ORIGINAL ARTICLE
Rec. Nat. Prod. 8:3 (2014) 242-261
Chemical Diversity and Biological Activity of the Volatiles of Five
Artemisia Species from Far East Russia
Gulmira Özek1*, Yerlan Suleimen2, Nurhayat Tabanca3,
Roman Doudkin4,5,6, Petr G. Gorovoy4, Fatih Göger1, David E. Wedge7,
Abbas Ali3, Ikhlas A. Khan3,8 and Kemal Hüsnü C. Başer1,9,10
1
Department of Pharmacognosy, Faculty of Pharmacy, Anadolu University, Eskişehir, 26470, Türkiye
2
The Institute of Applied Chemistry, Department of Chemistry, L.N. Gumilyov Eurasian National
University, 010008 Astana, Kazakhstan
3
National Center for Natural Products Research, The University of Mississippi, University,
MS 38677, USA
4
Laboratory of Chemotaxonomy, Pacific Institute of Bioorganic Chemistry of the Far Eastern Branch of
the Russian Academy of Sciences, 690022 Vladivostok, Russia
5
Department of Biodiversity and Marine Biology, School of Natural Sciences, Far Eastern Federal
University, 8, Sukhanova st., 690950, Vladivostok, Russia
6
Laboratory of Flower Introduction, Botanical Garden Institute of the Far Eastern Branch of the Russian
Academy of Sciences, 142, Makovskogo., 690024, Vladivostok, Russia
7
USDA-ARS Natural Products Utilization Research Unit, University of Mississippi, University,
MS 38677 USA
8
Department of Pharmacognosy, School of Pharmacy, The University of Mississippi, University,
MS 38677 USA
9
Department of Botany and Microbiology, King Saud University, College of Science, 11451 Riyadh,
Saudi Arabia
10
Bahcesehir University, Technology Transfer Office, Besiktas, 34353 Istanbul, Türkiye
(Received August 27, 2013; Revised January 21, 2014; Accepted February 19, 2014)
Abstract: Artemisia argyi, A. feddei, A. gmelinii, A. manshurica, and A. olgensis (Asteraceae) were collected in
Far East Russia. Oils were hydrodistilled and simultaneously analyzed by GC-FID and GC/MS. Main
constituents were found as follows in Artemisia oils: selin-11-en-4α-ol (18.0%), 1,8-cineole (14.2.0%), artemisia
alcohol (12.9%), borneol (9.7%) in A. argyi; camphor (31.2%), 1,8-cineole (17.6%), α-thujone (5.7%) in A.
feddei; longiverbenone (12.0%), isopinocamphone (8.9%), 1,8-cineole (6.7%), camphor (5.8%), trans-p-menth2-en-1-ol (5.3%) in A. gmelinii; germacrene D (11.2%), rosifoliol (10.1%), caryophyllene oxide (6.8%),
eudesma-4(15),7-dien-1β-ol (5.6%) in A. manshurica; eudesma-4(15),7-dien-1β-ol (6.9%), caryophyllene oxide
(5.6%), guaia-6,10(14)-dien-4β-ol (5.1%) and hexadecanoic acid (5.0%) in A. olgensis. Oils were subsequently
submitted for antifungal and antimosquito evaluations. Artemisia species oils showed biting deterrent effects in
Aedes aegypti and Artemisia gmelinii oil with the most active biting deterrence index values of 0.82 ± 0.1 at 10
µg/mL. Larval bioassay of A. gmelinii and A. olgensis oils showed higher larvicidal activity against Ae. aegypti
larvae with LD50 values of 83.8 (72.6 – 95.7) ppm and 91.0 (73.8 – 114.5) ppm, respectively. Antifungal
activity was evaluated against the strawberry anthracnose-causing fungal plant pathogens Colletotrichum
acutatum, C. fragariae and C. gloeosporioides using direct overlay bioautography assay and all showed nonselective weak antifungal activity. Antioxidant evaluation of the oils was performed by using β-carotene
bleaching, Trolox equivalent and DPPH tests. The tested Artemisia oils demonstrated moderate antioxidant
activity.
Keywords: Artemisia; essential oil; antifungal; botanical insecticidal; mosquito control; antioxidant activity.
©2014 ACG Publications. All rights reserved.
* Corresponding author. E-mail address: gozek@anadolu.edu.tr; gulmiraozek@gmail.com,
Tel.: +90-222-3350580/3716; fax:+ 90-222-3306809
The article was published by Academy of Chemistry of Globe Publications
www.acgpubs.org/RNP © Published 05/01/2014 EISSN: 1307-6167
Özek et al., Rec. Nat. Prod. (2014) 8:3 242-261
1. Introduction
Artemisia L. is from the Asteraceae-Anthemideae-Artemisiinae and ranks among the most
species-rich plant genera. The genus contains approximately 500 taxa at specific or subspecific levels
almost exclusively found in the northern hemisphere. Artemisia is centered in and most likely
originated from Central Asia [1, 2]. It was well documented in literature that Artemisia species have
been used since ancient times for food and medicinal purposes [3]. The genus Artemisia has been the
subject of numerous chemical and biological studies, yielding primarily sesquiterpene lactones [4,5],
diterpenes, coumarins [1], polyacetylenes [6] and flavonoids [1,7,8] as the main metabolites.
Biological activity of Artemisia species includes antitumor [9-16], antimalarial [17,18], antibacterial
[19,20], antifungal [21,22], antimutagenic [22,23], repellent and antifeedant [24], larvicidal [25,26]
and vasorelaxant [27] properties.
Previous chemical investigations of A. argyi demonstrated the presence of coumarins [9],
flavones [8, 15, 23, 28-30], mono- and sesquiterpenes [31-36], lactones [11], ketones [27], sitosterols
[37] and lipophilic constituents [38]. Pharmacological studies on A. argyi proved terpinen-4-ol and βcaryophyllene as the antiasthmatic principles of the oil [39-40]. Antitumor [9, 12, 15, 16, 28, 33, 41],
cytotoxic [13], antimutagenic [23], anti-inflammatory, antioxidative [42], antibacterial [20], antifungal
[21,22], antifeedant [24, 26] and vasorelaxant [27] activities of A. argyi were reported earlier. In
Traditional Chinese Medicine (TCM), A. argyi is used as raw material and processed into moxa wool
[43]. This plant is also identified as “Aeyup” and used as important medicinal material in traditional
Korean medicine [44]. Huang and Liu (1999) [45] provided a basis for A. argyi and A. indica
differentiation, application and utilization using their macroscopical and microscopical characteristics,
TLC and UV spectra [45]. A. feddei was subjected earlier to investigation for coumarins [46],
sesquiterpene lactones [47-50] and monoterpenes [51]. Scopoletin (coumarin) detected in the water
extract of Artemisia feddei was reported as an inducible nitric oxide synthesis inhibitory active
constituent. [46], while the oil demonstrated antibacterial activity [19]. A. gmelinii was also reported
for coumarins with scopoletin as major constituent [52]. A literature search did not reveal any
scientific reports on the composition of A. manshurica and A. olgensis volatiles.
As a continuation of our investigations on Artemisia oils, we studied the chemical composition
and biological activity of essential oil from five Artemisia species: Artemisia argyi Lév. et Vaniot, A.
feddei Lév. et Vaniot, A. gmelinii Web. ex Stechm., A. manshurica (Komarov) Komarov, A. olgensis
(Vorobiev) Worosch. collected in Far East region of Russia. In a program aimed at discovering natural
fungicides and insecticides as alternatives to conventional synthetic agrochemicals, unique Artemisia
species from Russia were evaluated for biopesticide activity. The oils were tested for antifungal
activity using direct bioautography assays against three Colletotrichum species and for deterrent and
larvicidal activity against Aedes aegypti (L.). Also, in a second research effort to study natural sources
for effective antioxidants, Artemisia essential oils were subjected to investigation by three antioxidant
methods: (i) β-carotene bleaching assay, (ii) Trolox equivalent (TEAC) assay, (iii) 1,1-diphenyl-2picrylhydrazyl (DPPH) assay. There are several reports on antioxidant activity of Artemisia oils [6, 53,
54] compared to α-tocopherol, butylated hydroxytoluene (BHT) and tertiary butylhydroquinone
(TBHQ). There has been a growing interest in research concerning natural antioxidant active
compounds, including the plant extracts and essential oils that are less damaging to the mammalian
health and environment. Antioxidants retard oxidation and are often added to numerous meat and
poultry products to prevent or slow oxidative degradation of fats. Free radical scavenging, chelating of
pro-oxidant metal ions or quenching singlet-oxygen formation mechanisms are involved in antioxidant
action of natural antioxidants [7]. The present work is the first report on the chemical composition and
biological activity of Artemisia oils from the Far East of Russia.
2. Materials and Methods
2.1. Plant materials
Plant materials, voucher specimens codes, plant parts studied and essential oil yields are
given in Table 1. Voucher specimens were kept at the Herbarium of the Department of Botany of Far
Eastern Federal University, Russia. Botanical identifications were carried out by R. Doudkin and P.
243
Chemical diversity and biological activities of five Artemisia species
244
Gorovoy from Pacific Institute of Bioorganic Chemistry (Laboratory of Chemotaxonomy) of the Far
Eastern Branch of the Russian Academy of Sciences.
Table 1. Collection data for the Artemisia species studied
Artemisia ssp.
Artemisia argyi
Artemisia feddei
Artemisia gmelinii
Artemisia manshurica
Artemisia olgensis
Collection place
Primorsky Krai, Nadejdinsky
District, meadow around
Terekhovka village
Primorsky Krai, Nadejdinsky
District, stream near to
Terekhovka village
Primorsky Krai, Partizansky
District, Nakhodkinsky crossing
Primorsky Krai, Partizansky
District, Nakhodkinsky crossing
Primorsky Krai, Olginsky
District, “Siniye Skali”, west side
of Olga village
Voucher
specimen
No
Oil yield
(%)
Plant part
used for
distillation
Oil color
27891
0.36
Aerial
Turquoise
27883
0.20
Aerial
Green
27887
1.60
Aerial
Turquoise
27876
0.16
Aerial
Yellowish
27879
0.05
Aerial
Yelloworange
2.2. Chemicals
All organic solvents and reagents used were of analytical or chromatographic grade.
Anhydrous sodium sulfate (ACS-ISO, for analysis), n-hexane, acetone (ACS, for analysis) and
dimethyl sulfoxide (DMSO) were purchased from Carlo Erba (Italy). Technical grade commercial
fungicides benomyl, cyprodinil, azoxystrobin, and captan (Chem Service, Inc., West Chester, PA,
USA) were used as fungicide standards at 2 mM in 2 µL of 95% ethanol. DPPH was supplied from
Sigma-Aldrich Chemie (Steinheim, Germany). For the antifungal assay, potato-dextrose broth (Difco,
Detroit, MI, USA), glass silica gel thin layer chromatography (TLC) plates with a fluorescent indicator
(250 mm, Silica Gel GF Uniplate, Analtech, Inc., Newark, DE, USA), and a moisture chamber (398-C,
Pioneer Plastics, Inc., Dixon, KY, USA) were used. Monobasic sodium phosphate (Fisher Scientific
Chemical Co., Fairlawn, NJ) and adenine (Sigma-Aldrich, St. Louis, MO) were used for mosquito
biting bioassay. DEET (99.1 % purity; N,N-diethyl-3-methylbenzamide, Sigma Aldrich, St. Louis,
MO) was used as a positive control. Molecular biology grade ethanol was obtained from Fisher
Scientific Chemical Co. (Fairlawn, NJ).
2.3. Isolation of essential oils
Air dried aerial parts of the collected Artemisia species were hydrodistilled separately for 3 h
using a Clevenger-type apparatus according to the procedure published in European Pharmacopoeia.
Percent yields (v/w) of the oils calculated on a moisture free basis are given in Table 1. The oils were
dried over anhydrous sodium sulphate and stored in sealed vials in dark, at 4° C, until GC-FID and
GC/MS analyses. The oils were dissolved in n-hexane to conduct chromatographic determination of
their composition.
2.4. Gas Chromatography – Mass Spectrometry (GC/MS)
The oils were analyzed by capillary GC-FID and GC/MS techniques using an Agilent
5975 GC-MSD system (Agilent, USA; SEM Ltd., Istanbul, Turkey). The same column and analytical
conditions were used for both GC/MS and GC-FID. HP-Innowax FSC column (60m × 0.25mm, 0.25
µm film thickness, Agilent, Walt & Jennings Scientific, Wilmington, Delaware, USA) was used with
helium as a carrier gas (0.8 mL/min). GC oven temperature was kept at 60°C for 10 min and
programmed to 220°C at a rate of 4°C/min, and kept constant at 220°C for 10 min and then
programmed to 240°C at a rate of 1°C/min. The split ratio was adjusted at 40:1. Flame ionization
Özek et al., Rec. Nat. Prod. (2014) 8:3 242-261
detection and injector temperature were performed at 250°C. Mass spectrums were taken at 70 eV.
Mass range was from m/z 35 to 450.
2.5. Gas Chromatography (GC-FID)
The GC-FID analysis was carried out using an Agilent 6890N GC system (SEM Ltd., Istanbul,
Turkey). FID detector temperature was 300°C. In order to obtain t h e same elution order with
GC/MS, simultaneous injection was done by using the same column and appropriate operational
conditions.
2.6. Identification and quantification of compounds
Identification of the volatile constituents was achieved by parallel comparison of their retention
indices and mass spectra with data published in the WILEY GC/MS Library (Wiley, New York, NY,
USA), MASSFINDER software 4.0 (Dr. Hochmuth Scientific Consulting, Hamburg, Germany)
(Hochmuth, 2008), ADAMS Library and NIST Library (Adams 2007), and the in-house “Başer
Library of Essential Oil Constituents” database, obtained from chromatographic runs of pure
compounds performed with the same equipment and conditions. A C9-C30 n-alkane standard
solution (Fluka, Buchs, Switzerland) was used to spike the samples in the calculation of retention
indices (RI). Quantification of volatiles components was performed on the basis of their GC-FID
peak area using integration data.
2.7. Antifungal activity test
The oils were evaluated for antifungal activity against strawberry anthracnose-causing plant
pathogens, Colletotrichum acutatum, C. fragariae and C. gloeosporioides using the direct overlay
bioautography assay described by Wedge [55].
2.8. Insects
Ae. aegypti (L.) used in these studies were from a laboratory colony maintained since 1952
at the Mosquito and Fly Research Unit at Center for Medical, Agricultural and Veterinary
Entomology, USDA-ARS, Gainesville, Florida. This colony is maintained since 1952 using standard
procedures [56]. The eggs were stored in laboratory to use as per need. Mosquitoes were reared to the
adult stage by feeding the larvae on a diet of 2:1 alfalfa pellets (US Nutrition Inc. Bohemia, NY)
and hog chow (Ware Milling 150 ALF Drive, Houston, MS 38851). The diet contents were ground in
a grinder and passed through sieve no. 40, 425 micron (USA Standard Sieve, Humboldt MFG. Co.
Norridge, IL 60706).
2.9. Mosquito biting bioassays
Experiments were conducted by using a six-celled in vitro Klun & Debboun (K & D) module
bioassay system developed by Klun et al. 2005 [57] for quantitative evaluation of bite deterrent
properties of candidate compounds for human use. This bioassay method determines specifically
measured biting (feeding) deterrent properties of the chemicals. Briefly the assay system consists of a
six well blood reservoir with each of the 3 cm × 4 cm wells containing 6 mL of blood. As reported
earlier [58], female mosquitoes feed as well on the CPDA-1 (citrate-phosphate-dextrose-adenine) +
ATP as they do on blood. Therefore, we used the CPDA-1 + ATP instead of human blood. CPDA-1
was prepared by dissolving 3.33 g sodium citrate, 0.376 g citric acid, 4.02 g dextrose, 0.28 g
monobasic sodium phosphate and 0.346 g of adenine in 1026 mL of de-ionized water. ATP was
added to CPDA-1 to yield 10-3 M ATP (AABB 2005). CPDA-1 and ATP preparations were freshly
made on the day of the test. DEET was used as a positive control. Molecular biology grade ethanol
was obtained from Fisher Scientific Chemical Co. (Fairlawn, NJ). Five Artemisia essential oils
were tested in this study and used DE ET at 25 nmol/cm2 as a positive control. All the treatments
were prepared in acetone. The stock solutions were kept in a refrigerator at 3-4°C. Treatments were
prepared fresh at the time of bioassay.
245
Chemical diversity and biological activities of five Artemisia species
246
The temperature of the solution in the reservoirs was maintained at 37°C by continuously
passing the warm water through the reservoir using a circulatory bath. The reservoirs were covered
with a layer of collagen membrane. This CPDA-1+ATP solution membrane unit simulated a human
host for mosquito feeding. The test compounds were randomly applied to six 4 cm × 5 cm areas of
organdy cloth and positioned over the membrane-covered CPDA-1+ATP solution with a separator
placed between the treated cloth and the six-celled module. A six celled K & D module containing
five females per cell was positioned over cloth treatments covering the six CPDA-1+ATP solution
membrane wells, and trap doors were opened to expose the treatments to these females. The number
of mosquitoes biting through cloth treatments in each cell was recorded after a 3 min exposure and
mosquitoes were prodded back into the cells. These mosquitoes were then squashed to determine the
number which has actually engorged the solution. A replicate consisted of six treatments: four test
compounds, DEET (a standard mosquito repellent compound) and acetone treated cloth as solvent
control. The 25 nmol DEET/cm2 cloth dose was used as a standard, because it suppresses mosquito
biting by 80% as compared to controls [57]. A set of replications was conducted on different days
using new lots. Treatments were replicated 15 times in oil.
2.10. Larval bioassays
Bioassays were conducted by using the bioassay system described by Pridgeon et al. (2009)
[59] to determine the larvicidal activity of five Artemisia species from Far East Russia against Ae.
aegypti. In brief, the eggs were hatched under vacuum (1-h) by placing a piece of a paper towel
with eggs in a cup filled with 100 mL of deionized water containing small quantity of larval diet.
Larvae were removed from vacuum and held overnight in the cup in a temperature-controlled
chamber maintained at a temperature of 27±2°C and 70 ± 5% RH at a photoperiod regimen of
12:12 (L:D) h. Five 1-d-old first instar Ae. aegypti were added to each well of 24-well plates placed
on illuminated light box by using a disposable 22.5-cm Pasteur pipette with a droplet of water. Fifty
µL of larval diet (2% slurry of 2:1 alfalfa pellets and hog chow) were added to each well by using a
Finnpipette stepper (Thermo Fisher, Vantaa, Finland). All chemicals to be tested were diluted in
dimethyl sulfoxide (DMSO). Eleven microliters of the test chemical was added to the labeled wells,
and in control treatments 11 µL of DMSO alone was added. Each well had a total volume of 1.1
mL. After the treatment, the plates were swirled in clockwise and counter clockwise motions and
front and back and side to side five times to ensure even mixing of the chemicals. Larval mortality
was recorded 24- and 48-h after treatment. Larvae that showed no movement in the well after manual
disturbance of water by a pipette tip were recorded as dead. A series of dosages (4 - 5 concentrations)
were used in each treatment to get a range of mortality. Treatments were replicated 15 times in oil.
LD50 values for larvicidal data were calculated by using the Probit procedure of SAS (SAS Institute
2007). Control mortality was corrected by using Abbott’s formula.
2.11. Statistical analyses
Since the K&D module bioassay system can handle only 4 treatments along with negative and
positive controls, in order to make direct comparisons among more than four test compounds and to
compensate for variation in overall response among replicates, repellency was quantified as Biting
Deterrence Index (BDI). BDI’s were calculated using the following formula:
Where PNBi,j,k denotes the mean proportion of females not biting in test compound i for replication j
and day k (i=1-4, j=1-5, k=1-2), PNBc,j,k denotes the mean proportion of females not biting in
solvent control for replication j and day k (j=1-5, k=1-2) and PNBd,j,k denotes the mean proportion
of females not biting in response to DEET (positive control) for replication j and day k (j=1-5, k=1-
Özek et al., Rec. Nat. Prod. (2014) 8:3 242-261
247
2). This formula adjusts for variation in response among replication days and incorporates
information from the solvent control as well as positive control.
A BDI value of 0 indicates an effect similar to acetone. A BDI value significantly greater than
0 indicates an anti-biting effect relative to ethanol. BDI values not significantly different from 1
are statistically similar to DEET. BDI values were analyzed by using the ANOVA procedure of SAS
(SAS Institute 2007) and means were separated using the Ryan-Einot-Gabriel-Welsch Multiple Range
method.
2.12. Antioxidant activity tests
Antioxidant activity was evaluated on three tests: TEAC [60], 1,1- Diphenyl-2-picrylhydrazyl
(DPPH•) radical scavenging test [61] and inhibition of β-carotene/linoleic acid co-oxidation [62, 63],
which were carried out using procedures described previously.
3. Results and Discussion
Within scope of the present work, we carried out the gas-chromatography of the essential oils
of Artemisia argyi, A. feddei, A. gmelinii, A. manshurica, and A. olgensis. Hydrodistillation of the
dried aerial parts of five Artemisia species gave oils with specific odors and different colors
(Table 1). The oil yield was found as highest in A. gmelinii (1.60%) and lowest in A. olgensis
(0.05%). The list of detected compounds with their relative percentages, retention indices and
percentages of compound is given in Table 2 in order of their elution time on the HP-Innowax FSC
column. All the volatile constituents detected in the oils of the five Artemisia species were classified
in order of abundance as monoterpene (C10H16) and sesquiterpene (C15H24) hydrocarbons, their
oxygenated derivatives, and non-isoprenoid compound (Table 3). The oils of A. argyi, A. feddei and
A. gmelinii were found to be rich with oxygenated monoterpenes, while the oils of A. manshurica and
A. olgensis consisted primarily of oxygenated sesquiterpenes.
Table 2. Chemical composition of the volatiles of Artemisia species
Compounda
Content (%)d
RRIb
RRIc
Ref.
Aae
Aff
Agg
Amh
Aoi
Tricyclene
1014
1017
[64]
tk
0.1
-
-
-
α-Pinene
1032
1032
[65]
0.3
0.1
0.1
-
0.1
Santolina triene
1043
1031
[7]
t
-
-
2.6
-
Camphene
1076
1085
[64]
0.4
1.8
0.2
-
-
β-Pinene
1118
1118
[64]
0.2
0.1
1.1
-
0.5
Myrcene
1174
1156
[64]
-
-
-
t
0.5
α-Phellandrene
1180
1186
[66]
-
-
0.2
-
-
α-Terpinene
1188
1179
[64]
0.4
0.4
0.2
-
-
Dehydro-1,8-cineole
1195
1200
[67]
0.1
0.1
t
-
-
Limonene
1203
1205
[64]
t
-
0.1
-
t
1,8-Cineole
1210
1204
[68]
14.2
17.6
6.7
-
-
2-Pentyl furan
1244
1237
[69]
T
0.1
-
-
t
γ-Terpinene
1255
1256
[64]
0.9
0.9
0.3
-
t
(E)-β-Ocimene
1266
1252
[70]
-
-
-
t
0.3
p-Cymene
1280
1279
[64]
1.2
1.4
0.7
-
t
Terpinolene
1290
1283
[64]
0.2
0.3
0.1
-
-
Chemical diversity and biological activities of five Artemisia species
a
Compound
RRI
b
c
RRI
248
Content (%)d
Ref.
Aae
Aff
Agg
Amh
Aoi
-
0.1
-
-
-
1,2,3-Trimethyl benzene
1355
Artemisia ketone
1358
1358
[71]
0.1
-
0.7
-
Nonanal
1390
1389
[72]
-
-
-
-
0.2
Yomogi alcohol
1403
1401
[73]
3.8
0.2
0.1
-
-
Santolina alcohol
1405
1413
[73]
0.1
-
-
-
-
Artemisyl acetate
1423
0.6
-
-
-
-
α-Thujone
1435
1428
[73]
0.1
5.7
1.2
-
-
β-Thujone
1445
1438
[74]
1.1
2.8
0.8
-
-
α-Cubebene
1467
1468
[75]
-
-
0.1
-
-
trans-Sabinene hydrate
1474
1474
[76]
3.2
1.0
0.3
-
-
α-Longipinene
1479
1469
[77]
-
t
0.2
-
-
α-Copaene
1497
1497
[70]
0.2
t
0.5
0.4
0.3
Decanal
1499
-
0.1
-
-
-
Artemisia alcohol
1510
1512
[71]
12.9
0.2
0.1
-
-
Chrysanthenone
1531
1540
[71]
T
1.3
0.1
-
-
Camphor
1533
1532
[64]
1.4
31.2
5.8
0.5
-
α-Gurjunene
1539
1529
[78]
-
t
0.1
-
-
Dihydroachillene
1547
-
0.3
t
-
-
β-Cubebene
1549
1547
[78]
-
-
0.4
0.1
0.2
cis-Sabinene hydrate
1556
1556
[79]
2.0
0.9
0.3
-
-
Isopinocamphone
1562
-
-
8.9
-
-
trans-p-Menth-2-en-1-ol
1571
1622
[80]
0.4
0.5
5.3
-
-
cis-Chrysanthenyl acetate
1582
1583
[71]
0.1
-
-
-
-
Pinocarvone
1584
1587
[78]
0.2
0.4
2.8
-
-
Bornyl acetate
1586
1582
[74]
0.3
0.3
0.4
0.8
0.5
Nopinone
1597
1597
[78]
-
t
0.4
-
-
β-Elemene
1600
1602
[81]
-
-
t
0.3
-
Thymol methyl ether
1604
1611
-
-
-
-
0.2
epi-Bicyclosesquiphellandrene
1605
-
-
-
0.2
-
β-Copaene
1609
-
-
0.1
-
-
Terpinen-4-ol
1611
1617
[66]
4.1
-
0.9
-
-
β-Caryophyllene
1612
1604
[70]
-
3.0
1.9
4.0
2.0
cis-p-Menth-2-en-1-ol
1640
1645
[66]
0.3
0.4
3.9
-
0.3
Thuj-3-en-10-al
1642
-
0.1
-
-
-
Myrtenal
1648
1648
[78]
0.2
0.3
0.9
-
-
Sabinaketone
1651
1651
[77]
-
0.1
0.1
-
-
Isobornyl propionate
1655
1676
0.1
-
-
-
-
Sabinyl acetate
1658
-
0.2
-
-
trans-Pinocarvyl acetate
1661
-
-
-
-
0.1
Özek et al., Rec. Nat. Prod. (2014) 8:3 242-261
a
Compound
RRI
b
c
249
Content (%)d
RRI
Ref.
Aae
Aff
Agg
Amh
Aoi
cis-Verbenol
1663
1663
[78]
0.1
0.1
-
-
-
(Z)-β-Farnesene
1668
1670
[82]
t
-
-
1.0
0.4
trans-Pinocarveol
1670
1646
[80]
0.3
0.5
1.0
-
-
epi-Zonarene
1675
1675
[78]
-
-
0.2
-
-
δ-Terpineol
1680
1680
[75]
0.3
0.2
0.1
-
-
trans-Verbenol
1683
1666
[83]
0.6
0.5
-
-
-
Isoborneol
1684
1669
[72]
-
-
0.2
-
-
cis-Piperitol
1687
1692
[66]
-
-
1.3
-
-
α-Humulene
1689
1689
[78]
0.1
0.1
0.5
1.2
0.3
Drima-7,9(11)-diene
1694
-
-
0.5
-
-
(E)-β-Farnesene
1695
0.2
-
-
-
-
Myrtenyl acetate
1704
-
-
0.1
-
-
γ-Muurolene
1704
1704
[78]
-
-
0.1
1.0
0.4
α-Terpineol
1706
1706
[78]
3.0
0.3
0.7
-
-
Borneol
1719
1719
[78]
9.7
3.6
3.3
-
-
Verbenone
1725
1725
[81]
-
0.3
-
-
-
Germacrene D
1726
1726
[78]
-
-
0.9
11.2
4.2
(Z,E)-α-Farnesene
1737
-
-
-
2.9
2.0
p-Mentha-1,5-dien-8-ol
1738
1714
[83]
-
t
0.2
-
-
α-Muurolene
1740
1742
[66]
-
-
-
0.6
0.7
β-Selinene
1742
1731
[66]
0.3
t
0.7
-
-
Piperitone
1746
1744
[66]
-
0.7
1.8
-
-
Carvone
1751
1750
[66]
0.1
0.3
-
-
-
trans-Piperitone oxide
1754
-
-
0.4
-
-
Bicyclogermacrene
1756
1756
[78]
-
-
0.3
0.5
0.2
cis-Piperitol
1757
1757
[71]
0.2
0.2
3.2
-
-
(E,E)-α-Farnesene
1758
1750
[84]
-
-
-
1.4
0.6
cis-Chrysanthenol
1764
4.4
0.1
0.2
-
-
δ-Cadinene
1773
1773
[77]
-
0.1
0.7
1.1
0.9
γ-Cadinene
1776
1779
[81]
-
-
0.1
0.4
0.2
cis-Carvyl acetate
1782
-
0.1
-
-
-
β-Sesquiphellandrene
1783
1783
[77]
-
-
-
0.3
-
ar-Curcumene
1786
1786
[77]
0.1
t
0.1
1.3
0.6
Cadina-1,4-diene (=Cubenene)
1799
1799
[78]
-
-
0.1
-
-
Benzene propanal
1800
-
0.3
-
-
-
Cumin aldehyde
1802
0.1
0.3
0.1
-
-
Myrtenol
1805
0.2
0.3
1.1
-
-
α-Campholene alcohol
1806
0.1
-
0.3
-
-
Liguloxide
1811
-
-
0.1
-
-
Fragranol
1824
-
-
3.8
-
-
1807
[66]
Chemical diversity and biological activities of five Artemisia species
a
Compound
RRI
b
c
RRI
250
Content (%)d
Ref.
Aae
Aff
Agg
Amh
Aoi
t
0.1
-
-
0.2
(E,E)-2,4-Decadienal
1827
trans-Carveol
1845
1845
[78]
0.2
0.1
0.3
-
-
cis-Calamenene
1853
1849
[85]
-
0.1
0.2
-
0.3
m-Cymen-8-ol
1856
-
-
0.2
-
-
Fragranyl isobutyrate
1866
-
-
0.2
-
-
p-Cymen-8-ol
1864
1865
[66]
0.1
0.2
-
-
-
(E)-Geranyl acetone
1868
1868
[77]
t
0.1
-
-
0.4
trans-Myrtanol
1872
-
-
0.3
-
-
Aplotaxene
1880
-
-
-
-
0.2
cis-Carveol
1882
0.3
0.1
-
-
-
epi-Cubebol
1900
-
-
0.2
-
-
α-Calacorene
1931
-
t
0.1
-
t
1,5-Epoxy-salvial(4)14-ene
1945
0.1
-
0.1
0.2
0.6
Palustrol
1949
-
0.1
-
-
Cubebol
1957
-
0.1
0.2
-
-
Isocaryophyllene oxide
2001
2001
[77]
0.2
0.3
0.1
0.7
0.3
Caryophyllene oxide
2008
2008
[76]
2.2
4.4
1.6
6.8
5.6
Perilla alcohol
2029
0.1
t
0.4
-
Salvial-4(14)-en-1-one
2037
0.2
0.1
0.1
2.1
2.5
Pentadecanal
2041
-
0.1
-
-
-
Guaia-6,10(14)-dien-4-ol isomer*
2029
-
-
-
-
1.5
(E)-Nerolidol
2050
2049
[75]
t
t
0.2
1.0
0.5
Ledol
2057
2057
[78]
-
0.2
-
-
-
Humulene epoxide-II
2071
2071
[78]
0.2
0.3
0.4
1.5
0.8
Junenol
2073
-
0.1
-
0.9
1.1
Guaiyl acetate
2094
-
-
-
t
0.8
p-Mentha-1,4-dien-7-ol
2073
-
0.2
t
-
-
Caryophylla-2(12),6(13)-dien-5-one
2074
0.1
0.1
t
-
-
cis-Sesquisabinene hydrate
2085
0.1
-
-
0.4
-
Caryophyll-5-en-12-al
2098
0.1
-
-
-
-
Cubenol
2080
2080
[87]
0.2
-
-
Cumin alcohol
2100
2068
[88]
Salviadienol
2128
Hexahydrofarnesyl acetone
2131
2132
Rosifoliol
2144
Spathulenol
2144
Nor-Copaonone
2179
γ-Eudesmol
2185
Eremoligenol
2183
Eugenol
2186
1878
1918
1934
2016
[78]
[84]
[75]
[86]
t
0.1
0.2
-
-
0.1
0.1
0.1
1.4
1.9
[89]
0.1
0.3
0.1
-
0.6
2144
[90]
-
-
-
10.1
-
2150
[79]
0.3
0.4
1.5
0.4
4.9
-
-
-
0.6
0.9
-
0.3
-
1.0
-
-
-
-
1.1
-
0.2
-
-
-
-
2179
2186
[81]
[78]
Özek et al., Rec. Nat. Prod. (2014) 8:3 242-261
a
Compound
RRI
b
c
251
Content (%)d
RRI
Ref.
Aae
Aff
Agg
Amh
Aoi
2189
[91]
-
-
-
-
1.6
-
0.3
-
-
0.4
-
-
-
0.7
0.6
0.2
-
-
-
-
-
0.1
-
-
-
-
-
-
-
0.6
T-Cadinol
2187
Nonanoic acid
2192
T-Muurolol
2209
Zingiberenol
2188
Clovenol
2205
Torreyol
2207
ar-Turmerol
2214
2214
[77]
0.1
0.2
-
-
0.2
α-Bisabolol
2232
2233
[93]
-
-
-
-
0.2
Carvacrol
2239
2239
[65]
0.2
0.1
-
-
-
trans-α-Bergamotol
2247
2247
[77]
-
-
-
-
0.3
Torilenol
2248
0.1
0.1
-
3.3
3.8
α-Cadinol
2255
2231
[80]
-
-
-
1.5
1.4
β-Eudesmol
2257
2231
[80]
-
0.8
-
-
-
Longiverbenone (= Vulgarone B)
2265
-
0.4
12.0
-
1.2
Alismol (=6,10(14)-Guaiadien-4β-ol)
2272
-
-
-
-
5.1
Selin-11-en-4α-ol
2273
18.0
0.6
-
-
0.5
Cyperenone
2276
0.1
-
-
-
-
Oxo-α-Ylangene
2289
-
0.5
-
-
-
Decanoic acid
2298
2288
[94]
-
-
-
-
1.0
Tricosane
2300
2300
[78]
-
0.1
-
-
-
(6S, 7R)-Bisabolone
2311
0.2
-
-
-
-
Caryophylla-2(12),6(13)-dien-5β-ol
(=Caryophylladienol I )
2316
Caryophylla-2(12),6(13)-dien-5α-ol
(=Caryophylladienol II)
2324
2209
2205
2272
[92]
[90]
[77]
2316
[77]
0.3
0.3
-
-
-
2324
[77]
0.1
0.2
-
-
-
0.4
-
0.6
-
2.5
Eudesma-4(15),7-dien-ol isomer*
2326
Eudesm-4(15),7-dien-1β-ol
2362
2351
[95]
-
0.2
-
5.6
6.9
Manoyl oxide
2376
2347
[83]
-
-
-
-
2.2
Caryophylla-2(12),6-dien-5α-ol
(=Caryophyllenol I)
2389
2389
[90]
0.1
0.2
-
-
0.6
Caryophylla-2(12),6-dien-5β-ol
(=Caryophyllenol II)
2392
2392
[77]
0.4
0.8
0.3
-
1.3
-
0.1
-
-
-
(Z)-Nuciferal
2393
Chamazulene
2420
2373
[64]
0.1
-
0.1
-
-
Pentacosane
2500
2500
[77]
-
0.1
-
-
-
Dodecanoic acid
2503
2504
[96]
-
-
t
-
0.8
14-Hydroxy-α-muurolene
2535
-
-
t
-
0.4
γ-Costol
2533
0.1
-
-
-
-
α-Costol
2604
-
0.1
-
-
-
β-Costol
2606
0.1
t
-
-
-
14-Hydroxy-δ-cadinene
2607
-
-
0.1
-
0.4
Chemical diversity and biological activities of five Artemisia species
a
Compound
RRI
b
c
252
Content (%)d
RRI
Ref.
Aae
Aff
Agg
Amh
Aoi
Phytol
2622
2620
[84]
0.1
0.1
0.1
-
t
Tetradecanoic acid
2670
2672
[97]
0.2
0.2
-
-
1.2
Heptacosane
2700
2700
[98]
-
t
-
-
0.5
Hexadecanoic acid
2931
2930
[85]
0.9
1.5
0.3
3.5
5.0
95.2
94.8
88.4
74.6
77.4
Total
a
Compounds were identified by comparison of their RI (determined rel. to n-alkanes (C9–C30) and mass spectra with those
of authentic compounds or with databases) (see Exper. part).
b
Relative retention indices (RRI) experimentally determined against n-alkanes on HP-Innowax FSC column.
c
Relative retention indices reported in literature.
d
The contents (%) of the individual components were calculated based on the peak area (FID response).
e
Aa: Artemisia argyi; f Af: A. feddei; g Ag: A. gmelinii; h Am: A. manshurica; i Ao: A. olgensis.
k
t: Trace (< 0.1 %); * Correct isomer not identified.
Table 3. Distribution of main compound classes in the Artemisia oils studied
Compound class
Monoterpene hydrocarbons
Oxygenated monoterpenes
Sesquiterpene hydrocarbons
Oxygenated sesquiterpenes
Other
Aa
Af
%
Ag
3.6
65.2
0.9
24.1
1.4
5.2
71.3
3.3
11.5
3.5
3.0
58.6
7.8
18.1
0.9
Am
Ao
2.6
1.3
27.7
39.5
3.5
1.4
1.4
12.9
49.6
12.1
Aa : A. argyi; Af: A. feddei; Ag: A. gmelinii; Am: A. manshurica; Ao: A. olgensis.
Ninety six compounds representing 95.2 % of the oil were characterized in A. argyi.
Monoterpenes (68.8%) consisted primarily of oxygenated forms (65.2%) were represented by 1,8cineole (14.2%), artemisia alcohol (12.9%), borneol (9.7%), cis-chrysanthenol (4.4%), terpinen-4-ol
(4.1%) and yomogi alcohol (3.8%) as major constituents. Sesquiterpenes (25.0%) were mostly
comprised by oxygenated forms (24.1%) with selin-11-en-4α-ol (18.0%) and caryophyllene oxide
(2.2%). General profile of A. argyi volatiles from Far East Russia was found to be quite different
from that having been reported previously. Xu et al. 2007 [99] reported about 7- ethyl-1,4-dimethylazulene (17.3%), 1,8-cineole (10.3%) and β-limonenol (8.2%) as the main volatile components of the
essential oil from A. argyi. The inflorescence oil of A. argyi collected in China was earlier reported
to contain 1,8-cineole (4.5%), borneol (3.6%), terpineol (10.2%), spathulenol (10.0%), caryophyllene
oxide (6.5%), juniper camphor (8.7%), chamazulene (2.0%), and camphor (3.5%) as major
components [21]. The flowers of A. argyi were found to be rich in attractant substances for
pollination: cylcofenchene, α-pinene, α-myrcene, D-limonene, caryophyllene, and germacrene D
[100]. The composition of leaf oil was reported to be different from oil from flowers with αcubebene, cadinene, bornyl acetate, germacrene D, borneol, D-limonene, α-myrcene and αphellandrene as main constituents [101].
One hundred and nine compounds representing 94.8 % of the oil were characterized in A.
feddei. Monoterpenes (76.5%) with dominance of oxygenated monoterpenes (71.3%) comprised the
most abundance group in the oil with camphor (31.2%), 1,8-cineole (17.6%) and α-thujone (5.7%) as
the major constituents. Sesquiterpenes (14.8%) were also comprised mostly by oxygenated forms with
caryophyllene oxide (4.4%) as the main representative of this class. Comparison with literature data
demonstrated diversity of the oil of A. feddei from Far East Russia. A. feddei oil from China was
reported earlier had significant differences in composition with chamazulene (9.0%), α-terpineol
(8.2%), α-phellandrene (5.8%), α-terpinyl acetate (5.1%), camphor (4.0%) and terpinen-4-ol (3.0%)
[19].
Özek et al., Rec. Nat. Prod. (2014) 8:3 242-261
Essential oil obtained from A. gmelinii, yielded 108 compounds representing 88.4% of the
oil. More than half (61.6%) of the oil was comprised by monoterpenes with oxygenated terpenes
predominating (58.6%). Isopinocamphone (8.9%), 1,8-cineole (6.7%), camphor (5.8%), trans-pmenth-2-en-1-ol (5.3%), cis-p-menth-2-en-1-ol (3.9%) and fragranol (3.8%) were found to be the
main monoterpenes constituents. Sesquiterpenes (25.9%) were dominated by oxygenated forms
which accounted for 18.1% of the oil with longiverbenone (12.0%) as major constituent. A literature
search revealed compositional diversity of terpenoids in A. gmelinii from different localities.
Artemisia ketone (28.2%) and 1,8-cineole (13.0%) were major constituents of the Himalayan
species A. gmelinii (Mathela et al. 1994). A. gmelinii was recently reported to contain α-thujone
(63.2%), germacrene D (2.2-36.5%), vulgarone B (18.9-38.5%), borneol (0.3-8.0%), βcaryophyllene (0.1-9.9%) and selin-11-en-4-α-ol (7.4%) as major volatiles [102]. Moldavian species,
A. gmelinii oil was comprised of α-thujone [103]. A. gmelinii essential oil from Central Asia, yielded
1,8-cineol (21-40%), camphor (10-31%), borneol (4-17%) and terpinen-4-ol (4-8%) [104].
A. manshurica oil was characterized by 52 compounds constituting 83.6% of the oil.
Sesquiterpenes (76.2%) were found in the highest abundance in the oil. Among sesquiterpene
hydrocarbons (36.7%), germacrene D (11.2%) and β-caryophyllene (4.0%) were the major
constituents, while rosifoliol (10.1%), caryophyllene oxide (6.8%) and eudesm-4(15),7-dien-1β- ol
(5.6%) were the primary oxygenated forms (39.5%). Monoterpenes were present in scarce amounts
(3.9%) in the oil.
Seventy eight compounds constituting 77.4% of the A. olgensis oil were detected.
Sesquiterpenes (62.5%) were comprised of mostly oxygenated forms (49.6%) with eudesm4(15),7-dien-1β-ol (6.9%), caryophyllene oxide (5.6%), guaiadien-4β-ol (5.1%), spathulenol (4.9%),
and torilenol (3.8%) as the major constituents. Non-oxygenated sesquiterpene hydrocarbons (12.9%)
were composed of primarily germacrene D (4.2%) and monoterpenes were detected in scarce
amounts (2.8%).
Artemisia oils were evaluated for their antifungal activity against the strawberry anthracnosecausing fungal plant pathogens Colletotrichum acutatum, C. fragariae and C. gloeosporioides using
the direct overlay bioautography assay (Table 4). Anthracnose diseases of strawberry (Fragaria ×
ananassa Duch.) are caused by the fungal pathogens Colletotrichum acutatum, C. fragariae and C.
gloeosporioides [55]. C. fragariae is most often associated with anthracnose crown rot of strawberries
grown in hot, humid areas such as the southeastern United States [55]. Evaluation of the five
Artemisia essential oils in direct bioautography assay was evaluated using two concentrations at 80 µg
and 160 µg applications against three Colletotrichum species. Three Artemisia oils (A. argyi, A. feddei
and A. manshurica) demonstrated clear zones inhibition between 1.75 to 4.0 mm zone inhibitions
which was less active than the commercial fungicide captan. Artemisia olgensis oil did not show
activity whereas A. gmelinii oil demonstrated diffuse inhibitory zones where fewer fungal mycelia
and spores grew on the bioautography plate. Therefore, no further antifungal studies were warranted
on these five Artemisia species.
The five Artemisia essential oils were also evaluated for mosquito biting deterrency against Ae.
aegypti by using the K & D module bioassay system. Based on biting deterrence index (BDI)
values, Artemisia gmelinii showed the highest activity which was near to DEET, commercial standard
(Figure 1). Many species of Artemisia are known to have repellent action against insects and are
used in different parts of the world most often by burning plant parts [105, 106]. Hwang et al.
(1985) [107] isolated compounds from essential oil of A. vulgaris and reported various levels of
repellency in different compounds tested [ 1 0 7 ] . A. argyi, A . feddei, A . manshurica and A.
olgensis oils showed some activity but not significant. O n l y A. gmelinii oil possess the
monoterpenoid fragranol (3.8%) and sesquiterpenoid longiverbenone (12.0%). Therefore, these
compounds may be the source of mosquito biting deterrent activity in A. gmelinii.
253
Chemical diversity and biological activities of five Artemisia species
254
Table 4. Antifungal activity of five Artemisia essential oils using direct bioautography with three
Colletotrichum test species.
Sample
A. argyi
A. feddei
A. gmelinii
A. manshurica
A. olgensis
Benomyl* at 1.16
µg
b
Captan at 1.2 µg
Cyprodinilb at 0.9
µg
Azoxystobinb at
1.61 µg
Mean Fungal Growth Inhibition (mm) ± SEMa
C. acutatum
C. fragariae
C. gloeosporoides
80 µg/spot
160 µg/spot
80 µg/spot
160µg/spot
80µg/spot
160 µg/spot
2.5 ± 0.71
2.0 ± 0.00
diffuse
zones
1.75 ± 0.35
not active
3.5 ± 0.71
2.5 ± 0.71
diffuse
zones
2.0 ± 0.00
not active
2.5 ± 0.71
3.0 ± 0.00
4.0 ± 0.00
3.5 ± 0.71
diffuse zones
diffuse zones
2.0 ± 0.00
not active
2.5 ± 0.71
not active
3.0 ± 0.00
3.0 ± 0.00
diffuse
zones
2.0 ± 0.00
not active
3.5 ± 0.71
3.5 ± 0.71
diffuse
zones
2.5 ± 0.71
not active
d
d
d
11.5 ± 0.71
9.5 ± 0.71
12.0 ± 0.82
d
31.75 ± 2.36
d
d
24.0 ± 0.82
d
a
Mean inhibitory zones and standard deviations (SD) were used to determine the level of antifungal activity against each
fungal species.
b
Technical grade agrochemical fungicides (without formulation) with different modes of action were used as internal
standards.
d
Diffuse zones on the bioautography plate where the fungal growth is visually in interspersed with few mycelia.
Figure 1. Mean values of Biting Deterrence Index (BDI ± standard error) of essential oils from aerial
parts of Artemisia spp. tested against Ae. aegypti females. All oils were tested at the concentration of
10 µg/cm2. Ethanol was solvent control and DEET at 25 nmol/cm2 was used as positive control.
Proportion not biting in DEET ranged between 0.87 to 0.90 whereas ethanol control showed values
between 0.38 – 0.39.
Some Artemisia species have potent larvicidal properties and A. vulgaris oil and extract both
were reported to be toxic to mosquito larvae [105, 108]. In the present study, A. manshurica and
A. olgensis showed mosquito larvicidal activity against Ae. aegypti whereas A. argyi, A. feddei and
A. gmelinii oils did not show any activity at the screening dose of 125 ppm. LD50 values in A.
manshurica and A. olgensis oils were 82.4 (78.0-87.0) ppm and 89.4 (83.6-95.7) ppm and LD90
Özek et al., Rec. Nat. Prod. (2014) 8:3 242-261
values were 122.7 (113.7-162.7) ppm and 139. (125.6-162.7) ppm respectively at 24-h post treatment
(Figure 2). There was no substantial increase in mortality at 48-h post treatment. A. manshurica and
A. olgensis oils were rich in oxygenated sesquiterpenes which may be responsible for the larvicidal
activity.
Figure 2. LD50 and LD90 values (± 95% CI) of Artemisia spp. against 1-d old Ae. aegypti at 24-h post
treatment
The inhibitory effect of the Artemisia essential oils on lipid peroxidation was determined by the
β-carotene/linoleic acid bleaching test. This test simulates the oxidation of the membrane lipid
components in the presence of antioxidants inside the cells. Antioxidant activity of the oils was
determined by measuring the ability of the volatile constituents to inhibit the conjugated diene
hydroperoxide formation from linoleic acid and β-carotene coupled oxidation in an emulsified
aqueous system loses its orange color when reacting with free radicals. The presence of the oil with
antioxidant activity can hinder the extent of β-carotene bleaching by neutralizing the linoleate-free
radical formed in the system. In this test system, A. feddei and A. argyi oils demonstrated
moderate antioxidant activity with 4.1-6.1% of inhibition (Figure 3).
Figure 3. The inhibition percentage of peroxides formation in the presence of Artemisia oils as
compared to BHT by β-carotene/linoleic acid bleaching test (logarithmic diagram).
We also measured the relative capacity of antioxidants to scavenge the ABTS˚+ radical
compared to the antioxidant potency of Trolox (standard). A. argyi and A. gmelinii essential oils
demonstrated moderate antioxidant activity. Highest TEAC values were estimated for A. argyi and
A. gmelinii oils as 1.58 mM and 1.33 mM at 30 min, respectively. A. manshurica demonstrated lowest
activity with TEAC as 0.5 mM. (Figure 4).
255
Chemical diversity and biological activities of five Artemisia species
256
Figure 4. Determination of AOA of Artemisia oils by Trolox equivalent antioxidant capacity
(TEAC) test
Each of the tested oils as well as BHT (standard) reduced DPPH to yellow colored
product and the absorbance at 517 nm declined. Among the tested oils, A. argyi and A. gmelinii
demonstrated noteworthy activity with an IC50 of 8 mg/mL and 13.7 mg/mL, respectively. The oils
of A. feddei, A. manshurica and A. olgensis (40 mg/mL) did not possess such reducing effects
and it was not possible to measure concentrations for a 50% inhibition (Table 5).
Table 5. Antioxidant activity of five Artemisia oils in DPPH test
Free radical
scavenging
activity, µg/mL
DPPH IC50
Aa
Af
Ag
Am
Ao
BHT*
8
>40
13.7
>40
>40
10
* Standard; Aa: A. argyi; Af: A. feddei; Ag: A. gmelinii; Am: A. manshurica; Ao: A. olgensis.
In conclusion, the present work was a study into chemistry and biological activity of five
Artemisia species from Far East Russia. Artemisia oils have unique chemical composition with their
high contents of oxygenated mono- and sesquiterpenes. Five tested Artemisia oils demonstrated
moderate antioxidant and antifungal activity, whereas three Artemisia species showed promising
mosquito activity against the yellow fever mosquito Aedes aegypti. A. gmelinii oil offers potential
for biting deterrent activity and further studies need to be focused on the active chemistry in the
biting deterrent activity. A. manshurica and A. olgensis oils showed higher larvicidal activity and may
be useful in the search for new natural mosquito larvicidal compounds. These results could be useful
in the discovery for new natural mosquito repellent and larvicidal compounds. Bio-insecticides may
be also effective, selective, bio-degradable and associated with little or no-resistance of the pest and
less toxic to the environment.
Acknowledgments
This study was supported by a grant from the Deployed War-Fighter protection (DWFP)
Research Program and the U.S. Department of Defense through the Armed Forces Pest Management
Board (AFPMB) and USDA, ARS grant No. 56-6402-1-612. We thank Ms. J. L. Robertson and Ms.
R. Pace for the antifungal bioassays and thank to Dr. James J. Becnel, Mosquito and Fly Research
Unit, Center for Medical, Agricultural and Veterinary Entomology, USDA-ARS, Gainesville, for
supplying Ae. aegypti eggs.
Özek et al., Rec. Nat. Prod. (2014) 8:3 242-261
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