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Essential oils from Ocimum basilicum cultivars: analysis of their composition and determination of the effect of the major compounds on Haemonchus contortus eggs

Published online by Cambridge University Press:  22 March 2021

A.I.P. Sousa
Affiliation:
Laboratory of Plant Biochemistry, Federal University of Maranhão, São Luís, MA, Brazil
C.R. Silva
Affiliation:
Laboratory of Parasite Control, Federal University of Maranhão, São Luís, MA, Brazil
H.N. Costa-Júnior
Affiliation:
Laboratory of Parasite Control, Federal University of Maranhão, São Luís, MA, Brazil
N.C.S. Silva
Affiliation:
Laboratory of Parasite Control, Federal University of Maranhão, São Luís, MA, Brazil
J.A.O. Pinto
Affiliation:
Agronomy Department, Federal University of Sergipe, São Cristóvão, SE, Brazil
A.F. Blank
Affiliation:
Agronomy Department, Federal University of Sergipe, São Cristóvão, SE, Brazil
A.M.S. Soares
Affiliation:
Laboratory of Plant Biochemistry, Federal University of Maranhão, São Luís, MA, Brazil
L.M. Costa-Júnior*
Affiliation:
Laboratory of Parasite Control, Federal University of Maranhão, São Luís, MA, Brazil
*
Author for correspondence: L.M. Costa-Júnior, E-mail: livio.martins@ufma.br

Abstract

The continuous use of synthetic anthelmintics against gastrointestinal nematodes (GINs) has resulted in the increased resistance, which is why alternative methods are being sought, such as the use of natural products. Plant essential oils (EOs) have been considered as potential products for the control of GINs. However, the chemical composition and, consequently, the biological activity of EOs vary in different plant cultivars. The aim of this study was to evaluate the anthelmintic activity of EOs from cultivars of Ocimum basilicum L. and that of their major constituents against Haemonchus contortus. The EOs from 16 cultivars as well the pure compound linalool, methyl chavicol, citral and eugenol were used in the assessment of the inhibition of H. contortus egg hatch. In addition, the composition of three cultivars was simulated using a combination of the two major compounds from each. The EOs from different cultivars showed mean Inhibition Concentration (IC50) varying from 0.56 to 2.22 mg/mL. The cultivar with the highest egg-hatch inhibition, Napoletano, is constituted mainly of linalool and methyl chavicol. Among the individual compounds tested, citral was the most effective (IC50 0.30 mg/mL). The best combination of compounds was obtained with 11% eugenol plus 64% linalool (IC50 0.44 mg/mL), simulating the Italian Large Leaf (Richters) cultivar. We conclude that different cultivars of O. basilicum show different anthelmintic potential, with cultivars containing linalool and methyl chavicol being the most promising; and that citral or methyl chavicol isolated should also be considered for the development of new anthelmintic formulations.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Albuquerque, ACA, Bassetto, CC, Almeida, FA and Amarante, AFT (2017) Development of Haemonchus contortus resistance in sheep under suppressive or targeted selective treatment with monepantel. Veterinary Parasitology 246, 112117.CrossRefGoogle ScholarPubMed
Almeida, I, Alviano, DS, Vieira, DP, Alves, PB, Blank, AF, Lopes, AHCS, Alviano, CS and Rosa, MDSS (2007) Antigiardial activity of Ocimum basilicum essential oil. Parasitology Research 101, 443452.CrossRefGoogle ScholarPubMed
Andre, WPP, Ribeiro, WLC, Cavalcante, GS, et al. (2016) Comparative efficacy and toxic effects of carvacryl acetate and carvacrol on sheep gastrointestinal nematodes and mice. Veterinary Parasitology 218, 5258.CrossRefGoogle ScholarPubMed
Blank, AF, Souza, EM, Arrigoni-Blank, MDF, Paula, JWA and Alves, PB (2007) Maria Bonita: a linalool type basil cultivar. Pesquisa Agropecuária Brasileira 42, 18111813.CrossRefGoogle Scholar
Castilho, CVV, Fantatto, RR, Gaínza, YA, Bizzo, HR, Barbi, NS, Leitão, SG and Chagas, ACS (2017) In vitro activity of the essential oil from Hesperozygis myrtoides on Rhipicephalus (Boophilus) microplus and Haemonchus contortus. Brazilian Journal of Pharmacognosy 27, 7076.CrossRefGoogle Scholar
Castro, LM, Pinto, NB, Mota, TO, Moura, MQ, Castro, LLD, Madrid, IM, Freitag, RA and Berne, MEA (2017) Atividade ovicida do óleo essencial e do extrato hidroalcoólico de Ocimum basilicum sobre nematódeos gastrintestinais de ovinos. Science and Animal Health 5, 138150.CrossRefGoogle Scholar
Coles, GC, Bauer, C, Borgsteede, FHM, Geerts, S, Klei, TR, Taylor, MA and Waller, PJ (1992) 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. Veterinary Parasitology 44, 3544.CrossRefGoogle ScholarPubMed
Costa-Júnior, LM, Miller, RJ, Alves, PB, Blank, AF, Li, AY and Pérez de León, AA (2016) Acaricidal efficacies of Lippia gracilis essential oil and its phytochemicals against organophosphate-resistant and susceptible strains of Rhipicephalus (Boophilus) microplus. Veterinary Parasitology 228, 6064.CrossRefGoogle ScholarPubMed
Cruz, EM, Costa-Junior, LM, Pinto, JAO, et al. (2013) Acaricidal activity of Lippia gracilis essential oil and its major constituents on the tick Rhipicephalus (Boophilus) microplus. Veterinary Parasitology 195, 198202.CrossRefGoogle ScholarPubMed
El-Soud, NHA, Deabes, M, El-Kassem, LA and Khalil, M (2015) Chemical composition and antifungal activity of Ocimum basilicum L. essential oil. Open Access Macedonian Journal of Medical Sciences 3, 374379.CrossRefGoogle ScholarPubMed
FAO (2004) Resistance management and integrated parasite control in ruminants, Guidelines. Rome, Animal Production and Health Division, FAO, pp. 78118.Google Scholar
Ferreira, LE, Benincasa, BI, Fachin, AL, Contini, SHT, França, SC, Chagas, ACS and Beleboni, RO (2018) Essential oils of Citrus aurantifolia, Anthemis nobile and Lavandula officinalis: in vitro anthelmintic activities against Haemonchus contortus. Parasites & Vectors 11, 269.CrossRefGoogle ScholarPubMed
Garcia-Bustos, JF, Sleebs, BE and Gasser, RB (2019) An appraisal of natural products active against parasitic nematodes of animals. Parasites & Vectors 12, 122.CrossRefGoogle ScholarPubMed
Giachino, RRA, Tonk, CSFA, Bayram, E, Yuce, S, Telci, I and Furan, MA (2014) RAPD and essential oil characterization of Turkish basil (Ocimum basilicum L.). Plant Systematics and Evolution 300, 17791791.CrossRefGoogle Scholar
Govindarajan, M, Sivakumar, R, Rajeswary, M and Yogalakshmi, K (2013) Chemical composition and larvicidal activity of essential oil from Ocimum basilicum (L.) against Culex tritaeniorhynchus, Aedes albopictus and Anopheles subpictus (Diptera: Culicidae). Experimental Parasitology 134, 711.CrossRefGoogle Scholar
Güez, CM, de Souza, RO, Fischer, P, et al. (2017) Evaluation of basil extract (Ocimum basilicum L.) on oxidative, anti-genotoxic and anti-inflammatory effects in human leukocytes cell cultures exposed to challenging agents. Brazilian Journal of Pharmaceutical Sciences 53, e15098.CrossRefGoogle Scholar
Hassanpouraghdam, MB, Gohari, GR, Tabatabaei, SJ and Dadpour, MR (2010) Inflorescence and leaves essential oil composition of hydroponically grown Ocimum basilicum L. Journal of the Serbian Chemical Society 75, 13611368.CrossRefGoogle Scholar
Hierro, I, Valero, A and Navarro, MC (2006) In vivo larvicidal activity of monoterpenic derivatives from aromatic plants against L3 larvae of Anisakis simplex s.l. Phytomedicine 13, 527531.CrossRefGoogle ScholarPubMed
Katiki, LM, Chagas, ACS, Takahira, RK, Juliani, HR, Ferreira, JFS and Amarante, AFT (2012) Evaluation of Cymbopogon schoenanthus essential oil in lambs experimentally infected with Haemonchus contortus. Veterinary Parasitology 186, 312318.CrossRefGoogle ScholarPubMed
Katiki, LM, Barbieri, AME, Araujo, RC, Veríssimo, CJ, Louvandini, H and Ferreira, JFS (2017) Synergistic interaction of ten essential oils against Haemonchus contortus in vitro. Veterinary Parasitology 243, 4751.CrossRefGoogle ScholarPubMed
Khair, S, Bariyah, U, Khair-Ul-Bariyah, S, Ahmed, D and Ikram, M (2012) Ocimum basilicum: a review on phytochemical and pharmacological studies. Pakistan Journal of Chemistry 2, 7885.CrossRefGoogle Scholar
Kiferle, C, Ascrizzi, R, Martinelli, M, Gonzali, S, Mariotti, L, Pistelli, L, Flamini, G and Perata, P (2019) Effect of iodine treatments on Ocimum basilicum L.: biofortification, phenolics production and essential oil composition. PLoS One 14, e0226559.CrossRefGoogle ScholarPubMed
Kotze, AC, Hunt, PW, Skuce, P, et al. (2014) Recent advances in candidate-gene and whole-genome approaches to the discovery of anthelmintic resistance markers and the description of drug/receptor interactions. International Journal for Parasitology: Drugs Drug Resistance 4, 164184.Google ScholarPubMed
Lacey, E, Brady, RL, Prichard, RK and Watson, TR (1987) Comparison of inhibition of polymerisation of mammalian tubulin and helminth ovicidal activity by benzimidazole carbamates. Veterinary Parasitology 23, 105119.CrossRefGoogle ScholarPubMed
Lane, J, Jubb, T, Shephard, R, Webb-Ware, J and Fordyce, GLA (2015) Final report: priority list of endemic diseases for the red meat industries. 282 pp. Sydney, Australia, Meat and Livestock Australia.Google Scholar
Lang, G and Buchbauer, G (2012) A review on recent research results (2008-2010) on essential oils as antimicrobials and antifungals. A review. Flavour and Fragrance Journal 27, 1339.CrossRefGoogle Scholar
Lawrence, BM (1992) Chemical components of labiatae oils and their exploitation. pp. 399–436 in Harley, RM and Reynolds, T (Eds) Advances in labiate science. Kew, Royal Botanic Gardens.Google Scholar
Liber, Z, Stanko, KJ, Politeoc, O, Strikic, F, Kolakb, I, Milosc, M and Satovicb, Z (2011) Chemical characterization and genetic relationships among Ocimum basilicum L. cultivars. Chemistry & Biodiversity 8, 19781989.CrossRefGoogle ScholarPubMed
Lima, A, Carvalho, JF, Peixoto, MG, Blank, AF, Borges, LM and Costa Junior, LM (2016) Assessment of the repellent effect of Lippia alba essential oil and major monoterpenes on the cattle tick Rhipicephalus microplus. Medical and Veterinary Entomology 30, 7377.CrossRefGoogle Scholar
Macedo, ITF, Oliveira, LMB, André, WPP, et al. (2019) Anthelmintic effect of Cymbopogon citratus essential oil and its nanoemulsion on sheep gastrointestinal nematodes. Revista Brasileira de Parasitologia Veterinária 28, 522527.CrossRefGoogle ScholarPubMed
Mandelkow, E and Mandelkow, EM (1990) Microtubular structure and tubulin polymerization. Current Opinion in Cell Biology 2, 39.CrossRefGoogle ScholarPubMed
Martinez-Velazquez, M, Castillo-Herrera, GA, Rosario-Cruz, R, Flores-Fernandez, JM, Lopez-Ramirez, J, Hernandez-Gutierrez, R and Del Carmen Lugo-Cervantes, E (2011) Acaricidal effect and chemical composition of essential oils extracted from Cuminum cyminum, Pimenta dioica and Ocimum basilicum against the cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Parasitology Research 108, 481487.CrossRefGoogle Scholar
Martins, AGLA, Nascimento, AR, Filho, JEM, Filho, NEM, Souza, AG, Aragão, NE and Silva, DSV (2010) Atividade antibacteriana do óleo essencial do manjericão frente a sorogrupos de Escherichia coli enteropatogênica isolados de alfaces. Ciencia Rural 40, 17911796.CrossRefGoogle Scholar
Nieuwhof, GJ and Bishop, SC (2005) Costs of the major endemic diseases of sheep in Great Britain and the potential benefits of reduction in disease impact. Animal Science 81, 2329.CrossRefGoogle Scholar
Ottai, MES, Ahmed, SS and El Din, MM (2012) Genetic variability among some quantitative characters, insecticidal activity and essential oil composition of two Egyptian and French sweet basil varieties. Australian Journal of Basic and Applied Sciences 6, 185192.Google Scholar
Pascual-Villalobos, MJ and Ballesta-Acosta, MC (2003) Chemical variation in an Ocimum basilicum germplasm collection and activity of the essential oils on Callosobruchus maculatus. Biochemical Systematics and Ecology 31, 673679.CrossRefGoogle Scholar
Peixoto, MG, Costa-Júnior, LM, Blank, AF, et al. (2015) Acaricidal activity of essential oils from Lippia alba genotypes and its major components carvone, limonene, and citral against Rhipicephalus microplus. Veterinary Parasitology 210, 118122.CrossRefGoogle ScholarPubMed
Pinto, JAO, Blank, AF, Nogueira, PCL, Arrigoni-Blank, MF, Andrade, TM, Sampaio, TS and Pereira, KLG (2019) Chemical characterization of the essential oil leaves of basil genotypes cultivated in different seasons. Boletín Latinoamericano y del Caribe de Plantas Medicinais y Aromaticas 18, 5870.CrossRefGoogle Scholar
Ravid, U, Putievsky, E, Katzir, I and Lewinsohn, E (1997) Enantiomeric composition of linalool in the essential oils of Ocimum species and in commercial basil oils. Flavour and Fragrance Journal 12, 293296.3.0.CO;2-3>CrossRefGoogle Scholar
Robert, FHS and O'Sullivan, PJ (1950) Methods for egg counts and larvae cultures for strongyles infecting. Australian Journal of Agricultural Research 1, 299.Google Scholar
Rodríguez-González, Á, Álvarez-García, S, González-López, Ó, Silva, F and Casquero, PA (2019) Insecticidal properties of Ocimum basilicum and Cymbopogon winterianus against Acanthoscelides obtectus, insect pest of the common bean (Phaseolus vulgaris, L.). Insects 10, 151.CrossRefGoogle Scholar
Rodríguez, AV, Goldberg, V, Viotti, H and Ciappesoni, G (2015) Early detection of Haemonchus contortus infection in sheep using three different faecal occult blood tests. Open Veterinary Journal 5, 9097.Google ScholarPubMed
Sajjadi, SE (2006) Analysis of the essential oils of two cultivated basil (Ocimum basilicum L.) from Iran. Daru – Journal of Faculty of Pharmacy 14, 128130.Google Scholar
Santoro, GF, Cardoso, MG, Guimarães, LGL, Mendonça, LZ and Soares, MJ (2007) Trypanosoma cruzi: activity of essential oils from Achillea millefolium L., Syzygium aromaticum L. and Ocimum basilicum L. on epimastigotes and trypomastigotes. Experimental Parasitology 116, 283290.CrossRefGoogle Scholar
Sharopov, FS, Satyal, P, Ali, NAA, Pokharel, S, Zhang, H, Wink, M, Kukaniev, MA and Setzer, WN (2016) The essential oil compositions of Ocimum basilicum from three different regions: Nepal, Tajikistan, and Yemen. Chemistry & Biodiversity 13, 241248.CrossRefGoogle ScholarPubMed
Silva, VA, Sousa, JP, Guerra, FQS, Pessôa, HLF, Freitas, AFR, Alves, LBN and Lima, EO (2015) Antibacterial activity of Ocimum basilicum essential oil and linalool on bacterial isolates of clinical importance. International Journal of Pharmacognosy and Phytochemical Research 7, 10661071.Google Scholar
Silva, CR, Lifschitz, AL, Macedo, S, Campos, N, Viana-Filho, M, Alcântara, A, Araújo, JG, Alencar, L and Costa-Junior, LM (2021) Combination of synthetic anthelmintics and monoterpenes: assessment of efficacy, and ultrastructural and biophysical properties of Haemonchus contortus using atomic force microscopy. Veterinary Parasitology 290, 109345.CrossRefGoogle ScholarPubMed
Soares, AMS, Penha, TA, Araújo, SA, Cruz, EMO, Blank, AF and Costa-Júnior, LM (2016) Assessment of different Lippia sidoides genotypes regarding their acaricidal activity against Rhipicephalus (Boophilus) microplus. Revista Brasileira de Parasitologia Veterinária 25, 401406.CrossRefGoogle ScholarPubMed
Telci, I, Bayram, E, Yilmaz, G and Avci, B (2006) Variability in essential oil composition of Turkish basils (Ocimum basilicum L.). Biochemical Systematics and Ecology 34, 489497.CrossRefGoogle Scholar
Van Wyk, JA and Mayhew, E (2013) Morphological identification of parasitic nematode infective larvae of small ruminants and cattle: a practical lab guide. Onderstepoort Journal of Veterinary Research 80, 539.CrossRefGoogle ScholarPubMed
Vieira, RF and Simon, JE (2000) Chemical characterization of basil (Ocimum spp.) found in the markets and used in traditional medicine in brazil. Economic Botany 54, 207216.CrossRefGoogle Scholar
Yang, L, Wen, KS, Ruan, X, Zhao, YX, Wei, F and Wang, Q (2018) Response of plant secondary metabolites to environmental factors. Molecules 23, 762.CrossRefGoogle ScholarPubMed