Skip to main content
Log in

Repellency of aerial parts of Teucrium polium L. essential oil formulation against Anopheles stephensi

  • Original Research Article
  • Published:
International Journal of Tropical Insect Science Aims and scope Submit manuscript

Abstract

Plants have traditionally been used as eco-friendly tools for insect management with insecticide/repellent activities. Natural-based agents, compared to chemical insecticides/repellents that have harmful effects on humans and environment, seem to be more effective and safer compounds. The repellent activity of Teucrium polium L. essential oil (TPEO) and its repellent emulsified formulation (REF) were evaluated against Anopheles stephensi (An. stephensi) mosquitoes using a Klun & Debboun (K&D) module under laboratory conditions. The safety of REF was established by the Draize skin irritation study. The chemical components of TPEO were investigated using gas chromatography/mass spectrometry (GC/MS) technique. The most repellent activity (95%) was observed in the highest concentration of TPEO. The REF containing 20% EO was found to have 92% repellent effect with six hours of durability. The most significant components identified were nerolidol (57.22%), α-farnesene (8.41%), spathulenol (6.12%), germacrene D (5.64%), β-caryophyllene (3.71%), β-farnesene (3.25%), and caryophyllene oxide (2.31%). TPEO-emulsified formulation with significant repellency and no skin irritation has the potential to develop as a commercial repellent after specific quality control tests.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abdelgaleil SAM, Al-Nagar NMA, Abou-Taleb HK, Shawir MS (2022) Effect of monoterpenes, phenylpropenes and sesquiterpenes on development, fecundity and fertility of Spodoptera littoralis (Boisduval). Int J Trop Insect Sci 42:245–253

    Article  Google Scholar 

  • Aburjai T, Hudaib M, Cavrini V (2006) Composition of the Essential Oil from Jordanian Germander (Teucrium polium L.). J Essent Oil Res 18:97–99

  • Adams RP (2007) Identification of Essential Oil Components by Gas Chromatography/ Quadrupole Mass Spectrometry. Allured Publishing Co., Carol Stream, Illinois

    Google Scholar 

  • Aghili Khorasani MTI (2008) Makhzan ul-Advia, The Institue of Medical History. Iran University of Medical Sciences, Tehran, Iran, Islamic and Complementary Medicine Studies

    Google Scholar 

  • Araújo MJ, Câmara CA, Born FS, Moraes MM, Badj CA (2012) Acaricidal activity and repellency of essential oil from Piper aduncum and its components against Tetranychus urticae. Exp Appl Acarol 57:139–155

    Article  PubMed  Google Scholar 

  • Asgharipour MR, Shabankare HG (2017) Comparison of chemical composition of Teucrium polium L. essential oil affected by phenological stages. Bangladesh J Bot 46:583–588

    Google Scholar 

  • Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils–a review. Food Chem Toxicol 46:446–475

    Article  PubMed  CAS  Google Scholar 

  • Bedini S, Guarino S, Echeverria MC et al (2020) Allium sativum, Rosmarinus officinalis, and Salvia officinalis essential oils: A spiced shield against blowflies. Insects 11:143

    Article  PubMed Central  Google Scholar 

  • Belmekki N, Bendimerad N, Bekhechi C, Fernandez X (2013) Chemical analysis and antimicrobial activity of Teucrium polium L. essential oil from Western Algeria. J Med Plant Res 7:897–902

    CAS  Google Scholar 

  • Bigham M, Hosseininaveh V, Nabavi B, Talebi K, Esmaeilzadeh NS (2010) Effects of essential oil from Teucrium polium on some digestive enzyme activities of Musca domestica. Entomol Res 40:37–45

    Article  Google Scholar 

  • Bülow N, König WA (2000) The role of germacrene D as a precursor in sesquiterpene biosynthesis: investigations of acid catalyzed, photochemically and thermally induced rearrangements. Phytochemistry 55:141–168

    Article  PubMed  Google Scholar 

  • Cantrell CL, Klun JA, Bryson CT, Kobaisy M, Duke SO (2005) Isolation and identification of mosquito bite deterrent terpenoids from leaves of American (Callicarpa americana) and Japanese (Callicarpa japonica) beautyberry. J Agric Food Chem 53:5948–5953

    Article  PubMed  CAS  Google Scholar 

  • Chaaban A, Nogueira Martins CE, Bretanha LC (2018) Insecticide activity of Baccharis dracunculifolia essential oil against Cochliomyia macellaria (Diptera: Calliphoridae). Nat Prod Res 32:2954–2958

    Article  PubMed  CAS  Google Scholar 

  • Chan WK, Tan LTH, Chan KG, Lee LH, Goh BH (2016) Nerolidol: A sesquiterpene alcohol with multi-faceted pharmacological and biological activities. Molecules 21:529

    Article  PubMed Central  Google Scholar 

  • Da Silva RCS, Milet-Pinheiro P, da Silva PCB et al (2015) (E)-caryophyllene and α-humulene: Aedes aegypti oviposition deterrents elucidated by gas chromatography-electrophysiological assay of Commiphora leptophloeos leaf oil. PLoS ONE 10:e0144586

    Article  PubMed  PubMed Central  Google Scholar 

  • Debboun M, Strickman D (2013) Insect repellents and associated personal protection for a reduction in human disease. Med Vet Entomol 27:1–9

    Article  PubMed  CAS  Google Scholar 

  • Dehghankar M, Ravasan NM, Tahghighi A, Karimian F, Karami M (2021) Bioactivities of rose-scented geranium nanoemulsions against the larvae of Anopheles stephensi and their gut bacteria. PLoS ONE 16:e0246470

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Di Campli E, Di Bartolomeo S, Pizzi PD et al (2012) Activity of tea tree oil and nerolidol alone or in combination against Pediculus capitis (head lice) and its eggs. Parasitol Res 111:1985–1992

    Article  PubMed  PubMed Central  Google Scholar 

  • Ebadollahi A, Taghinezhad E (2020) Modeling and optimization of the insecticidal effects of Teucrium polium L.essential oil against red flour beetle (Tribolium castaneum Herbst) using response surface methodology. Inf Process Agric 7:286–293

    Google Scholar 

  • Eskandari SE, Firooz A, Nassiri-Kashani M et al (2018) Safety evaluation of nano-liposomal formulation of amphotericin B (Sina Ampholeish) in animal model as a candidate for treatment of cutaneous leishmaniasis. J Arthropod Borne Dis 12:269–275

    PubMed  PubMed Central  Google Scholar 

  • Farahbakhsh J, Najafian S, Hosseinifarahi M, Gholipour S (2021) Essential oil composition and phytochemical properties from leaves of felty germander (Teucrium polium L.) and spearmint (Mentha spicata L.). J Essent Oil Bear Plants 24:147–159

    Article  CAS  Google Scholar 

  • Fidyt K, Fiedorowicz A, Strządała L, Szumny A (2016) β-caryophyllene and β-caryophyllene oxide—natural compounds of anticancer and analgesic properties. Cancer Med 5:3007–3017

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Flint H, Salter S, Walters S (1979) Caryophyllene: an attractant for the green lacewing. Environ Entomol 8:1123–1125

    Article  CAS  Google Scholar 

  • Galati E, Mondello M, D’Aquino A et al (2000) Effects of Teucrium divaricatum Heldr. ssp. divaricatum decoction on experimental ulcer in rats. J Ethnopharmacol 72:337–342

    Article  PubMed  CAS  Google Scholar 

  • Garud A, Ganesan K, Garud N, Vijayaraghavan R (2013) Topical preparation of newer and safer analogs of N, N-diethyl-2-phenylacetamide (DEPA) against Aedes aegypti mosquitoes. J Cosmet Dermatol Sci Appl 3(1A):22–27

    Google Scholar 

  • Ghabbari M, Guarino S, Caleca V et al (2018) Behavior-modifying and insecticidal effects of plant extracts on adults of Ceratitis capitata (Wiedemann)(Diptera Tephritidae). J Pest Sci 91:907–917

    Article  Google Scholar 

  • Gillij YG, Gleiser RM, Zygadlo JA (2008) Mosquito repellent activity of essential oils of aromatic plants growing in Argentina. Bioresour Technol 99:507–2515

    Article  Google Scholar 

  • Hamouda AB, Bnina EB, Chaieb I, Laarif A, Jannet HB (2021) Cyclic and acyclic alcohols: a structure-activity relationship study correlation between insecticidal activity and chemical structure. Int J Trop Insect Sci 41:961–968

    Article  Google Scholar 

  • Haris A, Azeem A, Binyameen M (2022) Mosquito repellent potential of Carpesium abrotanoides essential oil and its main components against a dengue vector, Aedes aegypti (Diptera: Culicidae). J Med Entomol 59:801–809

    Article  PubMed  CAS  Google Scholar 

  • Inocente EA, Nguyen B, Manwill PK et al (2019) Insecticidal and antifeedant activities of Malagasy medicinal plant (Cinnamosma sp.) extracts and drimane-type sesquiterpenes against Aedes aegypti mosquitoes. Insects 10:373

  • Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66

    Article  PubMed  CAS  Google Scholar 

  • Kerbouche L, Hazzit M, Ferhat MA, Baaliouamer A, Miguel MG (2015) Biological activities of essential oils and ethanol extracts of Teurium polium subsp. capitatum (L.) Briq. and Origanum floribundum munby. J Essent Oil Bear Plants 18:1197–1208

    Article  CAS  Google Scholar 

  • Khani A, Heydarian M (2014) Fumigant and repellent properties of sesquiterpene-rich essential oil from Teucrium polium subsp. capitatum (L.). Asian Pac J Trop Med 7:956–961

    Article  PubMed  CAS  Google Scholar 

  • Khater HF, Selim AM, Abouelella GA et al (2019) Commercial Mosquito Repellents and Their Safety Concerns. In: Kasenga FH (ed) Malaria. IntechOpen. United Kingdom

  • Kim EH, Kim HK, Choi DH, Ahn YJ (2003) Acaricidal activity of clove bud oil compounds against Tyrophagus putrescentiae (Acari: Acaridae). Appl Entomol Zool 38:261–266

    Article  CAS  Google Scholar 

  • Kiran SR, Devi PS (2007) Evaluation of mosquitocidal activity of essential oil and sesquiterpenes from leaves of Chloroxylon swietenia DC. Parasitol Res 101:413–418

    Article  PubMed  Google Scholar 

  • Kiran SR, Devi PS (2013) Repellency of essential oil and sesquiterpenes from leaves of Chloroxylon swietenia DC against mosquito bites. VRI Phytomedicine 1:103–108

    Google Scholar 

  • Klun JA, Debboun M (2000) A new module for quantitative evaluation of repellent efficacy using human subjects. J Med Entomol 37:177–181

    Article  PubMed  CAS  Google Scholar 

  • Klun JA, Khrimian A, Margaryan A, Kramer M, Debboun M (2003) Synthesis and repellent efficacy of a new chiral piperidine analog: Comparison with deet and bayrepel activity in human-volunteer laboratory assays against Aedes aegypti and Anopheles stephensi. J Med Entomol 40:293–299

    Article  PubMed  CAS  Google Scholar 

  • Kohli C, Kumar R, Meena GS, Singh MM, Sahoo J, Ingle GK (2014) Usage and perceived side effects of personal protective measures against mosquitoes among current users in delhi, J Parasitol Res 2014:Article ID 628090

  • Koutsaviti K, Giatropoulos A, Pitarokili D, Papachristos D, Michaelakis A, Tzakou O (2015) Greek Pinus essential oils: larvicidal activity and repellency against Aedes albopictus (Diptera: Culicidae). Parasitol Res 114:583–592

    Article  PubMed  Google Scholar 

  • Lograda T, Ramdani M, Chalard P, Figueredo G, Deghar A (2014) Chemical Analysis and Antimicrobial Activity of Teucrium polium L. Essential Oil from Eastern Algeria. Am J Adv Drug Deliv 2:697–710

  • Markheiser A, Rid M, Biancu S, Gross J, Hoffmann C (2020) Tracking short-range attraction and oviposition of European grapevine moths affected by volatile organic compounds in a four-chamber olfactomete. Insects 11:45

    Article  PubMed Central  Google Scholar 

  • Moghtader M (2009) Chemical composition of the essential oil of Teucrium polium L. from Iran. Am Eurasian J Agric Environ Sci 5:843–846

  • Mozaffarian VA (1966) Dictionary of Iranian Plant Names. Farhang Mo'aser, Tehran, Iran

  • Mwangi JK, Ndung’u M, Gitu L (2013) Repellent activity of the essential oil from Capparis tomentosa against maize weevil Sitophilus zeamais. J Manag Dev 1:9–13

    Google Scholar 

  • Nacéra B, Nassima B, Chahrazed B, Xavier F (2013) Chemical analysis and antimicrobial activity of Teucrium polium L. essential oil from Western Algeria. J Med Plant Res 7:897–902

    Google Scholar 

  • Nararak J, Sathantriphop S, Kongmee M et al (2019) Excito-repellent activity of β-caryophyllene oxide against Aedes aegypti and Anopheles minimus. Acta Trop 197:105030

    Article  PubMed  CAS  Google Scholar 

  • Ndiath MO (2013) Insecticides and insecticide resistance. In: Ariey F, Gay F, Ménard R (eds) Malaria Control and Elimination, Methods in Molecular Biology. Humana, New York, pp 287–304

    Google Scholar 

  • Nerio LS, Olivero-Verbel J, Stashenko E (2010) Repellent activity of essential oils: A review. Bioresour Technol 101:372–378

    Article  PubMed  CAS  Google Scholar 

  • Othman MB, Salah-Fatnassi KBH, Ncibi S, Elaissi A, Zourgu L (2017) Antimicrobial activity of essential oil and aqueous and ethanol extracts of Teucrium polium L. subsp. gabesianum (L.H.) from Tunisia. Physiol Mol Biol Plants 23:723–729

    Article  PubMed  PubMed Central  Google Scholar 

  • Paluch G, Grodnitzky J, Bartholomay L, Coats J (2009) Quantitative structure− activity relationship of botanical sesquiterpenes: Spatial and contact repellency to the yellow fever mosquito, Aedes aegypti. J Agric Food Chem 57:7618–7625

    Article  PubMed  CAS  Google Scholar 

  • Paluch GE, Zhu J, Bartholomay L, Coats RJ (2011) Amyris and siam-wood essential oils: Insect activity of sesquiterpenes. Pestic Househ Struct Resid Pest Manag 1015:5–18

    Article  Google Scholar 

  • Pavela R, Govindarajan M (2017) The essential oil from Zanthoxylum monophyllum a potential mosquito larvicide with low toxicity to the non-target fish Gambusia affinis. J Pest Sci 90:369–378

    Article  Google Scholar 

  • Perrino EV, Valerio F, Gannouchi A, Trani A, Mezzapesa G (2021) Ecological and plant community implication on essential oils composition in useful wild officinal species: A pilot case study in Apulia (Italy). Plants 10:574

  • Raeia F, Ashooria N, Eftekhara F, Yousefzadib M (2014) Chemical composition and antibacterial activity of Teucrium polium essential oil against urinary isolates of Klebsiella pneumoniae. J Essent Oil Res 26:65–69

    Article  Google Scholar 

  • Sosa ME, Tonn CE (2008) Plant secondary metabolites from Argentinean semiarid lands: bioactivity against insects. Phytochem Rev 7:3–24

    Article  CAS  Google Scholar 

  • Suleiman RA, Mgani QA, Nyandoro SS (2014) Chemical compositions and mosquito repellency of essential oils from Artabotrys hexapetalus and Artabotrys rupestris. Int J Biol Chem Sci 8:2804–2812

    Article  CAS  Google Scholar 

  • Tabanca N, Demirci B, Ali A, Ali Z, Blythe EK, Khan IA (2015) Essential oils of green and red Perilla frutescens as potential sources of compounds for mosquito management. Ind Crops Prod 65:36–44

    Article  CAS  Google Scholar 

  • Tahghighi A, Maleki-Ravasan N, Djadid ND et al (2019) GC–MS analysis and anti–mosquito activities of Juniperus virginiana essential oil against Anopheles stephensi (Diptera: Culicidae). Asian Pac J Trop Biomed 9:168–175

    Article  CAS  Google Scholar 

  • Wang ZQ, Perumalsamy H, Wang M, Shu S, Ahn YJ (2016) Larvicidal activity of Magnolia denudata seed hydrodistillate constituents and related compounds and liquid formulations towards two susceptible and two wild mosquito species. Pest Manag Sci 72:897–906

    Article  PubMed  CAS  Google Scholar 

  • Wangrawa DW, Badolo A, Guelbéogo WM et al (2021) Larvicidal, oviposition-deterrence, and excito-repellency activities of four essential oils: an eco-friendly tool against malaria vectors Anopheles coluzzii and Anopheles gambiae (Diptera: Culicidae). Int J Trop Insect Sci 41:1771–1781

    Article  Google Scholar 

  • WHO (2020) World Malaria Report 2020. https://www.who.int/publications/i/item/9789240015791

  • You CX, Zhang WJ, Guo SS et al (2015) Chemical composition of essential oils extracted from six Murraya species and their repellent activity against Tribolium castaneum. Ind Crops Prod 76:681–687

    Article  CAS  Google Scholar 

  • YuQing L, Ming X, QingChen Z, FangYuan Z, JiQian W (2010) Toxicity of β-caryophyllene from Vitex negundo (Lamiales: Verbenaceae) to Aphis gossypii Glover (Homoptera: Aphididae) and its action mechanism. Acta Entomol Sin 53:396–404

    Google Scholar 

  • Zhu L, Tian Y (2011) Chemical composition and larvicidal activity of Blumea densiflora essential oils against Anopheles anthropophagus: a malarial vector mosquito. Parasitol Res 109:1417–1422

    Article  PubMed  Google Scholar 

Download references

Funding

This research did not receive any specific grant from the funding agencies.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Saeedeh Ghafari.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest among them.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tahghighi, A., Ghafari, S., Ghanavati, S. et al. Repellency of aerial parts of Teucrium polium L. essential oil formulation against Anopheles stephensi. Int J Trop Insect Sci 42, 3541–3550 (2022). https://doi.org/10.1007/s42690-022-00863-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42690-022-00863-x

Keywords

Navigation