Next Article in Journal
CDK11 Loss Induces Cell Cycle Dysfunction and Death of BRAF and NRAS Melanoma Cells
Next Article in Special Issue
Phenolic Plant Extracts Versus Penicillin G: In Vitro Susceptibility of Staphylococcus aureus Isolated from Bovine Mastitis
Previous Article in Journal
Role of TRPV1 and TRPA1 Ion Channels in Inflammatory Bowel Diseases: Potential Therapeutic Targets?
Previous Article in Special Issue
Curcumin and (−)- Epigallocatechin-3-Gallate Protect Murine MIN6 Pancreatic Beta-Cells against Iron Toxicity and Erastin-Induced Ferroptosis
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:

Chemical Profile and Biological Activities of Essential Oil from Artemisia vulgaris L. Cultivated in Brazil

Sonia Malik
Ludmilla Santos Silva de Mesquita
Carolina Rocha Silva
José Wilson Carvalho de Mesquita
Emmeline de Sá Rocha
Jayakumar Bose
Rambod Abiri
Patricia de Maria Silva Figueiredo
3 and
Livio M. Costa-Júnior
Graduate Program in Health Sciences, Biological and Health Sciences Center, Federal University of Maranhão, São Luís 65085-580, MA, Brazil
Australian Research Council Centre of Excellence in Plant Energy Biology, School of Agriculture, Food and Wine, Waite Research Institute, University of Adelaide, PMB 1, Glen Osmond, SA 5064, Australia
Department of Pharmacy, Biological and Health Sciences Center, Federal University of Maranhão, São Luís 65085-580, MA, Brazil
Department of Pathology, Biological and Health Sciences Center, Federal University of Maranhão, São Luís 65085-580, MA, Brazil
Department of Biochemistry, Faculty of Biotechnology and Biomolecular Sciences, University Putra Malaysia, UPM Serdang 43400, Selangor DE, Malaysia
Young Researchers and Elite Club, Islamic Azad University, Kermanshah, Iran
Author to whom correspondence should be addressed.
Pharmaceuticals 2019, 12(2), 49;
Submission received: 27 February 2019 / Revised: 19 March 2019 / Accepted: 26 March 2019 / Published: 1 April 2019
(This article belongs to the Special Issue Plant Phytochemicals on Drug Development)


Essential oil from the leaves of Artemisia vulgaris L. (Compositae) cultivated in Brazil was investigated for its chemical composition and biological activities including antibacterial, antifungal, and anthelmintic. The constituents of essential oils isolated by hydro-distillation were examined by GC-MS and a total of 18 components were identified. The essential oil was dominated by oxygenated sesquiterpenes (44.4%), sesquiterpene hydrocarbons (33.3%), and oxygenated monoterpenes (16.6%). Caryophyllene (37.45%), germacrene D (16.17%), and humulene (13.66%) were the major components. The essential oils from A. vulgaris showed bactericidal and fungicidal properties against Staphylococcus aureus and Candida albicans, respectively. Anthelmintic activity against Haemonchus contortus was absent in this essential oil. Altogether above results indicate that essential oils from A. vulgaris can be used for various medicinal purposes.

Graphical Abstract

1. Introduction

Increasing resistance and other side effects caused by the repeated use of similar antibiotics or anti-parasitics enforced the researchers to find suitable natural compounds as alternatives. A large number of plant derived compounds play an important role in the natural defence system against all living microorganisms [1]. In vitro investigations of antimicrobial and antifungal activities have been carried out for several medicinal crops including Baccharis trimera [2], Zingiber officinale [3,4], Mikania glomerata [5,6], Mentha piperita [3,7], Syzygium aromaticum [8], Cymbopogon citratus [9,10], Allium sativum [11,12], and Psidium guajava [6,11,13]. There is a huge interest in medicinal crops to extract oils and bioactive compounds to use them as food additives to delay or prevent growth and development of microorganisms [14,15,16,17,18].
The genus Artemisia is among the most widely distributed and largest genera of family Asteraceae, containing around 500 taxa [19,20,21]. Many Artemisia species grow in Northern Africa, North and Central America, and Eurasia [22]. Artemisia vulgaris Linn., commonly known as mugwort, is a rhizomatous perennial medicinal plant [23] and is widely used to treat to dyspepsia, rheumatic pains, fevers, diarrhea, worm infestations, vomiting, constipation, cramps, colic, hysteria, flatulence, menstrual problems, distention, epilepsy, to promote circulation, and as a sedative [24,25,26,27].
Several essential oils of aromatic plant are used for their antispasmodic, carminative, anti-parasitical, anti-inflammatory, antimicrobial, anti-helminthic, and insecticidal properties [22]. Biological activities of these essential oils are mainly attributed to volatile compounds, such as α-pinene, camphor, caryophyllene, camphene, germacrene D, 1,8-cineole, and α-thujone [22]. In this respect, various mugwort genotypes growing in different geographic regions showed varied components fraction. For example, oils from Italian mugwort was rich in camphor alone or together with myrcene, 1,8–cineole, or borneol [28,29]; German mugwort contained sabinene, myrcene, and 1,8-cineole [22]; Indian mugwort was rich in camphor, α-thujone, or thujone isomer [30]; French mugwort was rich in camphor, 1,8-cineole, and terpinen-4-ol [31]; Moroccan mugwort had camphor, isothujone, and thujone as major components [32]; Iranian mugwort dominated with α-pinene, menthol, β-eudesmol, and spathulenol [33], Cuban mugwort was rich in sesquiterpene [34]. However, there is no report on the chemical composition of Brazilian mugwort oils.
Knowing the exact chemical composition of Brazilian mugwort oil is critical to identify its biological properties (e.g., antimicrobial, anti-parasitical, and insecticidal). Among all the pathogens, Staphylococcus aureus [7], Escherichia coli [35], and Candida albicans are of great importance to public health [36]. S. aureus, a Gram-positive and round-shaped bacterium [7] is known to cause skin and severe bloodstream infections in patients using catheters and has also been frequently associated with pneumonias associated with mechanical ventilation [24]. C. albicans is the main etiological agent of candidiasis, the most common pathogen in humans which colonizes the genitourinary tracts, gastrointestinal tracts, teeth, mouth, as well as skin of more than 70% of the healthy population [37,38]. E. coli is a bacterium commonly found in the digestive tract of humans and warm-blooded animals. Some strains of E. coli can cause serious food-borne diseases. Haemonchus contortus, a parasitic gastrointestinal nematode, is a serious threat to small ruminants’ health. Diarrhea, low packed cell volume (PCV), anemia, peripheral, internal fluid accumulation, and dehydration are common signs of this nematode [39]. To ascertain the antimicrobial and anti-parasitical activity of Brazilian mugwort oils, it is necessary to test the efficacy of Brazilian mugwort oils against above pathogens.
Considering aforementioned literature, the main purpose of this study was to assess the chemical composition of essential oil extracted from the leaves of A. vulgaris grown in Brazil, and to identify its biological properties.

2. Material and Methods

2.1. Plant Material and Botanical Identification

Aerial parts (before the onset of flowering) of A. vulgaris were collected from plants growing in botanical garden at the Federal University of Maranhão, Sao Luís, Maranhão, Brazil in August 2016. Plants were identified and authenticated by Dr. Eduardo B. de Almeida Junior. The voucher specimens (number 8.637) were kept at the Herbarium of Federal University of Maranhão, Sao Luis, Brazil.

2.2. Extraction of Essential Oils

To extract the essential oils, leaves of A. vulgaris were dried at 40 °C in an oven with circulating air. These were then sliced into small pieces and subjected to extraction with water by hydro-distillation for 3 h using a Clevenger-type apparatus. The essential oils (1.3 mL) thus obtained was dried over anhydrous sodium sulphate and stored at 4 °C until use.

2.3. Identification of Compounds Using Gas Chromatography-Mass Spectrometry (GC-MS)

The analyses of essential oils were performed using GC-2010 plus gas chromatograph (Shimadzu, Japan) coupled to a GCMS-QP2010 SE mass spectrometry detector (Shimadzu, Japan) and equipped with an AOC20i auto-injector (Shimadzu, Japan). A capillary Rtx-5MS column (30 m × 0.25 mm i.d. × 0.25 µm film thickness, Restek, USA) was used for separation. Helium (at a flow rate of 1.0 mL/min) was used as carrier gas. Temperature was kept at 60 °C for 5 min and programmed to reach 240 °C at the rate of 3 °C per min. The samples were injected at the injected temperature of 250 °C. The injection volume was 1.0 μL in 1:30 split ratio. The mass spectra were obtained with electron impact ionization (70 eV) at full scan mode (40 to 500 m/z), using an ion source at 200 °C.

2.4. Identification of Compounds

The compounds were identified by comparing retention indices (RI) and mass spectra with data from the NIST 11.0 MS library and the literature.

2.5. Microorganisms and Growth Conditions

Staphylococcus aureus ATCC 25923, Escherichia coli ATCC 25922, and Candida albicans ATCC 90028, already maintained in laboratory, were used for the experiments. The strains were pre-cultured for 24 h on brain heart infusion (BHI; Difco, BD, USA) at 37 °C in the presence of 5% CO2.

2.6. Determination of Antimicrobial and Anti-Fungal Activities in Essential Oils

The antimicrobial and anti-fungal activities in essential oils of A. artemisia were determined through MIC, the microdilution technique according to the broth dilution methodology proposed by the Clinical and Laboratory Standards Institute (CLSI, 2013). In short, sterile 96-well plates were prepared with 50 μL of BHI broth and 50 μL of the essential oil followed by serial dilutions (1:2 to 1:128) done in triplicate After dilution, 2 μL of microbial suspension (0.5 on the MacFarland scale) was added to the samples. Then, 25 μL of chloramphenicol (20 μg/mL) was added to the well as positive control and 50 μL of BHI and 2 μL of microbial suspension were used as growth control. The plate was incubated at 35 °C in an incubator for 24 h for bacteria and 48 h for fungus. After the incubation period, 5 μL of the resazurin (0.1% w/v) was added.

2.7. Parasitological Procedures

Eggs and third stage larvae (L3) were obtained from a donor sheep with a monospecific infection of Haemonchus contortus. Experimental procedures were performed in accordance with the guidelines of the Animal Ethics Committee of Maranhão, Federal University and approved under protocol number 23115018061/2011-11.

2.8. Egg Hatching Assay (EHA)

Fresh faeces were collected, and the eggs were recovered using 25 μm sieves. Recovered eggs were added to a saturated NaCl solution and centrifuged (3000 rpm) for 3 min; floating eggs were recovered using a 25 μm sieve [40]. A suspension of 100 eggs/well was placed in a plate and 100 µL of essential oils of A. vulgaris and control (2%, v/v, methanol) was added. The essential oils of A. vulgaris were diluted in 2% (v/v) methanol at concentration of 10 mg/mL. Tests were performed with four replicates. The plate was incubated at 27 °C and RH > 80% for 48 h. Larvae and unhatched eggs were counted under an inverted microscope.

2.9. Larval Exsheathment Inhibition Assay (LEIA)

This test was performed according to Bahuaud et al. [41]. The essential oil of A. vulgaris was diluted in 2% (v/v) methanol and evaluated at concentration 1.2 mg/mL. The negative control was performed with 2% (v/v) methanol and PBS (0.1 M phosphate, 0.05 M NaCl, pH 7.2). The L3 larvae were incubated in the different treatments for 3 h at 22 °C. After incubation, the larvae were washed and centrifuged (3000 rpm) three times with PBS. Approximately 1000 larvae/tube was subjected to the artificial exsheathment process by contact with sodium hypochlorite (2.0%, w/v) and sodium chloride (16.5%, w/v). Tests were performed with four replicates. The percentages of larval exsheathment process were monitored at 0, 20, 40 and 60 min intervals by observing under an inverted microscope.

2.10. Larval Migration Inhibition Assay (LMIA)

The evaluation of larval migration inhibition was performed according to Jackson and Hoste [42]. Initially, H. contortus L3 larvae were subjected to the exsheathment process with 2.0% (w/v) sodium hypochlorite (w/v). After being sieved, the larvae were centrifuged in distilled water for 5 min at 407× g and were re-suspended in distilled water and centrifuged again. Larval suspension (100 μL; approximately 100 larvae) and essential oil of A. vulgaris (1000 μL at 10 mg/mL) were added to microtubes. The suspension was incubated for 2 h at 27 °C and ≥80% RH. After that, the tubes were centrifuged at 1500× g for 10 min and the supernatant was removed, reducing the volume by approximately 300 μL. Using culture plates, 200 μL of the samples at the concentrations described above were added to the wells, and then an apparatus containing 25 μm sieves were submerged in each well. A 50 μL volume of larval suspension was added to the corresponding apparatus and incubated for 2 h at 27 °C and ≥80% RH. Each apparatus was then removed carefully and the mesh was washed. Lugol was added to each well and larvae of each well and filter were counted. The assay was performed in quadruplicate and methanol (2%, v/v) was used as a negative control.

3. Results and Discussion

3.1. Chemical Composition of Essential Oil Extracted from Brazilian A. vulgaris Leaves

The essential oil extracted (0.5%, v/v) from the leaves of Brazilian A. vulgaris was analyzed by GC-MS chromatography (Table 1). The obtained results indicated the presence of 18 chemical compounds in the chromatogram, constituting 100% of the total components detected. The highest compositions of the compounds were 37.45% of caryophyllene, followed by germacrene-D (16.17%) and humulene with 13.66%.
Caryophyllene (β-caryophyllene) [43] is a natural bicyclic sesquiterpene usually found in various essential oils including clove, rosemary, and Cannabis [44,45]). This compound is commonly found mixed with α-humulene and isocaryophyllene in essential oils [43]. Caryophyllene is mainly used as a flavoring or fragrance enhancer in spice blends, citrus flavors, chewing gums, soap, detergents, creams or lotions, food products, and beverages. It is known to possess anaesthetic and anti-inflammatory activities [43]. Rasmann and colleagues [46] reported that sesquiterpene olefin (E)-b-caryophyllene plays an essential role in different separate pathways of induced defenses response against herbivores. Caryophyllene can act as antimicrobial agent in defense mechanisms against pathogens [47] such as Pseudomonas aeruginosa and Bacillus subtilis [48]. Caryophyllene is also reported to have allelopathic potential and shown to inhibit the seedlings development of various plant species [49,50].
Germacrenes, a group of volatile organic hydrocarbon compounds (particularly sesquiterpenes), produced in various plant species are known to act as insecticidal, antimicrobial, and insect pheromones [51,52]. This volatile organic compound has been observed in bryophytes, gymnosperms and angiosperms. Interestingly, germacrene D plays an important role as a precursor in sesquiterpenes synthesis such as selinenes and cadinenes [53,54]. Reportedly, germacrene D as predominant components has been found in the leaves of five plants extracts viz. Bursera fagaroides, B. mirandae, B. exselsa, B. copallifera, and B. ruticola [55]. Humulene, also known as α- humulene or α-caryophyllene is a naturally occurring monocyclic sesquiterpene characteristic of Humulus lupulus [56]. It is also found in Abies balsamea, Salvia officinalis, Comptonia peregrine, Cordia verbenacea, and Myrica gale [57,58,59]. Generally terpenes play a role in plants as an anti-herbivore defenses mechanism [60]. Lutz et al. determined the chemical profile of essential oils obtained from seven species of Artemisia grown in Canada and studied their antimicrobial and antioxidant activities [61].
Interestingly, monoterpenes hydrocarbons were not found in the essential oil in the present investigation, whereas one diterpene (phytol, 2.94%) was detected. Diterpenes are rare in essential oils and the presence of phytol can be considered as a standard for this species oil. According to Hussein et al. [19], the essential oil from aerial part of mugwort extracted in Egypt contained camphor and 3,5-dimethylcyclohexene as the major components (both with 13.83%), followed by germacrene-D and α-cubenene with 10.44%. However, they found phytol acetate instead of phytol, which were detected in the present work. In contrast to present findings, the monoterpene fraction dominated in the mugwort oils from European countries.

3.2. Anti-Microbial Activities Identification

The antimicrobial activity of essential oil of A. vulgaris was obtained (Table 2) from microdilution in BHI broth and expressed as Minimum Inhibitory Concentration (MIC), Minimum Bactericidal Concentration (MBC), and Minimum Fungicidal Concentration (MCF). The MIC of essential oil of A. vulgaris leaves in Escherichia coli ATCC 25922, Staphylococcus aureus (ATCC 25923), and Candida albicans ATCC 90028 were found at the 1:64, 1:16, and 1:32 dilution titre, respectively. MIC is considered as the lowest concentrations for recognizing the susceptibility of microorganisms to antimicrobial and is applied to judge the performance of all other methods of susceptibility testing. The minimum bactericidal concentration (MBC) affected by extracted essential oil of A. vulgaris leaves were reported in E. coli at the 1:8 dilution titre. MBC as the lowest concentration act as an antibacterial agent required to kill a microorganism. It could be identified from MIC experiments by sub-culturing to agar plates media that do not contain the test agent. MFC values for C. albicans were 1:8 dilution titre. The results revealed variable inhibition activity against E. coli, S. aureus, and C. albicans. The antimicrobial activity was evident with the increase in concentration of essential oil extracted from leaves of A. vulgaris. Reportedly, the essential oil of A. vulgaris presented lowest bactericidal potential for E. coli. The essential oil of A. vulgaris showed bactericidal activity for S. aureus and fungicide for C. albicans in the same concentration [24].

3.3. Anthelmintic Activity

The A. vulgaris essential oil was tested in high concentrations (10 mg/mL) against eggs (Egg hatching assay) and on two different larval behavior (10 mg/mL and 1.2 mg/mL in LMIA) of main gastrointestinal nematode from small ruminant H. contortus. The efficacy of A. vulgaris essential oil was low in inhibition of eggs hatch (7.4 ± 6.5%), either in larval exsheathment (4.1 ± 12.8%) and larval migration (1.9 ± 4.1 %). Extracts of several species of Artemisia were described as antihelmintic effect against H. contortus [62,63,64] and extract of A. vulgaris was efficient in vivo models against Trichinella spiralis [65]. However, few studies were performed using essential oils of Artemisia species against nematodes [66,67]. To our knowledge, this is the first report of A. vulgaris essential oil to test against nematode. Besides the efficacy of extracts of A. vulgaris on T. spiralis [65], the essential oil was not effective against eggs hatch (7.4 ± 6.5%), larval exsheathment (4.1 ± 12.8%), and larval migration (1.9 ± 4.1%). Essential oils of plants with (E)-caryophyllene and β-caryophyllene as main compound showed activity against eggs and adult of Schistosoma mansoni and inhibited larval migration of Strongyloides ratti, respectively [68,69,70]. β-Caryophyllene was effective for in vitro inhibition of the enzyme Glutathione S-transferase (GST), an important enzyme of detoxification in nematodes [71], however, the data are contradictory, with no efficacy of β-caryophyllene against a root-knot nematode, Meloidogyne incognita [72].

4. Conclusions

The essential oil from A. vulgaris cultivated in Brazil is a potential alternative source of caryophyllene, germacrene D, and humulene. The volatile compounds from this plant species possess antifungal and anti-bacterial properties. Hence, there is a potential for using this essential oil from A. vulgaris as disinfectants and preservatives against microorganisms. More studies are required to be focused on isolating the compounds from essential oils and to investigate their biological activities and mode of action in order to use these volatile compounds at commercial level.

Author Contributions

S.M. was responsible for the general layout of experiments, discussion, manuscript writing, editing as well as overall guidance. L.S.S.d.M. and J.W.C.d.M. executed the experiments related to GC/MS and helped in writing and revising the manuscript. R.A. and J.B. assisted in drafting late versions of the manuscript. C.R.S. and E.d.S.R. performed experiments to assess the biological activities and abetted in manuscript writing. P.d.M.S.F. and L.M.C.-J. helped analyzing the data and participated in drafting of the text.


This research was funded by Fundação de Amparo à Pesquisa e Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA), Brazil (grant number 10/2015; BEPP-01300/15).


S.M., L.S.S.d.M., J.W.C.d.M., C.R.S., E.d.S.R, P.d.M.S.F. and L.M.C.-J. would like to acknowledge Fundação de Amparo à Pesquisa e Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA), São Luis, Maranhão for financial support. Authors would like to acknowledge Maria Nilce de Sousa Ribeiro, Department of Pharmacy, Federal University of Maranhão for providing lab facilities.

Conflicts of Interest

The authors declare no conflict of interest.


  1. Rauha, J.P.P.; Remes, S.; Heinonen, M.; Hopia, A.; Kähkönen, M.; Kujala, T.; Kahkonen, M. Antimicrobial effects of Finnish plant extracts containing flavoniods and other phenolic compounds. Int. J. Food Microbiol. 2000, 56, 3–12. [Google Scholar] [CrossRef]
  2. Avancini, C.A.M.; Wiest, J.M.; Mundstock, E. Atividade bacteriostática e bactericida do decocto de Baccharis trimera (Less.) D.C., Compositae, carqueja, como desinfetante ou anti-séptico. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 2000, 52, 230–234. [Google Scholar] [CrossRef]
  3. Júnior, A.A.S.; Vizzotto, V.J.; Giorgi, E.; Macedo, S.G.; Marques, L.F. Plantas Medicinais, Caracterizacao E Cultivo; Epagri: Florianópolis, SC, Brazil, 1994. [Google Scholar]
  4. Konning, G.H.; Agyare, C.; Ennison, B. Antimicrobial activity of some medicinal plants from Ghana. Fitoterapia 2004, 75, 65–67. [Google Scholar] [CrossRef] [PubMed]
  5. Boyayan, M. Oguaco, planta nativa da mata Atlântica, tem mais propriedades terapêuticas do que se supunha. Revista Pesquisa Fapesp 2002, 74, 48–49. [Google Scholar]
  6. Holetz, F.B.; Pessini, G.L.; Sanches, N.R.; Cortez, D.A.G.; Nakamura, C.V.; Dias Filho, B.P. Screening of some plants used in the Brazilian folk medicine for the treatment of infectious diseases. Mem. Inst. Oswaldo Cruz. 2002, 97, 1027–1031. [Google Scholar] [CrossRef] [Green Version]
  7. Tassou, C.; Koutsoumanis, K.; Nychas, G.J.E. Inhibition of Salmonella enteritidis and Staphylococcus aureus in nutrient broth by mint essential oil. Food Res. Int. 2000, 33, 273–280. [Google Scholar] [CrossRef]
  8. López, P.; Sánchez, C.; Batlle, R.; Nerín, C. Solid- and vapor-phase antimicrobial activities of six essential oils:  Susceptibility of selected foodborne bacterial and fungal strains. J. Agric. Food Chem. 2005, 53, 6939–6946. [Google Scholar] [CrossRef] [PubMed]
  9. Cimanga, K.; Kambu, K.; Tona, L.; Apers, S.; De Bruyne, T.; Hermans, N.; Vlietinck, A.J. Correlation between chemical composition and antibacterial activity of essential oils of some aromatic medicinal plants growing in the Democratic Republic of Congo. J. Ethnopharmacol. 2002, 79, 213–220. [Google Scholar] [CrossRef]
  10. Di Stasi, L.C. Plantas Medicinais: Arte E Ciência: Um Guia De Estudo Interdisciplinar; Editora da Universidade Estadual Paulista: São Paulo, Brazil, 1996. [Google Scholar]
  11. Ahmad, I.; Beg, Z. Antimicrobial and phytochemical studies on 45 Indian medicinal plants against multi-drug resistant human pathogens. J. Ethnopharmacol. 2001, 74, 113–123. [Google Scholar] [CrossRef]
  12. Ankri, S.; Mirelman, D. Antimicrobial properties of allicin from garlic. Microbes Infect. 1999, 1, 125–129. [Google Scholar] [CrossRef]
  13. Voravuthikunchai, S.; Lortheeranuwat, A.; Jeeju, W.; Sririrak, T.; Phongpaichit, S.; Supawita, T. Effective medicinal plants against enterohaemorrhagic Escherichia coli O157:H7. J. Ethnopharmacol. 2004, 94, 49–54. [Google Scholar] [CrossRef] [PubMed]
  14. Gallego, A.; Malik, S.; Yousefzadi, M.; Makhzoum, A.; Tremouillaux-Guiller, J.; Bonfill, M. Erratum to: Taxol from Corylus avellana: Paving the way for a new source of this anti-cancer drug. Plant Cell Tissue Organ Cult. 2017, 129, 1–17. [Google Scholar] [CrossRef]
  15. Malik, S.; Bíba, O.; Grúz, J.; Arroo, R.R.J.; Strnad, M. Biotechnological approaches for producing aryltetralin lignans from Linum species. Phytochem. Rev. 2014, 13, 893–913. [Google Scholar] [CrossRef]
  16. Malik, S.; Bhushan, S.; Sharma, M.; Ahuja, P.S. Biotechnological approaches to the production of shikonins: A critical review with recent updates. Crit. Rev. Biotechnol. 2016, 36, 327–340. [Google Scholar] [CrossRef]
  17. Matsuura, H.N.; Malik, S.; Costa, F.; Yousefzadi, M.; Mirjalili, M.H.; Arroo, R.; Bhambra, A.S.; Strnad, M.; Bonfill, M.; Fett-Neto, A.G. Specialized plant metabolism characteristics and impact on target molecule biotechnological production. Mol. Biotechnol. 2018, 60, 169–183. [Google Scholar] [CrossRef] [PubMed]
  18. Mesquita, L.S.S.; Luz, T.R.S.A.; Mesquita, J.W.C.; Coutinho, D.F.; Amaral, F.M.M.; Ribeiro, M.N.S.; Malik, S. Exploring the anticancer properties of essential oils from family Lamiaceae. Food Rev. Int. 2018, 35, 105–131. [Google Scholar] [CrossRef]
  19. Hussein, H.A.S.A.A.; Hussein, M.S.; Tkachenko, K.G.; Nkomo, M.; Mudau, F.N. Essential oil composition of artemisia vulgaris grown in Egypt. Int. J. Pharm. Pharm. Sci. 2016, 8, 120–123. [Google Scholar]
  20. Mahmood, T.; Hassan, N.; Nazar, N.; Naveed, I. Phylogenetic analysis of different Artemisia species based on chloroplast gene rps11. Arch. Biol. Sci. 2011, 63, 661–665. [Google Scholar] [CrossRef]
  21. Negahban, M.; Moharramipour, S.; Sefidkon, F. Fumigant toxicity of essential oil from Artemisia sieberi Besser against three stored-product insects. J. Stored Prod. Res. 2007, 43, 123–128. [Google Scholar] [CrossRef]
  22. Judžentien, A.; Buzelyte, J. Chemical composition of essential oils of Artemisia vulgaris L. (mugwort) from North Lithuania. Chemija 2006, 17, 12–15. [Google Scholar]
  23. Adams, J.D.; Garcia, C.; Garg, G. Mugwort (Artemisia vulgaris, Artemisia douglasiana, Artemisia argyi) in the Treatment of menopause, premenstrual syndrome, dysmenorrhea and attention deficit hyperactivity disorder. Chin. Med. 2012, 3, 116–123. [Google Scholar] [CrossRef]
  24. Malinowski, L.R.L.; Rosa, E.A.R.; Picheth, C.M.T.F.; Campelo, P.M.S. Atividade antimicrobiana dos extratos aquoso e hidroalcoólico de folhas de Artemisia vulgaris. Rev. Bras. Farm. 2007, 88, 63–66. [Google Scholar]
  25. Rajaram, A.S.R.S.K.; Reddy, C.N.K.S.P.; Sibyala, V.S. Antifertility activity of Artemisia vulgaris leaves on female Wistar rats. Chin. J. Nat. Med. 2014, 3, 4. [Google Scholar]
  26. Tigno, X.T.; de Guzman, F.; Flora, A.M.; Theresa, V. Phytochemical analysis and hemodynamic actions of Artemisia vulgaris L. Clin. Hemorheol. Microcirc. 2000, 23, 167–175. [Google Scholar]
  27. Abiri, R.; Silva, A.L.M.; Mesquita, L.S.S.; Mesquita, J.W.C.; Atabaki, N.; Almeida, E.B.; Shaharuddin, N.A.; Malik, S. Towards a better understanding of Artemisia vulgaris: Botany, phytochemistry, pharmacological and biotechnological potential. Food Res. Int. 2018, 109, 403–415. [Google Scholar] [CrossRef] [PubMed]
  28. Mucciarelli, M.; Caramiello, R.; Maffei, M.; Chialva, F. Essential oils from some Artemisia species growing spontaneously in North-West Italy. Flavour Fragr. J. 1995, 10, 25–32. [Google Scholar] [CrossRef]
  29. Nano, G.M.; Bicchi, C.; Frattini, C.; Gallino, M. On the composition of some oils from Artemisia vulgaris. Planta Med. 1976, 30, 211–215. [Google Scholar] [CrossRef]
  30. Misra, L.N.; Singh, S.P. α-Thujone, the major component of the essential oil from Artemisia vulgaris growing wild in Nilgiri hills. J. Nat. Prod. 1986, 49, 941. [Google Scholar] [CrossRef]
  31. Benabdellah, M.; Benkaddour, M.; Hammouti, B.; Bendahhou, M.; Aouniti, A. Inhibition of steel corrosion in 2M H 3 PO 4 by Artemisia oil. Appl. Surf. Sci. 2006, 252, 6212–6217. [Google Scholar] [CrossRef]
  32. Näf-Müller, R.; Pickenhagen, W.; Willhalm, B. New irregular monoterpenes in Artemisia vulgaris. Helv. Chim. Acta 1981, 64, 1424–1430. [Google Scholar]
  33. Alizadeh, M.; Aghaei, M.; Sharifian, I.; Saadatian, M. Chemical composition of essential oil of Artemisia vulgaris from West Azerbaijan, Iran. Electron. J. Environ. Agric. Food Chem. 2012, 11, 493–496. [Google Scholar]
  34. Pino, J.A.; Rosado, A.; Fuentes, V. Composition of the essential oil of Artemisia vulgaris L. herb from Cuba. J. Essent. Oil Res. 1999, 11, 477–478. [Google Scholar] [CrossRef]
  35. Schmidt, A.; Kochanowski, K.; Vedelaar, S.; Ahrné, E.; Volkmer, B.; Callipo, L.; Heinemann, M. The quantitative and condition-dependent Escherichia coli proteome. Nat. Biotechnol. 2016, 34, 104–110. [Google Scholar] [CrossRef] [PubMed]
  36. Kumamoto, C.A.; Vinces, M.D. Contributions of hyphae and hypha-co-regulated genes to Candida albicans virulence. Cell. Microbiol. 2005, 7, 1546–1554. [Google Scholar] [CrossRef] [Green Version]
  37. Glory, A.; van Oostende, C.T.; Geitmann, A.; Bachewich, C. Depletion of the mitotic kinase Cdc5p in Candida albicans results in the formation of elongated buds that switch to the hyphal fate over time in a Ume6p and Hgc1p-dependent manner. Fungal Genet. Biol. 2017, 107, 51–66. [Google Scholar] [CrossRef] [PubMed]
  38. Noble, S.M.; Gianetti, B.A.; Witchley, J.N. Candida albicans cell-type switching and functional plasticity in the mammalian host. Nat. Rev. Microbiol. 2017, 15, 96–108. [Google Scholar] [CrossRef] [PubMed]
  39. Stevenson, L.A.; Chilton, N.B.; Gasser, R.B. Differentiation of Haemonchus placei from H. contortus (Nematoda: Trichostrongylidae) by the ribosomal DNA second internal transcribed spacer. Int. J. Parasitol. 1995, 25, 483–488. [Google Scholar] [CrossRef]
  40. Coles, G.C.; Bauer, C.; Borgsteede, F.H.M.; Geerts, S.; Klei, T.R.; Taylor, M.A.; Waller, P.J. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 1992, 44, 35–44. [Google Scholar] [CrossRef]
  41. Bahuaud, D.; De Montellano, C.M.O.; Chauveau, S.; Prevot, F.; Torres-Acosta, F.; Fouraste, I.; Hoste, H. Effects of four tanniferous plant extracts on the in vitro exsheathment of third-stage larvae of parasitic nematodes. Parasitology 2006, 132, 545–554. [Google Scholar] [CrossRef] [PubMed]
  42. Ghelardini, C.; Galeotti, N.; Mannelli, L.D.C.; Mazzanti, G.; Bartolini, A. Local anaesthetic activity of β-caryophyllene. Farmaco 2001, 56, 387–389. [Google Scholar] [CrossRef]
  43. Ormeño, E.; Baldy, V.; Ballini, C.; Fernandez, C. Production and diversity of volatile terpenes from plants on calcareous and siliceous soils: effect of soil nutrients. J. Chem. Ecol. 2008, 34, 1219. [Google Scholar] [CrossRef] [PubMed]
  44. Gertsch, J.; Leonti, M.; Raduner, S.; Racz, I.; Chen, J.Z.; Xie, X.Q.; Zimmer, A. Beta-caryophyllene is a dietary cannabinoid. Proc. Nat. Acad. Sci. USA 2008, 105, 9099–9104. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Rasmann, S.; Köllner, T.G.; Degenhardt, J.; Hiltpold, I.; Toepfer, S.; Kuhlmann, U.; Turlings, T.C.J. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 2005, 434, 732–737. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Cowan, M.M. Plant products as antimicrobial agents. Clin. Microbiol. Rev. 1999, 12, 564–582. [Google Scholar] [CrossRef] [PubMed]
  47. Sabulal, B.; Dan, M.; Kurup, R.; Pradeep, N.S.; Valsamma, R.K.; George, V. Caryophyllene-rich rhizome oil of Zingiber nimmonii from South India: chemical characterization and antimicrobial activity. Phytochemistry 2006, 67, 2469–2473. [Google Scholar] [CrossRef]
  48. Kil, B.S.; Han, D.M.; Lee, C.H.; Kim, Y.S.; Yun, K.Y.; Yoo, H.G. Allelopathic effects of Artemisia lavandulaefolia. Korean J. Ecol. 2000, 23, 149–155. [Google Scholar]
  49. Wang, H.; Nair, M.G.; Strasburg, G.M.; Booren, A.M.; Gray, J.I. Antioxidant polyphenols from tart cherries (Prunus cerasus). J. Agric. Food Chem. 1999, 47, 840–844. [Google Scholar] [CrossRef]
  50. Rivero-Cruz, B.; Rivero-Cruz, I.; Rodríguez, J.M.; Cerda-García-Rojas, C.M.; Mata, R. Qualitative and quantitative analysis of the active components of the essential oil from brickellia v eronicaefolia by nuclear magnetic resonance spectroscopy. J. Nat. Prod. 2006, 69, 1172–1176. [Google Scholar] [CrossRef]
  51. Li, F.Q.; Yang, S.P.; Chen, Y.; Lao, S.C.; Wang, Y.T.; Dong, T.T.X.; Tsim, K.W.K. Identification and quantitation of eleven sesquiterpenes in three species of Curcuma rhizomes by pressurized liquid extraction and gas chromatography-mass spectrometry. J. Pharm. Biomed. Anal. 2005, 39, 552–558. [Google Scholar]
  52. Bülow, N.; König, W.A. The role of germacrene D as a precursor in sesquiterpene biosynthesis: investigations of acid catalyzed, photochemically and thermally induced rearrangements. Phytochemistry 2000, 55, 141–168. [Google Scholar] [CrossRef]
  53. Marongiu, B.; Piras, A.; Porcedda, S.; Scorciapino, A. Chemical composition of the essential oil and supercritical CO2 extract of Commiphora myrrha (Nees) Engl. and of Acorus calamus L. J. Agric. Food Chem. 2005, 53, 7939–7943. [Google Scholar] [CrossRef] [PubMed]
  54. Noge, K.; Becerra, J.X. Germacrene D, a common sesquiterpene in the genus Bursera (Burseraceae). Molecules 2009, 14, 5289–5297. [Google Scholar] [CrossRef]
  55. Katsiotis, S.T.; Langezaal, C.R.; Scheffer, J.J.C. Analysis of the volatile compounds from cones of ten Humulus lupulus cultivars. Planta Med. 1989, 55, 634. [Google Scholar] [CrossRef]
  56. El Hadri, A.; del Rio, M.A.G.; Sanz, J.; Coloma, A.G.; Idaomar, M.; Ozonas, B.R.; Reus, M.I.S. Cytotoxic activity of α-humulene and transcaryophyllene from Salvia officinalis in animal and human tumor cells. An. Real Acad. Nac. Farm. 2010, 76, 343–356. [Google Scholar]
  57. Fernandes, E.S.; Passos, G.F.; Medeiros, R.; da Cunha, F.M.; Ferreira, J.; Campos, M.M.; Calixto, J.B. Anti-inflammatory effects of compounds alpha-humulene and (−)-trans-caryophyllene isolated from the essential oil of Cordia verbenacea. Eur. J. Pharm. 2007, 569, 228–236. [Google Scholar] [CrossRef] [PubMed]
  58. Legault, J.; Pichette, A. Potentiating effect of β-caryophyllene on anticancer activity of α-humulene, isocaryophyllene and paclitaxel. J. Pharm. Pharm. 2007, 59, 1643–1647. [Google Scholar] [CrossRef] [PubMed]
  59. Langenheim, J.H. Higher plant terpenoids: A phytocentric overview of their ecological roles. J. Chem. Ecol. 1994, 20, 1223–1280. [Google Scholar] [CrossRef] [PubMed]
  60. Wang, R.L.; Peng, S.L.; Zeng, R.S.; Ding, L.W.; Xu, Z.F. Cloning, expression and wounding induction of β-caryophyllene synthase gene from Mikania micrantha HBK and allelopathic potential of β-caryophyllene. Allelopathy J. 2009, 24, 35–44. [Google Scholar]
  61. Lutz, D.L.; Alviano, D.S.; Alviano, C.S.; Kolodziejczyk, P.P. Screening of chemical composition, antimicrobial and antioxidant activities of Artemisia essential oils. Phytochemistry 2008, 69, 1732–1738. [Google Scholar] [CrossRef]
  62. Iqbal, Z.; Lateef, M.; Ashraf, M.; Jabbar, A. Anthelmintic activity of Artemisia brevifolia in sheep. J. Ethnopharmacol. 2004, 93, 265–268. [Google Scholar] [CrossRef] [PubMed]
  63. Tariq, K.A.; Chishti, M.Z.; Ahmad, F.; Shawl, A.S. Anthelmintic activity of extracts of Artemisia absinthium against ovine nematodes. Vet. Parasitol. 2009, 160, 83–88. [Google Scholar] [CrossRef] [PubMed]
  64. Caner, A.; Döşkaya, M.; Deǧirmenci, A.; Can, H.; Baykan, Ş.; Üner, A.; Gürüz, Y. Comparison of the effects of Artemisia vulgaris and Artemisia absinthium growing in western Anatolia against trichinellosis (Trichinella spiralis) in rats. Exp. Parasitol. 2008, 119, 173–179. [Google Scholar] [CrossRef] [PubMed]
  65. Squires, J.M.; Ferreira, J.F.S.; Lindsay, D.S.; Zajac, A.M. Effects of artemisinin and Artemisia extracts on Haemonchus contortus in gerbils (Meriones unguiculatus). Vet. Parasitol. 2011, 175, 103–108. [Google Scholar] [CrossRef]
  66. Zhu, L.; Dai, J.L.; Yang, L.; Qiu, J. In vitro ovicidal and larvicidal activity of the essential oil of Artemisia lancea against Haemonchus contortus (Strongylida). Vet. Parasitol. 2013, 195, 112–117. [Google Scholar] [CrossRef] [PubMed]
  67. Caixeta, S.C.; Magalhães, L.G.; de Melo, N.I.; Wakabayashi, K.A.L.; de P. Aguiar, G.; de P. Aguiar, D.; Tavares, D.C. Chemical composition and in vitro schistosomicidal activity of the essential oil of Plectranthus neochilus grown in Southeast Brazil. Chem. Biodivers. 2011, 8, 2149–2157. [Google Scholar] [CrossRef] [PubMed]
  68. De Melo, N.I.; Magalhaes, L.G.; De Carvalho, C.E.; Wakabayashi, K.A.L.; De P. Aguiar, G.; Ramos, R.C.; Groppo, M. Schistosomicidal activity of the essential oil of Ageratum conyzoides L. (Asteraceae) against adult Schistosoma mansoni worms. Molecules 2011, 16, 762–773. [Google Scholar] [CrossRef]
  69. Olounladé, P.A.; Azando, E.V.B.; Hounzangbé-Adoté, M.S.; Ha, T.B.T.; Leroy, E.; Moulis, C.; Valentin, A. In vitro anthelmintic activity of the essential oils of Zanthoxylum zanthoxyloides and Newbouldia laevis against Strongyloides ratti. Parasitol. Res. 2012, 110, 1427–1433. [Google Scholar] [CrossRef] [PubMed]
  70. Babu, R.O.D.; Moorkoth, S.; Azeez, S.; Eapen, S.J. Virtual screening and in vitro assay of potential drug like inhibitors from spices against Glutathione-S-Transferase of Meloidogyne incognita. Bioinformation 2012, 8, 319. [Google Scholar] [CrossRef] [PubMed]
  71. Bai, P.H.; Bai, C.Q.; Liu, Q.Z.; Du, S.S.; Liu, Z.L. Nematicidal activity of the essential oil of Rhododendron anthopogonoides aerial parts and its constituent compounds against Meloidogyne incognita. Z. Naturforsch. C 2013, 68, 307–312. [Google Scholar] [CrossRef] [PubMed]
  72. Jackson, F.; Hoste, H. In vitro methods for the primary screening of plant products for direct activity against ruminant gastrointestinal nematodes. In Vitro Screening of Plant Resources for Extra-Nutritional Attributes in Ruminants: Nuclear and Related Methodologies; Springer: Dordrecht, The Netherlands, 2010; pp. 25–45. [Google Scholar]
Table 1. Chemical composition (%) of Artemisia vulgaris essential oils.
Table 1. Chemical composition (%) of Artemisia vulgaris essential oils.
No.CompoundRI *%
2Bornyl acetate12871.46
3Lavandulyl acetate12982.83
6Germacrene D148216.17
10Germacrene B15581.39
11Nerolidol, acetate15700.49
13Caryophyllene oxide15835.67
15Isoaromadendrene epoxide16062.17
16Longipinocarveol, trans-16340.65
* Retention index.
Table 2. Antimicrobial activity of Artemisia vulgaris essential oils against Staphylococcus aureus, Escherichia coli, and Candida albicans *.
Table 2. Antimicrobial activity of Artemisia vulgaris essential oils against Staphylococcus aureus, Escherichia coli, and Candida albicans *.
-MicroorganismPositive ControlCC
E. coli15.615.60.156 µg/mL-+
S. aureus62.41250.078 µg/mL-+
C. albicans31.212520 IU/mL20 IU/mL+
* Concentration expressed in μL of essential oil/mL BHI broth; C + (Positive Control): For E. coli and S. aureus, chloramphenicol 0.02 mg/mL; Positive Control for C. albicans nystatin 100,000 IU/mL. CC: Positive growth control (there was visible microbial growth). MIC, Minimum Inhibitory Concentration; MBC, Minimum Bactericidal Concentration; MFC, Minimum Fungicidal Concentration.

Share and Cite

MDPI and ACS Style

Malik, S.; de Mesquita, L.S.S.; Silva, C.R.; de Mesquita, J.W.C.; de Sá Rocha, E.; Bose, J.; Abiri, R.; de Maria Silva Figueiredo, P.; Costa-Júnior, L.M. Chemical Profile and Biological Activities of Essential Oil from Artemisia vulgaris L. Cultivated in Brazil. Pharmaceuticals 2019, 12, 49.

AMA Style

Malik S, de Mesquita LSS, Silva CR, de Mesquita JWC, de Sá Rocha E, Bose J, Abiri R, de Maria Silva Figueiredo P, Costa-Júnior LM. Chemical Profile and Biological Activities of Essential Oil from Artemisia vulgaris L. Cultivated in Brazil. Pharmaceuticals. 2019; 12(2):49.

Chicago/Turabian Style

Malik, Sonia, Ludmilla Santos Silva de Mesquita, Carolina Rocha Silva, José Wilson Carvalho de Mesquita, Emmeline de Sá Rocha, Jayakumar Bose, Rambod Abiri, Patricia de Maria Silva Figueiredo, and Livio M. Costa-Júnior. 2019. "Chemical Profile and Biological Activities of Essential Oil from Artemisia vulgaris L. Cultivated in Brazil" Pharmaceuticals 12, no. 2: 49.

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop