Chemical composition and repellency of Nigella sativa L. seed essential oil against Anopheles gambiae sensu stricto

Document Type: Original Article

Authors

1 Department of Physical and Biological Sciences, Murang’a University, Box75-10200, Murang’a, Kenya

2 Department of Chemistry, Kenyatta University, P.O. Box 43844, Nairobi, Kenya

Abstract

Malaria which is caused by the Plasmodium parasite and transmitted through bites of infected female Anopheles mosquitoes is an important public health concern in Africa. Insect repellents are commercially available but most of the synthetic repellents have adverse effects to the user as well as the environment. Previous studies have shown that Nigella sativa L. seed extracts have insecticidal and insect repelling activity. The objective of the present study was to evaluate the repellence efficacy of essential oil of Nigella sativa L. seeds on Anopheles gambiae sensu stricto and to determine the chemical composition of the essential oil. The repellence activity of the essential oil was dose-dependent and comparable to that of DEET (N,N-diethyl-m-toluamide). The repellence of the oil was 98.81 and 100% at concentrations of 0.01 and 0.1 g/mL, respectively. GC-MS analysis showed the major components of the essential oil to be p-cymene (34.67%), α-thujene (11.55%), trans-4-methoxythujane (5.81%), β-pinene (4.66%), methylcyclohexane (3.11%), α-pinene (2.82) and longifolene (2.55%). The repellence activity of N. sativa seed oil against An. gambiae can be attributed to the presence of α-pinene, p-cymene and longifolene. These findings have confirmed that the essential oil of N. sativa seeds contains compounds that repel An. gambiae and therefore can be used to control spread of malaria through prevention of mosquito bites.

Graphical Abstract

Chemical composition and repellency of Nigella sativa L. seed essential oil against Anopheles gambiae sensu stricto

Keywords


Abdellatif, F., Hassani, A., 2015. Chemical composition of the essential oils from leaves of Melissa officinalis extracted by hydrodistillation, steam distillation, organic solvent and microwave hydrodistillation. J. Mater. Environ. Sci. 6(1), 207-213.

Adams, R.P., 1995. Identification of essential oil components by gas chromatography/mass spectroscopy. Allured publishing Co. Carol Stream, Illinois.

Adib-Hajbaghery, M., Rafiee, S., 2018.  Medicinal plants use by elderly people in Kashan, Iran. J. Nurs. Midwifery. Stud. 7(2), 67-73.

Adil, B., Tarik, A., Kribii, A., Ounine, K., 2015. The study of the insecticidal effect of Nigella sativa essential oil against Tuta absoluta larvae. IJSTR 4(10), 88-90.

Ahmed, A.M., 2007. A dual effect for the black seed oil on the malaria vector Anopheles gambiae: Enhances immunity and reduce the concomitant reproductive cost. J. Entomol. 4(1), 1-19.

Jeruto, P., Arama, P., Anyango, B., Nyunja, R., Taracha, C., Opiyo, S., 2017. Morphometric study of Senna didymobotrya (Fresen.) H.S. Irwin and Barneby in Kenya. J. Nat. Sci. Res. 7(6), 54-69.

Barnard, D.R., 2005. Biological assay methods for mosquito repellents. J. Am. Mosq. Contr. Assoc. 21(4), 12-16.

Barnard, D.R., Xue, R.D., 2004. Laboratory evaluation of mosquito repellents against Aedes albopictus, Culex nigripalpus, and Ochlerotatus triseriatus (Diptera: Culicidae). J. Med. Entomol. 41, 726 -730.

Botnick, I., Xue, W., Bar, E., Ibdah, M., Schwartz, A., Joel, DM., Lev, E., Fait, A., Lewinsohn, E., 2012. Distribution of primary and specialized metabolites in Nigella sativa Seeds, a spice with vast traditional and historical uses. Molecules 17, 10159-10177.

Burits, M., Bucar, F., 2000. Anti-oxidant activity of N. sativa essential oil. Phytother. Res. 14, 323-328.

Carroll, J.F., Demirci, B., Kramer, M., Bernier, U.R., Agramonte, N.M.K., Baser, K.H.C., Nurhayat, T.N., 2017. Repellency of the Origanum onites L. essential oil and constituents to the lone star tick and yellow fever mosquito. Nat. Prod. Res. 31(18), 2192-2197.

Costa, L.G., Garrick, J., Roque, P.J., Pellacani, C., 2015. Nutraceuticals in CNS Diseases: Potential Mechanisms of Neuroprotection. in Nutraceuticals: Efficacy, Safety, and Toxicity, Gupta, R.C., Ed., Elsevier, New York, NY, USA.

Dinagaran, S., Sridhar, S., Eganathan, P., 2016. Chemical composition and antioxidant activities of black seed oil (Nigella sativa L.). IJPSR 7(11), 4473-4479.

Esimone, C.O., Attama, A.A., Ngwu, G., Iloabanafo, C.A., Momoh, M.A., Onaku. L.O., 2011. Mosquito repellent activity of herbal ointments formulated with Ocimum gratissimum oil. J. Pharm. Res. 4, 3442-3444.

Farooqi, A.A., Sreeramy, B.S., Sirinivasappa, K.N., 2005. Cultivation of crops, Universities Press (India) Private Limited, Himayatnegar, Hydrerated India, pp. 60-63.

Fradin, M.S., Day, J.F., 2002. Comparative efficacy of insect repellents against mosquito bites. N. Engl. J. Med. 34, 13-18.

Ganesan, K., Xu, B., 2017. Ethnobotanical studies on folkloric medicinal plants in Nainamalai, Namakkal District, Tamil Nadu, India. Trends Phytochem. Res. 1(3), 153-168.

Govindarajan, M., Rajeswary, M., Hoti, S.L., Bhattacharyya, A., Benelli, G., 2016. Eugenol, α-pinene and β-caryophyllene from Plectranthus barbatus essential oil as eco-friendly larvicides against malaria, dengue and Japanese encephalitis mosquito vectors. Parasitol. Res. 115(2), 807-815.

Hajhashemi, V., Ghannadi, A., Jafarabadi, H., 2004. Black cumin seed essential oil, as a potent analgesic and antiinflammatory drug. Phytother. Res. 18(3), 195-199.

Haseena, S., Aithal, M., Das, K.K., Saheb, S.H., 2015. Phytochemical analysis of Nigella sativa and its effect on reproductive system. JPSR 7(8), 514-517.

Haselton, A.T., Aceved,o A., Kuruvilla, J., Werner, E., Kiernan, J., Dhar, P., 2015. Repellency of α-pinene against the house fly, Musca domestica. Phytochemistry 117, 469-475.

Keziah, E.A., Nukenine, E.N., Danga, S.P.Y., Younoussa, L., Esimone, C.O., 2015. Creams formulated with Ocimum gratissimum L. and Lantana camara L. crude extracts and fractions as mosquito repellents against Aedes aegypti L. (Diptera: Culicidae). J. Insect. Sci. 5(1), 45-49.

Kokoska, L., Havlik, J., Valterova, I., Sovova, H., Sajfrtova, M., Jankovska, I., 2008. Comparison of chemical composition and antibacterial activity of Nigella sativa seed essential oils obtained by different extraction methods. J. Food Prot. 71 (12), 2475-2480.

Lutz, A., Sfara, V., Alzogaray, R.A., 2014. Repellence produced by monoterpenes on rhodnius prolixus (Hemiptera: Reduviidae) decreases after continuous exposure to these compounds.  Insect Sci. 14, 1-6.

Maia, M.F., Moore, S.J., 2011. Plant-based insect repellents: a review of their efficacy, development and testing. Malaria J. 2011, 10 (Suppl 1), S1-S11.

Makenzi A.M., Manguro L.O.A, Owuor P.O., Opiyo S.A., 2019a. Flavonol glycosides with insecticidal activity from methanol extract of Annona mucosa Jacq. leave. Trends Phytochem. Res. 3(4), 287-296.

Makenzi, A.M., Manguro, L.A.O., Owuor, P.O., Opiyo, S.A., 2019b. Chemical constituents of Ocimum Kilimandscharicum Guerke acclimatized in Kakamega Forest, Kenya. Bull. Chem. Soc. Ethiopia 33(3), 527-539.

Manguro, L.O.A., Opiyo, S.A., Asefa, A., Dagne, E., Muchori, W.P., 2010. Chemical constituents of essential oils from three Eucalyptus species acclimatized in Ethiopia and Kenya. J. Essent. Oil. 13(5), 561-567.

Michelitsch, A., Rittmannsberger, A., Hufner, A., Ruckert, U., Likussar, W.W., 2004. Determination of isopropyl methyl phenols in black seed oil by differential pulse voltammetry. Phytochem. Anal. 15, 320-324.

Mohammadhosseini, M., Venditti, A., Sarker, S.D., Nahar, L., Akbarzadeh, A., 2019. The genus Ferula: Ethnobotany, phytochemistry and bioactivities - A review. Ind. Crop Prod. 129, 350-394.

Mohammed, S.J., Amin, H.H.H., Aziz, S.B., Sha, A.M., Hassan, S., Aziz, J.M.A., Heshu, S., Rahman, H.S., 2019. Structural Characterization, antimicrobial activity, and in vitro cytotoxicity effect of black seed oil. Evid-Based. Compl. Alt. Med. 2019, 1-9.

Moretti, A., D’Antuono, F.L., Elementi, S., 2004. Essential oils of N. sativa L. and Nigella damascene L. seeds. J. Essent. Oil Res. 16, 182-183.

Mouwakeh, A., Radácsi, P., Pluhár, Zs., Németh Zámboriné, É., Muránszky, G. Mohácsi-Farkas, Cs., Kiskó, G., 2018. Chemical composition and antimicrobial activity of Nigella sativa crude and essential oil. Acta Aliment. 47(3), 379-386.

Mukai, A., Takahashi, K., Ashitani, T., 2017. Natural autoxidation of longifolene and anti-termite activities of the products. J. Wood. Sci. 63, 360-368.

NIST 2017. Wiley Registry 11th Edition/NIST 2017 Mass Spectral Library DVD-ROM ISBN: 978-1-119-41223-6.

Njoroge, P.W., Opiyo, S.A., 2019a. Some antibacterial and antifungal compounds from root bark of Rhus natalensis. Am. Res. J. Chem. 9(5), 150-158.

Njoroge, P.W., Opiyo, S.A., 2019b. Antimicrobial activity of root bark extracts of Rhus natalensisa and Rhus ruspolii. Basic Sci. Med. 8(2), 23-28.

Nunes, H.S., Miguel, M.G., 2017. Rosa damascena essential oils: a brief review about chemical composition and biological properties. Trends Phytochem. Res. 1(3), 111-128.

Ochieng, C.O., Ishola, I., Opiyo, S.A., Manguro, L.O.A., Owuor, P.O., Wong, K.C., 2013. Phytoecdysteroids from the stem bark of Vitex doniana and their anti-inflammatory effects. Plant Medica 79, 52-59.

Ochieng, C.O., Opiyo, S.A., Mureka, E.W., Ishola, I.O., 2017. Cyclooxygenase inhibitory compounds from Gymnosporia heterophylla aerial parts. Fitoterapia 119, 168-174.

Ochung, A.A., Manguro, L.A.O., Owuor, P.O., Jondiko, I.O., Nyunja, R.A., Akala, H., Mwinzi, P., Opiyo, S.A., 2015. Bioactive carbazole alkaloids from Alysicarpus ovalifolius (Schumach). J. Korean Soc. Appl. Biol. Chem. 58(6), 839-846.

Ochung, A.A., Owuor, P.O., Manguro, L.A.O., Ishola, O.I., Nyunja, R.A., Ochieng, C.O., Opiyo, S.A., 2018. Analgesics from Lonchocarpus eriocalyx Harms. Trends Phytochem. Res. 2(4), 253-260.

Ogbonnia, U.O., Udu, I.A., Okorocha, E.A., Grace, O., Onwuchekwa, O., 1990. The effect of pyrethroid-based insecticides (rambo and raid mosquito coil) smoke on some biochemical indices in albino rats and the protective effect of aqueous extract of piper guineense. Middle East J. Sci Res. 24, 306-313.

Omolo, D.M., Okinyo, D., Ndiege, O.J., Lwade, W., Hassanali, A., 2004. Repellency of essential oils of some Kenyan plants against Anopheles gambiae. Phytochemistry 65, 2798-2799.

Opiyo, S.A., 2019. A review of 13C NMR spectra of drimane sesquiterpenes. Trends Phytochem. Res. 3(3), 147-180.

Opiyo, S.A., Manguro, L.A.O., Akinyi, D., Ochung, A.A., Ochieng, C.O., 2015. Biopesticidal extractives and compounds from Warburgia Ugandensis against maize weevil (Sitophilus zeamais). Nat. Prod. J. 5(4), 236 -243.

Opiyo, S.A., Manguro, L.O.A., Okinda-Owuor, P., Ateka, E.M., Lemmen, P. 2011a. 7-alpha-Acetylugandensolide and antimicrobial properties of Warburgia ugandensis extracts and isolates against sweet potato pathogens. Phytochem. Lett. 4, 161-165.

Opiyo, S.A., Manguro, L.O.A., Owuor, P.O., Ochieng, C.O., Ateka, E.M., Lemmen, P., 2011b. Antimicrobial compounds from Terminalia brownii against sweet potato pathogens. Nat. Prod J. 1, 116-120.

Pandey, S.K., Upadhyay, S. Tripathi, A.K., 2000. Insecticidal and repellent activities of thymol from the essential oil of Trachyspermum ammi (Linn) Sprague seeds against Anopheles stephensi Parasitol. Res. 105, 507-512.

Raj, G.A., Chandrasekaran, M., Krishnamoorthy, S., Jayaraman, M., Venkatesalu, V., 2015. Phytochemical profile and larvicidal properties of seed essential oil from Nigella sativa L. (Ranunculaceae), against Aedes aegypti, Anopheles stephensi, and Culex quinquefasciatus (Diptera: Culicidae). Parasitol. Res. 114: 3385-3391.

Thollet, D., Boland, W., Hasel, A., Lorest, F., Rose, R., Schnitzler, J., 2006. Techniques for molecular analysis practical approaches to plant volatile analysis. Plant J. 45, 540-560.

Wajs, A., Radoslaw, B., Kalemba, D., 2008. Composition of essential oil from seeds of N. sativa L. cultivated in Poland. Flav. Frag. J. 23, 126-132.

Wansi, J.D., Sewald, N., Nahar, L., Martin, C., Sarker, S.D., 2018. Bioactive essential oils from the Cameroonian rain forest: A review - Part I. Trends Phytochem. Res. 2(4), 187-234.

Wansi, J.D., Sewald, N., Nahar, L., Martin, C., Sarker, S.D., 2019. Bioactive essential oils from the Cameroonian rain forest: A review - Part II. Trends Phytochem. Res. 3(1), 3-52.

WHO, 1996. Evaluation and testing of insecticides. Report of the WHO Informal Consultation, Geneva.

Omolo, D.M., Okinyo, D., Ndiege, O.J., Lwade, W., Hassanali, A., 2004. Repellency of essential oils of some Kenyan plants against Anopheles gambiae. Phytochemistry 65, 2798-2799.

WHO, 2015. World Malaria Report. Africa: WHO, pp. 45-78.

WHO, 2017. World Malaria Report. Africa: WHO, pp. 21-34.

Wijayanti, F., Naim, M., Sina, I., 2019. Analysis of black seed effect on Aedes aegyptii. Int. J. Zool. Res. 15(1), 13-20.

Yap, H.H., Jahangir, K., Chong, A.S., Adanam, C.R., Chong, N.L., Malik, Y.A., Rohaizat, B., 1998. Field efficacy of a new repellent, KBR 3023, against Aedes albopictus (Skuse) and Culex quicnquefasciatus (Say) in a tropical environment. J. Vector Ecol. 23, 62-68.