP and 33.91–41.91 mg degenerative process in Parkinson's disease, melanogenesis in mammals
TEs/g oil for CUPRAC) (Ozer et al., 2017). and enzymatic browning in plants. Hence, tyrosinase inhibitors have
In the phosphomolybdenum assay, the EO showed weak antioxidant become increasingly important in the field of medicine, agriculture, and
capacity (5.52 ± 0.26 mmol TEs/g oil) but comparable to the activity cosmetics (Maghsoudi et al., 2013; Sawant et al., 2013).
of C. bortys EO (6.52–7.49 mg TEs/g oil) (Ozer et al., 2017). The inhibition of α-glucosidase and α-amylase which are enzymes
The chelating effect of the EO was evaluated by ferrous ion che- involved in the hydrolyse of polysaccharides, is an important step in
lating test and found as 1.94 ± 0.14 mg EDTAEs per gram of oil, in- controlling blood glucose level, and plants are known for their anti-
dicating poor metal chelating activity, but still higher than those of diabetic properties (Arumugam et al., 2013). Inhibitory activity of C.
Origanum vulgare subsp. vulgare EO (1.34 ± 0.21 mg EDTAEs/g oil) incana EO against α-amylase and α-glucosidase was moderate; 0.34 and
(Sarikurkcu et al., 2015). 0.10 mmol of acarbose equivalents per gram of EO, respectively. When
Antioxidant activities of EO were also presented as IC50 values, the results for α-amylase inhibition were compared, C. incana EO was a
which correspond to the concentration of the oil (mg/ml) required to more potent inhibitor then both Origanum vulgare subspecies (subsp.
inhibit 50% of the initial concentration of oxidant (Table 3). IC50 values vulgare and subsp. hirtum) EO (Sarikurkcu et al., 2015).
of essential oil were significantly lower activity than those of trolox and Results obtained from enzyme inhibitory activity assays with the
EDTA which are used as positive control, except for phosphomo- IC50 values in mg/ml are also summarized in Table 5. The EO showed
lybdenum test (p < 0.01). significant activity against α-amylase, with IC50 values very similar to
A number of reports are available in the literature showing that standard drug acarbose, while exhibiting very low inhibition against
oxygenated monoterpenes such as piperitenone, piperitenone oxide, tyrosinase and α-glucosidase (p < 0.01). The inhibitory activity of C.
linalool, thymol, and carvacrol are responsible for the antioxidant po- incana EO against α-amylase indicates its potential therapeutic use re-
tential of plant oils (Barbieri et al., 2016; Bicas et al., 2011; Bozovic levant for the treatment of diabetes mellitus type 2.
et al., 2015; Miguel, 2010). C. incana EO is mainly constituted by trans-
piperitone oxide and piperitenone oxide. These findings support the 4. Conclusions
view that certain aromatic plants are potential sources of antioxidants.
In this sense, C. incana EO can be a good natural antioxidant source for In summary, trans-piperitone oxide, piperitenone oxide, piper-
use as a nutraceutical, protective or cosmeceutical. itenone and thymol represented 85.88% of all C. incana EO

Table 3
Antioxidant activities of standards and the essential oil from C. incana by different assays.x
Samples Phosphomolybdenum DPPH radical ABTS radical CUPRAC reducing FRAP reducing Metal chelating

a b b b b
Essential oil (IC50: mg/ml) 0.169 ± 0.011 3.67 ± 0.02 1.45 ± 0.03 1.13 ± 0.001 1.49 ± 0.003 5.40 ± 0.39b
Trolox (IC50: mg/ml) 0.233 ± 0.005a 0.068 ± 0.004a 0.19 ± 0.01a 0.058 ± 0.001a 0.08 ± 0.003a –
EDTA (IC50: mg/ml) – – – – – 0.026 ± 0.001a

x
Different superscripts in the same column indicate significant differences (p < 0.01). EDTA, ethylenediaminetetraacetic acid (disodium salt).

164
J. Popović-Djordjević et al. Industrial Crops & Products 128 (2019) 162–166

Table 5
Inhibitory activities of standards and the essential oil from C. incana by different assays.x
Samples Tyrosinase α-Amylase α-Glucosidase Acetylcholinesterase Butyrylcholinesterase

b b b
Essential oil (IC50: mg/ml) 61.57 ± 8.70 4.85 ± 0.13 175.35 ± 37.20 na na
Kojic acid (IC50: mg/ml) 0.128 ± 0.001a – – – –
Acarbose (IC50: mg/ml) – 1.37 ± 0.01a 2.16 ± 0.05a – –
Galanthamine (IC50: mg/ml) – – – 0.0015 ± 0.0001 0.0018 ± 0.0002

x
Different superscripts in the same column indicate significant differences (p < 0.01). na, not active.

constituents. A good radical scavenging and reducing power ability as Bown, D., 1995. The Herb Society of America Encyclopedia of Herbs & Their Uses.
well as significant activity against α-amylase of C. incana EO were Dorling Kindersley, New York, NY.
Bozovic, M., Ragno, R., 2017. Calamintha nepeta (L.) Savi and its main essential oil
observed in the study, indicating its potential for use as functional food constituent pulegone: biological activities and chemistry. Molecules 22, 290.
sources or therapeutic. The present findings improved the knowledge of Bozovic, M., Pirolli, A., Ragno, R., 2015. Mentha suaveolens Ehrh. (Lamiaceae) essential oil
the composition and biological activity of C. incana EO which has been and its main constituent piperitenone oxide: biological activities and chemistry.
Molecules 20, 8605–8633.
insufficiently investigated up to now (or reported herein for the first Davis, P.H., Leblebici, E., Miller, L., 1982. Flora of Turkey and East Aegean Islands.
time). However, further studies are needed for obtaining a deeper in- University Press, Edinburgh.
sight into contribution of particular constituents to bioactivity of the Deighton, N., Glidewell, S.M., Deans, S.G., Goodman, B.A., 1993. Identification by EPR
spectroscopy of carvacrol and thymol as the major sources of free radicals in the
essential oil.
oxidation of plant essential oils. J. Sci. Food Agric. 63, 221–225.
Demirci, B., Temel, H.E., Portakal, T., Kırmızıbekmez, H., Demirci, F., Başer, K.H.C.,
Acknowledgement 2011. Inhibitory effect of Calamintha nepeta subsp. glandulosa essential oil on lipox-
ygenase. Turk. J. Biochem. 36, 290–295.
Formisano, C., Oliviero, F., Rigano, D., Saab, A.M., Senatore, F., 2014. Chemical com-
This work was partly performed within the project No. 172032 position of essential oils and in vitro antioxidant properties of extracts and essential
supported by the Ministry of Education, Science and Technological oils of Calamintha origanifolia and Micromeria myrtifolia, two Lamiaceae from the
Development of the Republic of Serbia. Lebanon flora. Ind. Crops Prod. 62, 405–411.
Güner, A., Özhatay, N., Ekim, T., Baser, K.H.C., 2000. Flora of Turkey and East Aegean
Islands. University Press, Edinburgh, UK.
Appendix A. Supplementary data Hanlidou, E., Kokkini, S., Bosabalidis, A.M., Bessière, J.-M., 1991. Glandular trichomes
and essential oil constituents of Calamintha menthifolia (Lamiaceae). Plant Syst. Evol.
177, 17–26.
Supplementary material related to this article can be found, in the Karousou, R., Hanlidou, E., Lazari, D., 2012. Essential-oil diversity of three Calamintha
online version, at doi:https://doi.org/10.1016/j.indcrop.2018.11.003. species from Greece. Chem. Biodivers. 9, 1364–1372.
Kitic, D., Palic, R., Ristic, M., Sojanovic, G., Jovanovic, T., 2001. The volatile constituents
of Calamintha sylvatica Bromf. subsp. sylvatica. Flavour Fragr. J. 16, 257–258.
References Kitic, D., Palic, R., Stojanovic, G., Ristic, M., 2002. Composition of the essential oil of
Calamintha vardarensis (Greuter et Burdet) Silic. J. Essent. Oil Res. 14, 58–59.
Abdelli, M., Moghrani, H., Aboun, A., Maachi, R., 2016. Algerian Mentha pulegium L. Kocak, M.S., Sarikurkcu, C., Cengiz, M., Kocak, S., Uren, M.C., Tepe, B., 2016. Salvia
leaves essential oil: chemical composition, antimicrobial, insecticidal and antioxidant cadmica: phenolic composition and biological activity. Ind. Crops Prod. 85, 204–212.
activities. Ind. Crops Prod. 94, 197–205. Maghsoudi, S., Adibi, H., Hamzeh, M., Ashrafi-Kooshk, M.R., Rezaei-Tavirani, M.,
Abu Khalaf, R., 2016. Exploring natural products as a source for antidiabetic lead com- Khodarahmi, R., 2013. Kinetic of mushroom tyrosinase inhibition by benzaldehyde
pounds and possible lead optimization. Curr. Top. Med. Chem. 16, 2549–2561. derivatives. J. Rep. Pharm. Sci. 2, 156–164.
Adams, R.P., 2007. Identification of Essential Oil Components by Gas Chromatography/ Marin, M., Novakovic, M., Vuckovic, I., Tesevic, V., Kolarevic, S., Vukovic-Gacic, B.,
Mass Spectrometry, fourth ed. Allured Publishing Corporation, Carol Stream, Illinois, 2018. Wild Thymus capitatus Hoff. Et Link. chemical composition, antioxidant and
USA. antimicrobial activities of the essential oil. J. Essent. Oil Bear. Pl. 21, 388–399.
Alan, S., Ocak, A., 2009. Taxonomical and morphological studies on the genus Calamintha Marongiu, B., Piras, A., Porcedda, S., Falconieri, D., Maxia, A., Goncalves, M.J., Cavaleiro,
Miller (Lamiaceae) in Turkey. Biol. Divers. Conserv. 2, 125–143. C., Salgueiro, L., 2010. Chemical composition and biological assays of essential oils of
Alan, S., Kürkçüoğlu, M., Ozek, T., Başer, K.H.C., 2009. Composition of the essential oils Calamintha nepeta (L.) Savi subsp. nepeta (Lamiaceae). Nat. Prod. Res. 24, 1734–1742.
of Calamintha tauricola P.H. Davis. J. Essent. Oil Res. 21, 143–145. Miguel, M.G., 2010. Antioxidant and anti-inflammatory activities of essential oils: a short
Apak, R., Güçlü, K., Özyürek, M., Esin Karademir, S., Erçaǧ, E., 2006. The cupric ion review. Molecules 15, 9252.
reducing antioxidant capacity and polyphenolic content of some herbal teas. Int. J. Mimica-Dukić, N., Couladis, M., Tzakou, O., Jančić, R., Slavkovska, V., 2004. Essential oil
Food Sci. Nutr. 57, 292–304. of Calamintha sylvatica Bromf. and Calamintha vardarensisilic. J. Essent. Oil Res. 16,
Arumugam, G., Manjula, P., Paari, N., 2013. A review: anti diabetic medicinal plants used 219–222.
for diabetes mellitus. J. Acute Dis. 2, 196–200. Ozer, M.S., Sarikurkcu, C., Ceylan, O., Akdeniz, I., Tepe, B., 2017. A comprehensive study
Atanasov, A.G., Waltenberger, B., Pferschy-Wenzig, E.M., Linder, T., Wawrosch, C., on chemical composition, antioxidant and enzyme inhibition activities of the essen-
Uhrin, P., Temml, V., Wang, L.M., Schwaiger, S., Heiss, E.H., Rollinger, J.M., tial oils of Chenopodium botrys collected from three different parts of Turkey. Ind.
Schuster, D., Breuss, J.M., Bochkov, V., Mihovilovic, M.D., Kopp, B., Bauer, R., Crops Prod. 107, 326–331.
Dirsch, V.M., Stuppner, H., 2015. Discovery and resupply of pharmacologically active Popovic-Djordjevic, J.B., Jevtic, I.I., Stanojkovic, T.P., 2018. Antidiabetics: structural
plant-derived natural products: a review. Biotechnol. Adv. 33, 1582–1614. diversity of molecules with a common aim. Curr. Med. Chem. 25, 2140–2165.
Ayvaz, A., Sagdic, O., Karaborklu, S., Ozturk, I., 2010. Insecticidal activity of the essential Ravid, U., Putievsky, E., Katzir, I., 1994. Enantiomeric distribution of piperitone in es-
oils from different plants against three stored-product insects. J. Insect Sci. 10. sential oils of someMentha spp., Calamintha incana (Sm.) Heldr. and Artemisia judaica
Balkan, C.E., Kordali, S., Bozhüyük, A.U., 2018. Antimicrobial effect of plant oils against L. Flavour Fragr. J. 9, 85–87.
some bacterias izolated from patients samples. J. Mol. Genet. Med. 12, 1–2. Sarikurkcu, C., Uren, M.C., Tepe, B., Cengiz, M., Kocak, M.S., 2014. Phenolic content,
Barbieri, N., Costamagna, M., Gilabert, M., Perotti, M., Schuff, C., Isla, M.I., Benavente, enzyme inhibitory and antioxidative activity potentials of Phlomis nissolii and P.
A., 2016. Antioxidant activity and chemical composition of essential oils of three pungens var. pungens. Ind. Crops Prod. 62, 333–340.
aromatic plants from La Rioja province. Pharm. Biol. 54, 168–173. Sarikurkcu, C., Zengin, G., Oskay, M., Uysal, S., Ceylan, R., Aktumsek, A., 2015.
Baytop, T., 1999. Therapy With Medicinal Plants in Turkey (Past and Present), 2nd ed. Composition, antioxidant, antimicrobial and enzyme inhibition activities of two
Nobel Tıp Kitapevi, Istanbul, Turkey. Origanum vulgare subspecies (subsp. vulgare and subsp. hirtum) essential oils. Ind.
Bicas, J.L., Neri-Numa, I.A., Ruiz, A.L.T.G., De Carvalho, J.E., Pastore, G.M., 2011. Crops Prod. 70, 178–184.
Evaluation of the antioxidant and antiproliferative potential of bioflavors. Food Sarikurkcu, C., Ozer, M.S., Calli, N., Popovic-Djordjevic, J., 2018. Essential oil compo-
Chem. Toxicol. 49, 1610–1615. sition and antioxidant activity of endemic Marrubium parviflorum subsp. oligodon. Ind.
Bonnier, G., 1959. Complete Illustree En Couleurs De France Suisse Et Belgium. Belin, Crops Prod. 119, 209–213.
Paris, France. . Sawant, R.L., Lanke, P.D., Wadekar, J.B., 2013. Tyrosinase inhibitory activity, 3D QSAR,
Bouchra, C., Achouri, M., Idrissi Hassani, L.M., Hmamouchi, M., 2003. Chemical com- and molecular docking study of 2,5-disubstituted-1,3,4-oxadiazoles. J. Chem.
position and antifungal activity of essential oils of seven Moroccan Labiatae against 2013 (7).
Botrytis cinerea Pers: Fr. J. Ethnopharmacol. 89, 165–169. Tepe, B., Sarikurkcu, C., Berk, S., Alim, A., Akpulat, H.A., 2011. Chemical composition,

165
J. Popović-Djordjević et al. Industrial Crops & Products 128 (2019) 162–166

radical scavenging and antimicrobial activity of the essential oils of Thymus boveii and Zengin, G., Sarikurkcu, C., Gunes, E., Uysal, A., Ceylan, R., Uysal, S., Gungor, H.,
Thymus hyemalis. Rec. Nat. Prod. 5, 208–220. Aktumsek, A., 2015a. Two Ganoderma species: profiling of phenolic compounds by
Tripathi, A.K., Prajapati, V., Ahmad, A., Aggarwal, K.K., Khanuja, S.P.S., 2004. HPLC-DAD, antioxidant, antimicrobial and inhibitory activities on key enzymes
Piperitenone oxide as toxic, repellent, and reproduction retardant toward malarial linked to diabetes mellitus, Alzheimer’s disease and skin disorders. Food Funct. 6,
vector Anopheles stephensi (Diptera:Anophelinae). J. Med. Entomol. 41, 691–698. 2794–2802.
Tümen, G., Baser, K.H.C., Kürkcüoglu, M., Demircakmak, B., 1995. Composition of the Zengin, G., Sarikurkcu, C., Uyar, P., Aktumsek, A., Uysal, S., Kocak, M.S., Ceylan, R.,
essential oil of Calamintha incana (Sm.) Boiss. from Turkey. J. Essent. Oil Res. 7, 2015b. Crepis foetida L. subsp. rhoeadifolia (Bleb.) Celak. as a source of multi-
679–680. functional agents: cytotoxic and phytochemical evaluation. J. Funct. Foods 17,
Viney, D.E., 1994. An Illustrated Flora of North Cyprus. Koenigstein, Germany. . 698–708.

166