In vitro activity of the essential oil from Hesperozygis myrtoides on Rhipicephalus (Boophilus) microplus and Haemonchus contortus

Abstract

Commercial antiparasitics have been the main tool to control parasites, but due to the resistance development, plant extracts have been widely investigated to find new molecules. The present study aimed to investigate the in vitro acaricide and anthelmintic activities of the essential oil from the aerial parts of Hesperozygis myrtoides (A.St.-Hil. ex Benth.) Epling, Lamiaceae. The essential oil was obtained by hydrodistillation analyzed by GC-FID and GC-MS. Four tests were conducted in vitro to screen the antiparasitic action of the essential oil. The evaluation on Rhipicephalus (Boophilus) microplus was performed with the adult immersion test at concentrations ranging from 0.391 to 25 mg/ml and the larval packet test from 3.125 to 100 mg/ml. For Haemonchus contortus the egg hatch test was performed from 0.012 to 25 mg/ml and the larval development test from 0.003 to 0.4 mg/ml. The LC50 and LC90 values were calculated by Probit. The main components identified in the essential oil were isomenthone (47.7%), pulegone (21.4%), limonene (7.7%), isomenthyl acetate (6.8%) and neoisomenthol (3.9%). In the larval packet test the LC50 and LC90 were 13.5 and 21.8mg/ml, respectively. In egg hatch test, the LC50 and LC90 were 0.249 and 0.797mg/ml, respectively, while in the larval development test were 0.072 and 0.167 mg/ml, respectively. This is the first report of the H. myrtoides evaluation against those parasites. The anthelmintic results proved its efficacy on H. contortus encouraging new research with a focus on their main bioactives.

References

  1. Adams, R.P., 2007. Identification of Essential oils Components by Gas Chromatography/Mass Spectrometry. Allured Publishing Corporation, Illinois.

    Google Scholar 

  2. Achi, Y.L., Zinsstag, J., Yao, K., Yeo, N., Dorchies, P., Jacquiet, P., 2003. Host specificity of Haemonchus spp. for domestic ruminants in the savanna in northern Ivory Coast. Vet. Parasitol. 116, 151–158.

    CAS  PubMed  Google Scholar 

  3. Alves, W.V., Lorenzetti, E.R., Goncalves, F.C., 2012. Utilização de acaricidas a base de plantas no controle de Rhipicephalis (Boophilus) microplus: uma contribuição para a produção e desenvolvimento sustentável. RBAS 2, 14–25.

    Google Scholar 

  4. Amer, S.A.A., Mohamed, F.S.A., Kamel, A.M., Darwish, Z.E.A., Hussein, H.E., El-Desouky, M.E., 2011. Acaricidal activity of some Lamiaceae plant essential oils against Tetranychus urticae Koch. J. Egypt. Soc. Acarol. 5, 11–17.

    Google Scholar 

  5. Apel, M.A., Ribeiro, V.L.S., Bordignon, S.A.L., Henriques, A.T., Von Poser, G., 2009. Chemical composition and toxicity of the essential oils from Cunila species (Lamiaceae) on the cattle tick Rhipicephalus (Boophilus) microplus. Parasitol. Res. 105, 863–868.

    PubMed  Google Scholar 

  6. Araújo, L.X., Novato, T.P.L., Zeringota, V., Matos, R.S., Senra, T.O.S., Maturano, R., Prata, M.C.A., Daemon, E., Monteiro, C.M.O., 2015. Acaricidal activity of thymol against larvae of Rhipicephalus microplus (Acari: Ixodidae) under semi-natural conditions. Parasitol. Res. 114, 3271–3276.

    PubMed  Google Scholar 

  7. Beati, L., Keirans, J.E., 2001. Analysis of the systematic relationships among ticks of the genera Rhipicephalus and Boophilus (Acari: Ixodidae) based on mitochondrial 12S ribosomal DNAgene sequences and morphological characters. J. Parasitol. 87, 32–48.

    CAS  PubMed  Google Scholar 

  8. Bianchi, M.W., Barré, N., Messad, S., 2003. Factors related to cattle infestation level and resistance to acaricides in Boophilus microplus tick populations in New Caledonia. Vet. Parasitol. 112, 75–89.

    CAS  PubMed  Google Scholar 

  9. Carvalho, C.O., Chagas, A.C.S., Cotinguiba, F., Furlan, M., Brito, L.G., Chaves, F.C.M., Stephan, M.P., Bizzo, H.R., Amarante, A.F.T., 2012. The anthelmintic effect of plant extracts on Haemonchus contortus and Strongyloides venezuelensis. Vet. Parasitol. 83, 260–268.

    Google Scholar 

  10. Castilho, C.V.V., Bizzo, H.R., Santos, M.C.S., Barbi, N.S., Dias, J.C.M., Aguiar, P.F., Dellacassa, E., Martinez, N., Pinto, S.C., Leitão, S.G., 2016. Evaluation of the chemical composition of the essential oil from Brazilian Poejo. Hesperozygis myrtoides (St. Hill. ex Benth.) Epling at different collection periods and sites. J. Essen. Oil Res. 28, https://doi.org/10.1080/10412905.2015.1133459.

  11. Chagas, A.C.S., Passos, W.M., Prates, H.T., Leite, R.C., Furlong, J., Fortes, I.C.P., 2002. Efeito acaricida de óleos essenciais e concentrados emulsionáveis de Eucalyptus spp. em Boophilus microplus. Braz. J. Vet. Res. Anim. Sci. 39, 247–253.

    Google Scholar 

  12. Chagas, A.C.S., De Barros, L.D., Cotinguiba, F., Furlan, M., Giglioti, R., Oliveira, M.C.S., Bizzo, H.R., 2012. In vitro efficacy of plant extracts and synthesized substances on Rhipicephalus (Boophilus) Microplus (Acari: Ixodidae). J. Parasitol. Res. 110, 295–303.

    Google Scholar 

  13. Chagas, A.C.S., Domingues, L.F., Fantatto, R.R., Giglioti, R., Oliveira, M.C.S., Oliveira, D.H., Mano, R.A., Jacob, R.G., 2014. In vitro and in vivo acaricide action of juvenoid analogs produced from the chemical modification of Cymbopogon spp. and Corymbia citriodora essential oil on the cattle tick Rhipicephalus (Boophilus) microplus. Vet. Parasitol. 205, 277–284.

    CAS  PubMed  Google Scholar 

  14. Chagas, A.C.S., Katiki, L.M., Silva, I.C., Giglioti, R., Esteves, S.N., Oliveira, M.C.S., Barioni Júnior, W., 2013. Haemonchus contortus: a multiple-resistant Brazilian isolate and the costs for its characterization and maintenance for research use. Parasitol. Int. 62, 1–6.

    PubMed  Google Scholar 

  15. Chagas, A.C.S., Niciura, S.C.N., Molento, M.B., 2011. Manual prático: Metodologias de diagnóstico da resistência e de deteccão de substâncias ativas em parasitas de ruminantes. Embrapa Informacão Tecnológica, Brasília.

    Google Scholar 

  16. Coles, G.C., 2005. Anthelmintic resistance - looking to the future: a UK perspective. Res. Vet. Sci. 78, 99–108.

    CAS  PubMed  Google Scholar 

  17. Coles, G.C., Bauer, C., Borgsteede, F.H.M., Geerts, S., Klei, T.R., Taylor, M.A., Waller, P.J., 1992. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods forthe detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 44, 35–44.

    CAS  PubMed  Google Scholar 

  18. Cowan, M.M., 1999. Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12, 564–582.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Cox, S.D., Mann, C.M., Markham, J.L., Bell, H.C., Gustafson, J.E., Warmingtn, J.R., Wyllic, S.G., 2000. The mode of antimicrobial action of essential oils of Melaleuca alternifolia (teatree oil). J. Appl. Microbiol. 88, 170–175.

    CAS  PubMed  Google Scholar 

  20. Cruz, E.M.O., Costa-Junior, L.M., Pinto, J.A.O., Santos, D.A., Araujo, S.A., Arrigoni-Blank, M.F., Bacci, L., Alves, P.B., Cavalcanti, S.C.H., Blank, A.F., 2013. Acaricidal activity ofLippia gracilis essential oil and its major constituents on the tick Rhipicephalus (Boophilus) microplus. Vet. Parasitol. 195, 198–202.

    PubMed  Google Scholar 

  21. Drummond, R.O., Ernest, S.E., Trevino, J.L., Gladney, W.J., Graham, O.H., 1973. Boophilus annulatus and Boophilus microplus: laboratory tests for insecticides. J. Econ. Entomol. 66, 130–133.

    CAS  PubMed  Google Scholar 

  22. Facey, P.C., Porter, R.B.R., Reese, P.B., Williams, L.A.D., 2005. Biological activity and chemical composition of the essential oil from Jamaican Hyptis verticillata Jacq. J. Agric. Food Chem. 53, 4774–4777.

    CAS  PubMed  Google Scholar 

  23. FAO Protection Bulletin, 1971. Recommended methods forthe detection and measurement of resistance of agricultural pests to pesticides. Tentative method for larvae of cattle ticks, Boophilus spp. FAO Method 19, 15–18.

    Google Scholar 

  24. Ferrarini, S.R., Duarte, M.O., Rosa, R.G., Rolim, V., Eifler-Lima, V.L., Von Poser, G., Ribeiro, V.L.S., 2008. Acaricidal activity of limonene, limonene oxide and b-amino alcohol derivatives on Rhipicephalus (Boophilus) microplus. Vet. Parasitol. 157, 149–153.

    CAS  PubMed  Google Scholar 

  25. Ferreira, L.E., Castro, P.M.N., Chagas, A.C.S., Franca, S.C., Beleboni, R.O., 2013. In vitro anthelmintic activity of aqueous leaf extract of Annonamuricata L. (Annonaceae) against Haemonchus contortus from sheep. Exp. Parasitol. 134, 327–332.

    CAS  PubMed  Google Scholar 

  26. Geary, T.G., Sangster, N.C., Thompson, D.P., 1999. Frontiers in anthelmintic pharmacology. Vet. Parasitol. 84, 275–295.

    CAS  PubMed  Google Scholar 

  27. Grisi, L., Leite, R.C., Martins, J.R.S., Barros, A.T.M., Andreotti, R., Cançado, P.H.D., Perez De León, A.A., Pereira, J.B., Villela, H.S., 2014. Reassessment of the potential economic impact of cattle parasites in Brazil. Braz. J. Vet. Parasitol. 23, 150–156.

    Google Scholar 

  28. Hubert, J., Kerboeuf, D., 1992. A microlarval development assay forthe detection of anthelmintic resistance in sheep nematodes. Vet. Rec. 130, 442–446.

    CAS  PubMed  Google Scholar 

  29. Jacquiet, P., Cabaret, J., Cheikh, D., Thiam, E., 1997. Identification of Haemonchus species in domestic ruminants based on morphometrics of spicules. Parasitol. Res. 83, 82–86.

    CAS  PubMed  Google Scholar 

  30. Jacquiet, P., Cabaret, J., Thiam, E., Cheikh, D., 1998. Host range and the maintenance of Haemonchus spp. in an adverse arid climate. Int. J. Parasitol. 28, 253–261.

    CAS  PubMed  Google Scholar 

  31. Jeon, J.H., Lee, H.S., 2011. Acaricidal activity of Tabebuia impetiginosa bark-derived constituent against domestic and spider mites (Arachnida: Acari). J. Korean Soc. Appl. Biol. Chem. 54, 551–557.

    CAS  Google Scholar 

  32. Kamaraj, C., Rahuman, A.A., 2011. Efficacy of anthelmintic properties of medicinal plant extracts against Haemonchus contortus. Res. Vet. Sci. 91, 400–404.

    CAS  PubMed  Google Scholar 

  33. Katiki, L.M., Chagas, A.C.S., Bizzo, H.R., Ferreira, J.F.S., Amarante, A.F.T., 2011. Anthelmintic activity of Cymbopogon martinii, Cymbopogon schoenanthus and Mentha piperita essential oils evaluated in four different in vitro tests. Vet. Parasitol. 183, 103–108.

    CAS  PubMed  Google Scholar 

  34. Koc, S., Oz, E., Cinbilgel, I., Aydin, L., Cetin, V., 2013. Acaricidal activity of Origanum bilgeri P.H Davis (Lamiaceae) essential oil and its major component, carvacrol against adults Rhipicephalus turanicus (Acari: Ixodidae). Vet. Parasitol. 193, 316–319.

    CAS  PubMed  Google Scholar 

  35. Lage, T.C.A., Montanari, R.M., Fernandes, S.A., Monteiro, C.M.O., Senra, T.O.S., Zeringota, V., Calmon, F., Matos, R.S., Daemon, E., 2013. Activity of essential oil of Lippia triplinervis Gardner (Verbenaceae) on Rhipicephalus microplus (Acari: Ixodidae). Parasitol. Res. 112, 863–869.

    PubMed  Google Scholar 

  36. Learmount, J., Stephens, N., Boughtflower, V., Barrecheguren, A., Rickell, K., Massei, G., Taylor, M., 2016. Three-year evaluation of best practice guidelines for nematode control on commercial sheep farms in the UK. Vet. Parasitol. 226, 116–123.

    PubMed  Google Scholar 

  37. Lopez-Arias, A., Villar-Argaiz, D., Chaparro-Gutierrez, J.J., Miller, R.J., Perez de Leon, A.A., 2014. Reduced efficacy of commercial acaricides against populations of resistant cattle tick Rhipicephalus microplus from two municipalities of Antio-quia, Colombia. Environ. Health Insights 8, 71–80.

    PubMed  Google Scholar 

  38. Marie-Magdeleine, C., Hoste, H., Mahieu, M., Varo, H., Archimede, H., 2009. In vitro effects of Cucurbita moschata seed extracts on Haemonchus contortus. Vet. Parasitol. 161, 99–105.

    CAS  PubMed  Google Scholar 

  39. Martinez-Velazquez, M., Rosario-Cruz, R., Castillo-Herrera, G., Flores-Fernandez, J.M., Alvarez, A.H., Lugo-Cervantes, E., 2011. Acaricidal effect of essential oils from Lippia graveolens (Lamiales: Verbenaceae), Rosmarinus officinalis (Lamiales: Lamiaceae), and Allium sativum (Liliales: Liliaceae) against Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). J. Med. Entomol. 48, 822–827.

    CAS  PubMed  Google Scholar 

  40. Martini, M.G., Bizzo, H.R., Moreira, D.L., Neufeld, P.M., Miranda, S.N., Alviano, C.S., Alviano, D.S., Leitão, S.G., 2011. Chemical composition and antimicrobial activities of the essential oils from Ocimum selloi and Hesperozygis myrtoides. Nat. Prod. Commun. 6, 1027–1030.

    CAS  PubMed  Google Scholar 

  41. Molefe, N.I., Tsotetsi, A.M., Ashafa, A.O.T., Thekisoe, O.M.M., 2012. In vitro anthelmintic effects of Artemisia afra and Mentha longifolia against parasitic gastrointestinal nematodes of livestock. Bangladesh J. Pharmacol. 7, 157–163.

    Google Scholar 

  42. Monteiro, C.M.O., Daemon, E., Silva, A.M.R., Maturano, R., Amaral, C., 2010. Acaricide and ovicide activities of thymol on engorged females and eggs of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Parasitol. Res. 106, 615–619.

    Google Scholar 

  43. Murrell, A., Barker, S.C., 2003. Synonymy of Boophilus Curtice, 1891 with Rhipicephalus Koch, 1844 (Acari: Ixodidae). Syst. Parasitol. 56, 169–172.

    PubMed  Google Scholar 

  44. Paraud, C., Marcotty, T., Lespine, A., Sutra, J.F., Pors, I., Devos, I., 2016. Cross-resistance to moxidectin and ivermectin on a meat sheep farm in France. Vet. Parasitol. 226, 88–92.

    CAS  PubMed  Google Scholar 

  45. Peixoto, M.G., Costa-Júnior, L.M., Blank, A.F., Lima, A.S., Menezes, T.S.A., Santos, D.A., Alves, P.B., Cavalcanti, S.C.H., Bacci, L., Arrigoni-Blank, M.F., 2015. Acaricidal activity of essential oils from Lippia alba genotypes and its major components carvone, limonene, and citral against Rhipicephalus microplus. Vet. Parasitol. 210, 118–122.

    CAS  PubMed  Google Scholar 

  46. Porter, R.B.R., Reese, P.B., Williams, L.A.D., Williams, D.J., 1995. Acaricidal and insecticidal activities of cadina-4,10(15)-dien-3-one. Phytochemistry 40, 735–738.

    CAS  PubMed  Google Scholar 

  47. Prates, H.T., Leite, R.C., Craveiro, A.A., Oliveira, A.B., 1998. Identification of some chemical components of the essential oil from Molasses Grass (Melinis minutiflora Beauv.) and their activity against cattle tick (Boophilus microplus). J. Braz. Chem. Soc. 9, 193–197.

    CAS  Google Scholar 

  48. Ribeiro, V.L.S., Santos, J.C., Bordignon, S.A.L., Apel, M.A., Henriques, A.T., Von Poser, G.L., 2010. Acaricidal properties of the essential oil from Hesperozygis ringens (Lamiaceae) on the cattle tick Riphicephalus (Boophilus) microplus. Bioresour. Technol. 101, 2506–2509.

    CAS  PubMed  Google Scholar 

  49. Rodríguez, A.V., Goldberg, V., Viotti, H., Ciappesoni, G., 2015. Early detection of Haemonchus contortus infection in sheep using three different faecal occult blood tests. Open Vet. J. 5, 90–97.

    PubMed  PubMed Central  Google Scholar 

  50. Rosado-Aguilar, J.A., Aguilar-Caballero, A., Rodriguez-Vivas, R.I., Borges-Argaez, R., Garcia-Vazquez, Z., Mendez-Gonzalez, M., 2010. Acaricidal activity of extracts from Petiveria alliacea (Phytolaccaceae) against the cattle tick, Rhipicephalus (Boophilus) microplus (Acari: ixodidae). Vet. Parasitol. 168, 299–303.

    CAS  PubMed  Google Scholar 

  51. Rose, H., Rinaldi, L., Bosco, A., Mavrot, F., de Waal, T., Skuce, P., Charlier, J., Torgerson, P.R., Hertzberg, H., Hendrickx, G., Vercruysse, J., Morgan, E.R., 2015. Widespread an the lmintic resistance in European farmed ruminants: a systematic review. Vet. Rec. 176, 546.

    CAS  PubMed  Google Scholar 

  52. Sangster, N.C., 1999. Anthelmintic resistance: past, present and future. Int. J. Parasitol. 29, 115–124.

    CAS  PubMed  Google Scholar 

  53. Sangster, N.C., 2001. Managing parasiticide resistance. Vet. Parasitol. 98, 89–109.

    CAS  PubMed  Google Scholar 

  54. SAS Statistical Analyses System, 2002/2010. SAS/Insight User’s Guide. Version 9.1.3. for Windows. SAS Institute, Cary NC.

    Google Scholar 

  55. SAS Institute Inc., 2002-2010. SAS for Windows 9.3, Cary, NC

    Google Scholar 

  56. Scoralik, M.G., Daemon, E., Monteiro, C.M.O., Maturano, R., 2012. Enhancing the acaricide effect of thymol on larvae of the cattle tick Rhipicephalus microplus (Acari: Ixodidae) by solubilization in ethanol. Parasitol. Res. 110, 645–648.

    PubMed  Google Scholar 

  57. Sikkema, J., Bont, J.A.M., Poolman, B., 1993. Interactions of cyclic hydrocarbons with biological membranes. J. Biol. Chem. 269, 8022–8028.

    Google Scholar 

  58. Sikkema, J., Bont, J.A.M., Poolman, B., 1995. Mechanisms of membrane toxicity of hydrocarbons. Microbiol. Rev. 59, 201–222.

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Sudekum, M.R.H., Poppenga, N., Raju, N., Braselton, W.E., 1992. Pennyroyal oil toxicosis in a dog. J. Am. Vet. Med. Assoc. 200, 817–818.

    CAS  PubMed  Google Scholar 

  60. Sztajnkrycer, M.D., Otten, E.J., Bond, G.R., Lindsell, C.J., Goetz, R.J., 2003. Mitigation of pennyroyal oil hepatotoxicity in the mouse. Acad. Emerg. Med. 10, 1024–1028.

    PubMed  Google Scholar 

  61. Tak, J.H., Kim, H.K., Lee, S.H., Ahn, Y.J., 2006. Acaricidal activities of paeonol and benzoic acid from Paeonia suffruticosa root bark and monoterpenoids against Tyrophagusputrescentiae (Acari: Acaridae). Pest Manag. Sci. 62, 551–557.

    CAS  PubMed  Google Scholar 

  62. Valente, P.P., Amorim, J.M., Castilho, R.O., Leite, R.C., Ribeiro, M.F.B., 2014. In vitro acaricidal efficacy of plant extracts from Brazilian flora and isolated substances against Rhipicephalus microplus (Acari: Ixodidae). Parasitol. Res. 113, 417–423.

    PubMed  Google Scholar 

  63. Várady, M., Corba, J., Letková, V., Kovác, G., 2009. Comparison oftwo versions of larval development test to detect anthelmintic resistance in Haemonchus contortus. Vet. Parasitol. 160, 267–271.

    PubMed  Google Scholar 

  64. 1994. Wiley Registry of Mass Spectral Data. Wiley Interscience, New York.

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ana Carolina S. Chagas.

Additional information

Authors’ contributions

CVVC extracted the essential oil and drafted the paper. RRF, YAG performed the bioassay work and HRB performed GC analyses. NSB, SGL participated in the results, discussion and writing the paper. ACSC organized data, set statistical analyses and the manuscript final writing.

Rights and permissions

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Castilho, C.V.V., Fantatto, R.R., Gaínza, Y.A. et al. In vitro activity of the essential oil from Hesperozygis myrtoides on Rhipicephalus (Boophilus) microplus and Haemonchus contortus. Rev. Bras. Farmacogn. 27, 70–76 (2017). https://doi.org/10.1016/j.bjp.2016.08.005

Download citation

Keywords

  • Phytotherapy
  • Medicinal plants
  • Essential oils
  • Pulegone
  • Acaricides
  • Anthelmintics