Selective nematocidal effects of essential oils from two cultivated Artemisia absinthium populations
-
Juan José García-Rodríguez
,
María-Fé Andrés
Abstract
Essential oils (EOs) obtained from two crops and populations of thujone-free cultivated Artemisia absinthium were tested against two nematode models, the mammalian parasite Trichinella spiralis, and the plant parasitic root knot nematode Meloidogyne javanica. The EOs were characterized by the presence of (Z)-epoxyocimene and chrysanthenol as major components and showed time and population dependent quantitative and qualitative variations in composition. The EOs showed a strong ex vivo activity against the L1 larvae of the nematode Trichinella spiralis with a reduction of infectivity between 72 and 100% at a dose range of 0.5–1 mg/ml in absence of cytotoxicity against mammalian cells. Moreover, the in vivo activity of the EO against T. spiralis showed a 66% reduction of intestinal adults. However, these oils were not effective against M. javanica.
1 Introduction
Parasitic nematodes that infect humans, animals, and plants cause serious diseases that are deleterious to human health and agricultural productivity. Chemical and biological control methods have reduced the impact of these parasites. However, development of resistance to nematocidal and anthelmintic agents and the increasing reduction in chemical control due to new regulations pose significant obstacles for ongoing effective parasite control.
In this context, animal parasitic nematodes [1–5] and plant parasitic nematodes [6–9] have been increasingly targeted by studies on the effects of essential oils. However, most research on parasitic nematodes has been done either on animals or in plants because of the inherent differences in host species [10].
The species Trichinella spiralis is responsible for the disease trichinellosis with an extensive geographical distribution as well as a wide range of hosts [11]. The estimated global prevalence of trichinellosis is 11 million people [12], while an increased prevalence and incidence in animal cases has been detected in eastern European countries [13]. Benzimidazoles are broad spectrum drugs used to treat trichinellosis; however these compounds have low bioavailability [14], and resistance against them has been reported in various target nematodes [15].
Root-knot nematodes (RKNs) belong to the genus Meloidogyne and constitute a large group of ubiquitous plant parasites. The four major species (M. incognita, M. javanica, M. arenaria and the temperate species M. hapla), and a few emerging ones are generally considered responsible for the vast majority of crop damage, with a global estimate of multibillion dollar annual losses on a worldwide scale [16]. Root-knot nematodes are very difficult to manage because of their wide host range and high rate of reproduction. Because many of the most effective chemicals used for controlling Meloidogyne sp. are highly toxic and are being gradually phased out by European Union (EU) environmental restrictions, it has become necessary to develop new control techniques based upon alternative substances safer for people and the environment. Thus, in the last few years much effort has focused on the study of the nematocidal activity of plant essential oils (EOs) and their constituents as potential sources of commercial products for management of RKNs [6].
Artemisia species have traditionally been used as anthelmintics [17] and different extracts and components (such as artemisinin from A. annua) have been reported as plant [18] and animal [3, 19] nematocidal agents. Artemisia absinthium L. (wormwood) is an aromatic and medicinal plant of ethnopharmacological interest [20] with reported antihelminthic effects [21]. The composition and biological effects of A. absinthium EO has been widely studied and found to have antimicrobial [22–24], antiprotozoal, and insect antifeedant effects [25, 26].
The composition of A. absinthium EO can vary depending on the plant origin [24]. One common component of A. absinthium EO is thujone, a GABA receptor antagonist [27], which is potentially toxic. Thujone-free Spanish populations of wormwood have been experimentally cultivated and the biological effects (insect antifeedant, antifungal, antioxidant, antiparasitic) and chemical composition of their different extracts (EO, organic, CO2-supercritical) have been evaluated [25, 28, 29]. Based on these results, a long-term field cultivation of selected A. absinthium germplasm has been established for its domestication and valorization [30].
In this work we have tested the in vitro and in vivo nematocidal activity of EOs from two populations and crops of cultivated A. absinthium with different domestication levels against two parasitic nematode models, the animal parasite Trichinella spiralis and the RKN Meloidogyne javanica.
2 Materials and methods
2.1 Plant material and cultivation
The plants for field cultivation were obtained from seeds of two populations (Teruel, T1 and Sierra Nevada, SN0) and planted in 2008 to produce the domesticated populations T2 and SN1 [30]. The experimental field is located in Ejea de los Caballeros, Zaragoza, Spain. A detailed description of the field and the cultivation parameters has been reported [28]. Flowering plants were harvested yearly and processed for EO extraction. The EOs studied here corresponded to crops collected in 2009 and 2010 (T2-09, T2-10, SN1-09, SN1-10).
2.2 Essential oil extraction and analysis
Plant material was distilled in an industrial stainless steel vapor pressure extraction as previously described [30]. The extracted EOs (0.135–0.172% and 0.101–0.114% yield, plant fresh weight, for T-SN populations and year) were analyzed by GC-MS using an Agilent 6890N gas chromatograph (Agilent Technologies, Palo Alto, CA, USA) coupled to an Agilent 5973N mass detector (electron ionization, 70 eV) (Agilent) and equipped with a 25 m×0.20 mm i.d. capillary column (0.2 μm film thickness) HP-1 (methyl silicone bonded) (Hewlett-Packard, Palo Alto, CA, USA). Working conditions were as follows: split ratio (20:1), injector temperature, 260 °C; temperature of the transfer line connected to the mass spectrometer, 280 °C; initial column temperature 70 °C, then heated to 270 °C at 4 °C min–1. Electron ionization mass spectra and retention data were used to assess the identity of compounds by comparing them with those of standards or found in the Wiley Mass Spectral Database (2001). Quantitative data were obtained from the TIC peak areas without the use of response factors.
2.3 Parasites
Trichinella spiralis MFEL/ES/S2 GM-1-ISS48 isolate (Trichinellosis Reference Center, Istituto Superiore di Sanitá, Roma, Italy) was used for ex vivo and in vivo assays. The parasites were maintained in the laboratory by periodical passage in outbred Swiss-CD-1 mice. The methods used for infection and muscle larvae and intestinal adult worm recovery have been previously described [31].
A field-selected M. javanica population from Barcelona (Spain) was maintained on Solanum lycopersicum L. plants (var. Marmande) in pot cultures at 25±1 °C, >70% relative humidity. Egg masses of M. javanica were handpicked from infected tomato roots 2 months after inoculation of the seedlings. Second-stage juveniles (J2) were obtained by incubating egg masses in a water suspension at 25 °C for 24 h.
2.4 Nematocidal effects
2.4.1 Ex vivo assays on T. spiralis:
The larvicidal activity was evaluated by measuring the infective capacity of the ex vivo-treated larvae. As a control, untreated larvae were also included in all assays. Larvae of T. spiralis suspended in HBSS medium were seeded in 24 well plates, (300±50/well) and incubated at 37 °C and 5% CO2 with the A. absinthium EOs at different concentrations (serial double dilutions from 1 to 0.03 mg/ml). After 24 h, the larvae from each well were collected and orally administered to the corresponding mice (6 per dosage). After 7 days, the infected animals were sacrificed by anesthesia and the adult worms present in the intestinal mucosa counted under an stereomicroscope. The experiment was repeated twice.
2.4.2 In vivo assays on T. spiralis:
Groups of 10 mice maintained in a temperature and light/dark controlled environment with water and food ad libitum were used for each experiment. All animal husbandry and experimental conditions were carried out according to the Directive 2010/63/EU of the European Parliament and the Council of the European Union and controlled in Spain by Royal Decree 53/2013 of 1 February, on the care and use of laboratory animals. Eight groups of male mice (6–8 weeks) were orally infected with 300±50 L1 larvae. Twenty-four hours later, the mice were treated with the oils at 50, 100, 150, 200, 250 and 500 mg/kg body weight (BW). Three additional groups were included as controls for infection, placebo, and treatment (albendazole 5 mg/kg BW dissolved in hydroxypropyl-β-cyclodextrin). Seven days after infection, the mice were sacrificed, their small intestine removed, opened lengthwise, and incubated in saline solution during 3 h at 37 °C to obtain adult worms from the mucosa. Worm counting was performed under a binocular lens, and the experiment was repeated twice.
2.4.3 In vitro assays on M. javanica:
Essential oil solutions in dimethyl sulfoxide (DMSO) with 0.6% Tween 20 (20 μg/μl), were placed (5 μl) in each well of 96-well plates to give a final concentration of 1 mg/ml. An inoculum of 100–150 J2 in 95 μl of water was added to each microwell and incubated at 25 °C. Percentages of dead J2 were recorded after 72 h. All treatments were replicated four times [6]. The data are presented as J2 mortality corrected according to Schneider–Orelli’s formula [32].
2.5 Cytotoxicity
J774 murine macrophages were seeded (70,000 cells/well) in flat-bottom 96-well microplates (Costar, NY, USA) with 100 μl of RPMI 1640 (Sigma-Aldrich) supplemented with 10% of fetal bovine serum and antibiotics. The cells were attached to the flat-bottom plates for 24 h at 37 °C and 5% CO2 atmosphere and then 100 μl of the oil diluted in the macrophage medium at the same concentrations as described for the in vitro assays were added to the wells. After 24 h, 20 μl of 1 mM resazurin were added to the plates and the cultures incubated for 3 h. The reduction of the redox dye was measured in a plate fluorometer at 535 nm and 590 nm of excitation and emission wavelengths, respectively (Infinite 200, TECAN, Männedorf, Switzerland).
2.6 Statistical analysis
Statistical analysis was performed using the SPSS v.20 (IBM, Armonk, NY, USA) software. The results of the T. spiralis assays were expressed as mean±standard error. The 50% inhibitory infectivity (II50) were determined by Probit analysis. The nematocidal in vivo results were statistically analyzed by using the non-parametric test (Kruskal–Wallis test), and by the Mann–Whitney U-test.
3 Results and discussion
3.1 Composition of the essential oils
Table 1 shows the composition of the EOs. (Z)-Epoxyocimene was the major component of all the EOs analyzed (26–43%), followed by chrysanthenol (13–30%). Linalool was also present in all samples, ranging between 3.4 and 4.3%. Among the sesquiterpenes, (E)-caryophyllene was found in all samples except for SN1-09 (2.5–5.4%). (5Z)-2,6-dimethylocta-5,7-diene-2,3-diol was found in T2-10 in relatively large amounts (20.2%), ranging between 1.9 and 1.7% for the other samples. An unknown compound of [M]+152 was also present in all samples (0.5–2%). None of the EOs analyzed contained thujone.
Composition of A. absinthium EOs from two cultivated populations (T2 and SN1) collected in 2009 and 2010.
| Compound | Abundance (% of total) | |||
|---|---|---|---|---|
| T2 | SN1 | |||
| 2009 | 2010 | 2009 | 2010 | |
| α-Pinene | 2.70 | 1.62 | ||
| Camphene | 1.07 | |||
| β-Myrcene | 0.68 | 1.15 | 1.13 | |
| β-Ocimene | 1.54 | 1.27 | ||
| 1,8-Cineole | 2.43 | |||
| Linalool | 4.28 | 3.42 | 3.49 | 3.54 |
| [M]+152 (81 68-79-41-53) | 1.25 | 0.54 | 1.94 | 0.49 |
| (Z)Epoxyocimene | 38.92 | 25.89 | 42.72 | 38.77 |
| (E)-Epoxyocimene | 7.74 | 0.99 | 2.45 | 2.16 |
| Chrysanthenol | 12.71 | 30.32 | 23.48 | 22.49 |
| (E)-3-Hexenyl butyrate | 1.26 | 1.34 | 1.30 | 1.64 |
| Chrysanthenyl acetate | 7.35 | 0.71 | 0.46 | |
| (5Z)-2,6-Dimethylocta-5,7-diene-2,3-diol | 1.72 | 20.21 | 1.72 | 1.90 |
| β-Elemene | 0.98 | 1.46 | 2.57 | |
| (E)-Caryophyllene | 4.20 | 2.47 | 5.43 | |
| Germacrene D | 1.36 | 1.15 | 5.99 | 1.86 |
| Sesquiterpene alcohol | 0.51 | 1.79 | 0.74 | |
| 7-Ethyl-1,4-dimethylazulene | 1.09 | 0.87 | ||
Chemical variations have been described for A. absinthium EOs from plants cultivated in vitro, in the greenhouse, and in the field [26]. Variable concentrations of these compounds were also found in EOs and supercritical extracts of the cultivated Spanish A. absinthium populations from which the plants used here originated [26] and have already been described in the EOs of wild populations [33, 34].
Two chemotypes have been described from the Iberian Peninsula: the (Z)-epoxyocimene type (with more than 50% of this compound) which was predominant in all populations, and a (Z)-epoxyocimene+chrysanthenyl acetate type (with 25–65% of (Z)-epoxyocimene and 15–50% of chrysanthenyl acetate). Wormwood EOs from other locations had (Z)-chrysanthenol as the main component [33], (Z)-epoxyocimene and β-thujone/ (Z)-chrysanthenyl acetate among other compositions [35]. The EOs of cultivated Spanish wormwood used here contained both the (Z)-epoxyocimene+(Z)-chrysanthenol chemotype.
3.2 Effects on parasitic nematodes (T. spiralis and M. javanica)
Table 2 shows the ex vivo activity obtained for the different EO concentrations tested against T. spiralis. A linear correlation between oil concentration and adult nematodes recovered from the intestinal mucosa was observed. All the EOs showed a high nematocidal activity (II50 values of 206 and 205 μg/ml for SN1 and 291 and 265 μg/ml for T2, respectively). The small variation observed in the nematocidal effects of the EOs correlated with their limited variation in composition.
Ex vivo activity of different A. absinthium EOs (T2 and SN1 populations, 2009 and 2010 harvest) against T. spiralis L1 muscle larvae.
| EO (mg/ml) | T2-09 | T2-10 | SN1-09 | SN1-10 | ||||
|---|---|---|---|---|---|---|---|---|
| AW | LRa%a | AW | LRa% | AW | LRa% | AW | LRa% | |
| 0.03 | 97.13±9.96 | 13.18 | 100.99±7.4 | 9.83 | 81.63±7.87 | 27.04 | 81.23±6.37 | 27.37 |
| 0.06 | 90.88±6.38 | 18.77 | 80.13±7.72 | 28.38 | 74.38±6.65 | 33.52 | 76.38±8.96 | 31.73 |
| 0.12 | 71.00±11.48 | 36.54 | 60.50±4.87 | 45.92 | 67.75±8.31 | 39.44 | 65.00±7.88 | 41.90 |
| 0.25 | 58.88±8.32 | 47.37 | 57.00±6.05 | 49.05 | 46.13±10.08 | 58.77 | 59.00±11.88 | 47.26 |
| 0.50 | 27.13±4.58 | 75.75 | 31.00±6.29 | 72.29 | 18.88±5.84 | 83.13 | 19.13±6.69 | 82.91 |
| 1 | 1.64±0.71 | 98.54 | 0.09±0.36 | 99.92 | 0.73±0.11 | 99.35 | 0.00±0.00 | 100 |
| Control | 111.9±8.35 | |||||||
Results are expressed as mean± standard error (SE) of adult worms (AW) recovered from intestine of mice infected with ex vivo treated larvae (n=12). aLarval reduction rate (p<0.05).
When T2-10 and SN1-10 EOs were tested in vivo, larval reduction values ≥50% were observed (49–66%) at doses between 100 and 500 mg/kg (Table 3) vs. 66% obtained with the reference drug albendazole (5 mg/kg).
In vivo activity of A. absinthium EOs (T2 and SN1 populations, 2009 and 2010 harvest) against intestinal infection by T. spiralis.
| EO | T2-10 | SN1-10 | ||
|---|---|---|---|---|
| Dose (mg/kg BW) | AW | LRa%a | AW | LRa% |
| 50 | 146.20±10.11 | –4.85 | 139.10±9.49 | 0.22 |
| 100 | 71.47±5.12 | 48.74 | 76.90±5.66 | 44.83 |
| 200 | 64.39±4.61 | 53.82 | 65.20±4.33 | 53.26 |
| 250 | 53.50±5.43 | 61.64 | 57.50±4.64 | 58.75 |
| 500 | 47.30±1.98 | 66.07 | 48.60±4.08 | 65.16 |
| Albendazoleb | 47.44±5.62 | 65.97 | ||
| Control | 139.44±5.17 | |||
aLarval reduction rate (p<0.05). bTested at 5 mg/kg.
Aqueous and ethanolic A. absinthium extracts have been shown to reduce the number of Haemonchus contortus adult worms in vitro and the faecal egg output in sheep infected with H. contortus, Trichuris ovis, Chabertia ovina, Bunostomum trigonocephalum and Oesophagostomum columbianum [19]. An ethanolic extract of A. absinthium showed in vitro trematocidal effects against Schistosoma mansoni, Echinostoma caproni, and Fasciola hepatica [36]. Furthermore, methanolic extracts of Artemisia, including A. absinthium, inhibited trichinellosis in rats [37]. However, this is the first report on trichinellosis inhibition by A. absinthium EO. None of the main components of the oils described here have been previously reported as nematocidals.
The oils were not cytotoxic to macrophage cells (growth inhibition <20%) at the highest concentration tested (200 μg/ml; data not shown). Therefore, (Z)-epoxyocimene+(Z)-chrysanthenol chemotype A. absinthium EOs might be considered for further development as anthelmintic agents.
In contrast, the A. absinthium EOs tested here were not nematocidal against the plant parasitic nematode M. javanica (Table 4). Previous reports have shown that aqueous extracts of A. absinthium roots and aerial parts inhibited M. incognita hatching and caused J2 mortality [38]. However, A. absinthium EOs tested against the pine wood nematode B. xylophilus [39] and the stem nematode D. dipsaci [40] also gave negative results.
Effects of A. absinthium EOs (1 μg/ml) on mortality of second stage juveniles (J2) of Meloidogyne javanica.
| EO | J2 mortality (%)a at 72 h |
|---|---|
| T2-09 | 5.44±1.83 |
| T2-10 | 11.56±2.57 |
| SN1-09 | 8.51±1.72 |
| SN1-10 | 8.09±0.43 |
aMean and standard error values corrected according to Schneider–Orelli’s formula.
Plant and animal endoparasitic nematodes have some similarities in their adapted structures to parasitism such as the cuticle [41]. Products secreted from the cuticle of animal parasitic nematodes share cross-reactive epitopes with those of plant parasitic nematodes [42]. Specifically, cross-reactive cuticle protein epitopes were identified in T. spiralis and M. incognita [43, 44]. However, A. absinthium EOs were highly effective against animal (T. spiralis), but not plant parasitic nematodes (M. javanica). This difference could be related to their lack of close phylogenetic relationship [45] and their different host-parasite interactions [10]. Trichinella spiralis L1 larvae induce the nurse cell [46] within the vertebrate striated skeletal muscles to feed and protect the parasite from host attack. Meloidogyne javanica J2 induce giant cells in the roots of the parasitized plants [47]. Furthermore, parasites have coevolved with their hosts towards compatible life histories, and therefore M. javanica is possibly more tolerant to plant products than T. spiralis.
4 Conclusion
The EOs of cultivated Spanish wormwood with a (Z)-epoxyocimene+(Z)-chrysanthenol chemotype showed a high nematocidal activity against T. spiralis without being cytotoxic to macrophage cells, while they were not active against the plant parasitic nematode M. javanica. The reason for this contrasting effect could be related to the partial tolerance of root knot nematodes to some plant derived compounds. The (Z)-epoxyocimene+(Z)-chrysanthenol chemotype EOs from cultivated A. absinthium may be considered potential candidates for the development of new drugs against helminth parasites of man and domestic animals.
Acknowledgments
This work has been partially funded by grant CTQ2012-38219-C03-01. L.F Julio acknowledges a JAE-CSIC predoctoral fellowship.
References
1. Giarratana F, Muscolino C, Beninati C, Giuffrida A, Panebianco A. Activity of Thymus vulgaris essential oil against Anisakis larvae. Exp Parasitol 2014;142:7–10.10.1016/j.exppara.2014.03.028Search in Google Scholar PubMed
2. De Aquino Mesquita ME, Silva Junior JB, Pannasol AM, de Oliveira EF, Vasconcelos OL, de Paula HC, et al. Anthelmintic activity of Eucalyptus staigeriana encapsulated oil on sheep gastrointestinal nematodes. Parasitol Res 2013;112: 3161–5.10.1007/s00436-013-3492-2Search in Google Scholar PubMed
3. Zhu L, Dai J, Yang L, Qiu J. Anthelmintic activity of Arisaema franchetianum and Ariasema lobatum essential oils against Haemonchus contortus. J Ethnopharmacol 2013;148:311–6.10.1016/j.jep.2013.04.034Search in Google Scholar PubMed
4. Macedo IT, Bevilaqua CM, de Oliveira AL, Camurça-Vasconcelos AL, Vieira Ld, Oliveira FR, et al. Anthelmintic effect of Eucalyptus staigeriana essential oil against goat gastrointestinal nematodes. Vet Parasitol 2010;173:93–8.10.1016/j.vetpar.2010.06.004Search in Google Scholar PubMed
5. Macedo IT, de Oliveira LM, Camurça-Vasconcelos AL, Ribeiro WL, dos Santos JM, de Morais SM, et al. In vitro effects of Coriandrum sativum, Tagetes minuta, Alpinia zerumbet and Lantana camara essential oil on Haemonchus contortus. Rev Bras Parasitol Vet 2013;22:463–9.10.1590/S1984-29612013000400004Search in Google Scholar PubMed
6. Andrés MF, González-Coloma A, Sanz J, Burillo J, Sainz P. Nematicidal activity of essential oils: a review. Phytochem Rev 2012;11:371–90.10.1007/s11101-012-9263-3Search in Google Scholar
7. Bai PH, Bai CQ, Liu QZ, Du SS, Liu SL. Nematocidal activity of the essential oil of Rhododendron anthopogonoides aerial parts and its constituent compound against Meloidogyne incognita. Z Naturforsch C 2013;68:307–12.10.1515/znc-2013-7-808Search in Google Scholar
8. Li W, Sun YN, Yan XT, Yang SY, Lee SJ, Byun HJ, et al. Isolation of nematocidal triterpenoid saponins from Pulsatilla koreana root and their activities against Meloidogyne incognita. Molecules 2013;18:5306–16.10.3390/molecules18055306Search in Google Scholar PubMed PubMed Central
9. Mattei D, Dias-Arieira CR, Biela F, Roldi M, da Silva TR, Rampim L, et al. Essential oil of Rosmarinus officinalis in the control of Meloidogyne javanica and Pratylenchus brachyurus in soybean. Biosci J 2014;30:469–76.Search in Google Scholar
10. Jasmer DP, Goverse A, Geert Smant G. Parasitic nematode interactions with mammals and plants. Annu Rev Phytopathol 2003;41:245–70.10.1146/annurev.phyto.41.052102.104023Search in Google Scholar PubMed
11. Pozio E. The broad spectrum of Trichinella hosts: from cold-to warm-blooded animals. Vet Parasitol 2005;132:3–11.10.1016/j.vetpar.2005.05.024Search in Google Scholar PubMed
12. Dupouy-Camet J. Trichinellosis: a worldwide zoonosis. Vet Parasitol 2000;93:191–200.10.1016/S0304-4017(00)00341-1Search in Google Scholar
13. Gottstein B, Pozio E, Nockler K. Epidemiology, diagnosis, treatment, and control of trichinellosis. Clin Microbiol Rev 2009;22:127–45.10.1128/CMR.00026-08Search in Google Scholar
14. García JJ, Bolas F, Torrado JJ. Bioavailability and efficacy characteristics of two different oral liquid formulations of albendazole. Int J Pharm 2003;250:351–8.10.1016/S0378-5173(02)00559-8Search in Google Scholar
15. Prichard RK. Markers for benzimidazole resistance in human parasitic nematodes? Parasitology 2007;134:1087–92.10.1017/S003118200700008XSearch in Google Scholar PubMed
16. Castagnone-Sereno P, Danchin EG, Perfus-Barbeoch L, Abad P. Diversity and evolution of root-knot nematodes, Genus Meloidogyne: new insights from the genomic era. Annu Rev Phytopathol 2013;51:203–20.10.1146/annurev-phyto-082712-102300Search in Google Scholar PubMed
17. Ramasubramaniaraja R, Niranjan Babu M. Antihelminthic studies and medicinal herbs – an overview. Int J Pharm Sci Rev Res 2010;5:39–47.Search in Google Scholar
18. D’Addabbo T, Pinarosa Avato T, Carbonara T, Argentieri MP, Radicci V, Leonetti P, et al. Nematocidal potential of Artemisia annua and its main metabolites. Eur J Plant Pathol 2013;137:295–304.10.1007/s10658-013-0240-5Search in Google Scholar
19. Squires JM, Ferreira JF, Lindsay DS, Zajac AM. Effects of artemisinin and Artemisia extracts on Haemonchus contortus in gerbils (Meriones unguiculatus). Vet Parasitol 2011;175: 103–8.10.1016/j.vetpar.2010.09.011Search in Google Scholar PubMed
20. Lachenmeier DW. Wormwood (Artemisia absinthium L.). A curious plant with both neurotoxic and neuroprotective properties? J Ethnopharmacol 2010;131:224–7.10.1016/j.jep.2010.05.062Search in Google Scholar PubMed
21. Tariq KA, Chishti MZ, Ahmad F, Shawl AS. Anthelmintic activity of extracts of Artemisia absinthium against ovine nematodes. Vet Parasitol 2009;160:83–8.10.1016/j.vetpar.2008.10.084Search in Google Scholar PubMed
22. Baykan Erel S, Reznicek G, Şenol SG, Karabay Yavaşogulu NÜ, Konyalioglu S, Zeybek AU. Antimicrobial and antioxidant properties of Artemisia L. species from western Anatolia. Turk J Biol 2012;36:75–84.Search in Google Scholar
23. Gandomi Nasrabadi H, Abbaszadeh S, Tayyar Hashtjin N, Yamrali I. Study of chemical composition of essential oil of afsantine (Artemisia absinthium) and inhibitory effects of the essential oil and its aqueous and alcoholic extracts on some food borne bacterial pathogens. J Med Plants 2012;11:120–7.Search in Google Scholar
24. Juteau F, Jerkovic I, Masotti V, Milos M, Mastelic J, Bessière JM, et al. Composition and antimicrobial activity of the essential oil of Artemisia absinthium from Croatia and France. Planta Med 2003;69:158–61.10.1055/s-2003-37714Search in Google Scholar PubMed
25. Martínez-Díaz R, Ibáñez-Escribano A, Burillo J, de las Heras L, del Prado G, Agulló-Ortuño MT, et al. Trypanocidal and trichomonacidal components of cultivated Artemisia absinthium Linnaeus (Asteraceae) essential oil. Mem Inst Oswaldo Cruz 2015;110:1–7.10.1590/0074-02760140129Search in Google Scholar PubMed PubMed Central
26. Bailén M, Julio LF, Diaz CE, Sanz J, Martínez-Díaz RA, Cabrera R, et al. Chemical composition and biological effects of essential oils from Artemisia absinthium L. cultivated under different environmental conditions. Ind Crop Prod 2013;49:102–7.10.1016/j.indcrop.2013.04.055Search in Google Scholar
27. Olsen RW. Absinthe and gamma-aminobutyric acid receptors. Proc Natl Acad Sci USA 2000;97:4417–8.10.1073/pnas.97.9.4417Search in Google Scholar PubMed PubMed Central
28. Burillo J. Cultivo experimental de ajenjo Artemisia absinthiumL. como potencial insecticida de origen natural. In: Burillo J, González-Coloma A, editors. Insecticidas y Repelentes De Origen Natural. Zaragoza: Centro de Investigación y Tecnología Agroalimentaria, 2009:19.Search in Google Scholar
29. González-Coloma A, Bailén M, Diaz CE, Fraga BM, Martínez-Díaz R, Zuñiga GE, et al. Major components of Spanish cultivated Artemisia absinthium populations: antifeedant, antiparasitic, and antioxidant effects. Ind Crop Prod 2012;37:401–7.10.1016/j.indcrop.2011.12.025Search in Google Scholar
30. Julio LF, Burillo J, Giménez C, Cabrera R, Díaz CE, Sanz J, et al. Chemical and biocidal characterization of two cultivated Artemisia absinthium populations with different domestication levels. Ind Crop Prod 2015;76:787–92.10.1016/j.indcrop.2015.07.041Search in Google Scholar
31. Wakelin D, Lloyd M. Immunity to primary and challenge infections of Trichinella spiralis: a re-examination of conventional parameters. Parasitology 1976;72:173–82.10.1017/S0031182000048472Search in Google Scholar PubMed
32. Santana O, Andres MF, Sanz J, Errahmani N, Abdeslam L, Gonzalez-Coloma A. Valorization of essential oils from Moroccan aromatic plants. Nat Prod Commun 2014;9:1109–14.10.1177/1934578X1400900812Search in Google Scholar
33. Judzentiene A, Budiene J. Compositional variation in essential oils of wild Artemisia absinthium from Lithuania. J Essent Oil Bear Pl 2010;13:275–85.10.1080/0972060X.2010.10643822Search in Google Scholar
34. Kordali S, Kotan R, Mavi A, Cakir A, Ala A, Yildirim A. Determination of the chemical composition and antioxidant activity of the essential oil of Artemisia dracunculus and of the antifungal and antibacterial activities of Turkish Artemisia absinthium, A. dracunculus, Artemisia santonicum, and Artemisia spicigera essential oils. J Agric Food Chem 2005;53:9452–8.10.1021/jf0516538Search in Google Scholar PubMed
35. Blagojevic P, Radulovic N, Palic R, Stojanovic G. Chemical composition of the essential oils of Serbian wild-growing Artemisia absinthium and Artemisia vulgaris. J Agric Food Chem 2006;54:4780–9.10.1021/jf060123oSearch in Google Scholar PubMed
36. Ferreira JF, Peaden P, Keiser J. In vitro trematocidal effects of crude alcoholic extracts of Artemisia annua, A. absinthium, Asimina triloba, and Fumaria officinalis: trematocidal plant alcoholic extracts. Parasitol Res 2011;109:1585–92.10.1007/s00436-011-2418-0Search in Google Scholar PubMed
37. Caner A, Doskaya M, Degirmenci A, Can H, Baykan S, Uner A, et al. Comparison of the effects of Artemisia vulgaris and Artemisia absinthium growing in western Anatolia against trichinellosis (Trichinella spiralis) in rats. Exp Parasitol 2008;119:173–9.10.1016/j.exppara.2008.01.012Search in Google Scholar PubMed
38. Dias CR, Schwan AV, Ezequiel DP, Sarmento MC, Ferraz S. Efeito de extractos aquosos de plantas medicinais na sobrevivencia de juvenis de Meloidogyne incognita. Nematol Bras 2000;24:203–10.Search in Google Scholar
39. Barbosa P, Lima AS, Vieira P, Dias LS, Tinoco MT, Barroso JG. Nematocidal activity of essential oils and volatiles derived from Portuguese aromatic flora against the pinewood nematode, Bursaphelenchus xylophilus. J Nematol 2010;42:8–16.Search in Google Scholar
40. Zouhar M, Douda O, Lhotsky D, Pavela R. Effect of plant essential oils on mortality of the stem nematode (Ditylenchus dipsaci). Plant Prot Sci 2009;45:66–73.10.17221/6/2009-PPSSearch in Google Scholar
41. Davies KG, Curtis RH. Cuticle surface coat of plant-parasitic nematodes. Annu Rev Phytopathol 2011;49:135–56.10.1146/annurev-phyto-121310-111406Search in Google Scholar PubMed
42. López de Mendoza ME, Curtis RH, Gowen SR. Identification and characterization of excreted-secreted products and surface coat antigens of animal and plant-parasitic nematodes. Parasitology 1999;118:397–405.10.1017/S0031182098003941Search in Google Scholar
43. López-Arellano ME. Immunomolocalization of Trichinella spiralis L1 surece and excreted/secreted antigens in situ. Int J Nematol 2002;12:55–8.Search in Google Scholar
44. López de Mendoza ME, Abrantes IM, Rowe J, Curtis RH. Immunolocalisation in plants of secretions form parasitic stages of Meloidogyne incognita and M. hispanica. Int J Nematol 2002;12:149–54.Search in Google Scholar
45. Blaxter M, Dorris M, De Ley P. Patterns and processes in the evolution of animal parasitic nematodes. Nematology 2000;2:243–55.10.1163/156854100508881Search in Google Scholar
46. Despommier DD. Trichinella spiralis and the concept of niche. J Parasitol 1993;79:472–82.10.2307/3283370Search in Google Scholar
47. Abad P, Favery B, Rosso MN, Castagnone-Sereno P. Root-knot nematode parasitism and host response: molecular basis of a sophisticated interaction. Mol Plant Pathol 2003;4:217–24.10.1046/j.1364-3703.2003.00170.xSearch in Google Scholar PubMed
©2015 by De Gruyter
Articles in the same Issue
- Frontmatter
- Chemical characterization, antioxidant and cytotoxic activities of the methanolic extract of Hymenocrater longiflorus grown in Iraq
- Preventive effect of total glycosides from Ligustri Lucidi Fructus against nonalcoholic fatty liver in mice
- Synthesis of platinum(II) complexes of 2-cycloalkyl-substituted benzimidazoles and their cytotoxic effects
- cDNA cloning and functional characterisation of four antimicrobial peptides from Paa spinosa
- Evaluation of the water soluble extractive of astragali radix with different growth patterns using 1H-NMR spectroscopy
- SPME collection and GC-MS analysis of volatiles emitted during the attack of male Polygraphus poligraphus (Coleoptera, Curcolionidae) on Norway spruce
- Selective nematocidal effects of essential oils from two cultivated Artemisia absinthium populations
Articles in the same Issue
- Frontmatter
- Chemical characterization, antioxidant and cytotoxic activities of the methanolic extract of Hymenocrater longiflorus grown in Iraq
- Preventive effect of total glycosides from Ligustri Lucidi Fructus against nonalcoholic fatty liver in mice
- Synthesis of platinum(II) complexes of 2-cycloalkyl-substituted benzimidazoles and their cytotoxic effects
- cDNA cloning and functional characterisation of four antimicrobial peptides from Paa spinosa
- Evaluation of the water soluble extractive of astragali radix with different growth patterns using 1H-NMR spectroscopy
- SPME collection and GC-MS analysis of volatiles emitted during the attack of male Polygraphus poligraphus (Coleoptera, Curcolionidae) on Norway spruce
- Selective nematocidal effects of essential oils from two cultivated Artemisia absinthium populations
