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In vitro and ex vivo activity of Melaleuca alternifolia against protoscoleces of Echinococcus ortleppi

Published online by Cambridge University Press:  20 October 2016

DANIELI URACH MONTEIRO
Affiliation:
Postgraduation Program in Pharmaceutical Sciences, Universidade Federal de Santa Maria, UFSM, Santa Maria, Brazil
MARIA ISABEL AZEVEDO
Affiliation:
Department of Industrial Pharmacy, Postgraduation Program in Veterinary Medicine, Universidade Federal de Santa Maria, UFSM, Santa Maria, Brazil
CARLA WEIBLEN
Affiliation:
Department of Industrial Pharmacy, Postgraduation Program in Veterinary Medicine, Universidade Federal de Santa Maria, UFSM, Santa Maria, Brazil
SÔNIA DE AVILA BOTTON
Affiliation:
Department of Industrial Pharmacy, Postgraduation Program in Veterinary Medicine, Universidade Federal de Santa Maria, UFSM, Santa Maria, Brazil
NADINE LYSYK FUNK
Affiliation:
Postgraduation Program in Pharmaceutical Sciences, Universidade Federal de Santa Maria, UFSM, Santa Maria, Brazil
CRISTIANE DE BONA DA SILVA
Affiliation:
Postgraduation Program in Pharmaceutical Sciences, Universidade Federal de Santa Maria, UFSM, Santa Maria, Brazil
RÉGIS ADRIEL ZANETTE
Affiliation:
Postgraduation Program in Biological Sciences: Pharmacology and Therapeutics, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil
THIAGO GUILHERME SCHWANZ
Affiliation:
Postgraduation Program in Pharmaceutical Sciences, Universidade Federal de Santa Maria, UFSM, Santa Maria, Brazil
MÁRIO LUIZ DE LA RUE*
Affiliation:
Postgraduation Program in Pharmaceutical Sciences, Universidade Federal de Santa Maria, UFSM, Santa Maria, Brazil
*
*Corresponding author. Departamento de Microbiologia e Parasitologia, Campus Universitário, Universidade Federal de Santa Maria, Avenida Roraima, 1000, Prédio 20 – Sala 4226, CEP 97105-970, Santa Maria, RS, Brazil. E-mail: [email protected]

Summary

Cystic echinococcosis is a zoonotic disease of difficult diagnosis and treatment. The use of protoscolicidal agents in procedures is of utmost importance for treatment success. This study was aimed at analysing the in vitro and ex vivo activity of Melaleuca alternifolia oil (tea tree oil – TTO), its nanoemulsion formulation (NE-TTO) and its major component (terpinen-4-ol) against Echinococcus ortleppi protoscoleces obtained from cattle. Concentrations of 2·5, 5 and 10 mg mL−1 of TTO, 10 mg mL−1 of NE-TTO and 1, 1·5 and 2 mg mL−1 of terpinen-4-ol were evaluated in vitro against protoscoleces at 5, 10, 15 and 30 min. TTO was also injected directly into hydatid cysts (ex vivo analysis, n = 20) and the viability of protoscoleces was evaluated at 5, 15 and 30 min. The results indicated protoscolicidal effect at all tested formulations and concentrations. Terpinen-4-ol (2 mg mL−1) activity was superior when compared with the highest concentration of TTO. NE-TTO reached a gradual protoscolicidal effect. TTO at 20 mg mL−1 showed 90% protoscolicidal action in hydatid cysts at 5 min. The results showed that TTO affects the viability of E. ortleppi protoscoleces, suggesting a new protoscolicidal option to the treatment of cystic equinococcosis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Adas, G., Arikan, S., Kemik, O., Oner, A., Sahip, N. and Karatepe, O. (2009). Use of albendazole sulfoxide, albendazole sulfone, and combined solutions as scolicidal agents on hydatid cysts (in vitro study). World Journal of Gastroenterology 15, 112116.CrossRefGoogle ScholarPubMed
Ahmadnia, S., Moazeni, M., Mohammadi-Samani, S. and Oryan, A. (2013). In vivo evaluation of the efficacy of albendazole sulfoxide and albendazole sulfoxide loaded solid lipid nanoparticles against hydatid cyst. Experimental Parasitology 135, 314319.CrossRefGoogle ScholarPubMed
Anton, N., Benoit, J. B. and Saulnier, P. (2008). Design and production of nanoparticles formulated from nano-emulsion templates-a review. Journal of Controlled Release 128, 185199.CrossRefGoogle ScholarPubMed
Bakkali, F., Averbeck, S., Averbeck, D. and Idaomar, M. (2008). Biological effects of essential oils – a review. Food and Chemical Toxicology 46, 446475.CrossRefGoogle ScholarPubMed
Balbinotti, H., Santos, G. B., Badaraco, J., Arend, A. C., Graichen, D. A. S., Haag, K. L. and Zaha, A. (2012). Echinococcus ortleppi (G5) and Echinococcus granulosus sensu stricto (G1) loads in cattle from Southern Brazil. Veterinary Parasitology 188, 255260.CrossRefGoogle ScholarPubMed
Baldissera, M. D., Da Silva, A. S., Oliveira, C. B., Santos, R. C. V., Vaucher, R. A., Raffin, R. P., Gomes, P., Dambros, M. G. C., Milleti, L. C., Boligon, A. A., Athayde, M. L. and Monteiro, S. G. (2014). Trypanocidal action of tea tree oil (Melaleuca alternifolia) against Trypanosoma evansi in vitro and in vivo used mice as experimental model. Experimental Parasitology 141, 2127.CrossRefGoogle ScholarPubMed
Baldissera, M. D., Grando, T. H., Souza, C. F., Gressler, L. T., Stefani, L. M., Silva, A. S. and Monteiro, S. G. (2016). In vitro and in vivo action of terpinen-4-ol, γ-terpinene, and α-terpinene against Trypanosoma evansi . Experimental Parasitology 162, 4348.CrossRefGoogle ScholarPubMed
Bowles, J., Blair, D. and McManus, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165173.CrossRefGoogle ScholarPubMed
Brunetti, E., Kern, P., Vuitton, D. A. and Panel, W. (2010). Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Tropica 114, 116.CrossRefGoogle ScholarPubMed
Carson, C. F., Hammer, K. A. and Riley, T. V. (2006). Melaleuca alternifolia (tea tree) oil: a review of antimicrobial and other medicinal properties. Clinical Microbiology Reviews 19, 5062.CrossRefGoogle ScholarPubMed
Carson, C. F., Smith, D. W., Lampacher, G. J. and Riley, T. V. (2008). Use of deception to achieve double-blinding in a clinical trial of Melaleuca alternifolia (tea tree) oil for the treatment of recurrent herpes labialis. Contemporary Clinical Trials 29, 912.CrossRefGoogle Scholar
Cox, S. D., Mann, C. M., Markham, J. L., Bell, H. C., Gustafson, J. E., Warmington, J. R. and Wyllie, S. G. (2000). The mode of antimicrobial action of the essential oil of Melaleuca alternifolia (tea tree oil). Journal of Applied Microbiology 88, 170175.CrossRefGoogle ScholarPubMed
de la Rue, M. L., Dinkel, A., Mackenstedt, U. and Romig, T. (2006). New data on Echinococcus spp. in Southern Brazil. Revista do Instituto de Medicina Tropical 48, 103104.CrossRefGoogle ScholarPubMed
de la Rue, M. L., Takano, K., Brochado, J., Costa, C. V., Soares, A. G., Yamano, K., Yagi, K., Katoh, Y. and Takahashi, K. (2011). Infection of humans and animals with Echinococcus granulosus (G1 and G3 strains) and E. ortleppi in Southern Brazil. Veterinary Parasitology 177, 97103.CrossRefGoogle Scholar
Eckert, J., Gemmell, M. A., Meslin, F.-X. and Pawłowski, Z. S. (2001). WHO/OIE Manual on Echinococcosis in Humans and Animals: a Public Health Problem of Global Concern. World Organization for Animal Health, Paris, France.Google Scholar
Flores, F. C., Lima, J. A., Ribeiro, R. F., Ourique, A. F., Rolim, C. M. B. and Silva, C. B. (2011). Nanostructured systems containing an essential oil: protection against volatilization. Química Nova 34, 968972.CrossRefGoogle Scholar
Flores, F. C., Lima, J. A., Ribeiro, R. F., Alves, S. H., Rolim, C. M. B., Beck, R. C. R. and Silva, C. B. (2013). Antifungal activity of nanocapsule suspensions containing tea tree oil on the growth of Trichophyton rubrum . Mycopathologia 175, 281286.CrossRefGoogle ScholarPubMed
Grenouillet, F., Umhang, G., Arbez-Gindre, F., Mantion, G., Delabrousse, E., Millon, L. and Boué, F. (2014). Echinococcus ortleppi infections in humans and cattle, France. Emerging Infectious Diseases 20, 21002102.CrossRefGoogle ScholarPubMed
Guarnera, E. A., Parra, A., Kamenetzky, L., Garcia, G. and Gutiérrez, A. (2004). Cystic echinococcosis in Argentina: evolution of metacestode and clinical expression in various Echinococcus granulosus strains. Acta Tropica 92, 153159.CrossRefGoogle ScholarPubMed
Hailong, L. V., Jiang, Y., Liao, M., Sun, H., Zhang, S. and Peng, X. (2013). In vitro and in vivo treatments of Echinococcus granulosus with Huaier aqueous extract and albendazole liposome. Parasitology Research 111, 961966.Google Scholar
Hammer, K. A., Carson, C. F., Riley, T. V. and Nielsen, J. B. (2006). A review of the toxicity of Melaleuca alternifolia (tea tree) oil. Food and Chemical Toxicology 44, 616625.CrossRefGoogle ScholarPubMed
Hart, P. H., Brand, C., Carson, C. F., Riley, T. V., Prager, R. H. and Finlay-Jones, J. J. (2000). Terpinen-4-ol, the main component of the essential oil of Melaleuca alternifolia (tea tree oil), suppresses inflammatory mediator production by activated human monocytes. Inflammation Research 49, 619626.CrossRefGoogle ScholarPubMed
Mahmoudvand, H., Harandi, M. F., Shakibaie, M., Aflatoonian, M. R., ZiaAli, N., Makki, M. S. and Jahanbakhsh, S. (2014). Scolicidal effects of biogenic selenium nanoparticles against protoscolices of hydatid cysts. International Journal of Surgery 12, 399403.CrossRefGoogle ScholarPubMed
Maravilla, P., Thompson, R. C. A., Palacios-Ruiz, J. A., Estcourt, A., Raminez-Solis, E., Mondragon-de-la-Peña, C., Moreno-Moller, M., Cardenas-Mejia, A., MataMiranda, P., Aguirre-Alcantara, M.-T., Bonilla-Rodriguez, C. and Flisser, A. (2004). Echinococcus granulosus cattle strain identification in an autocthonous case of cystic echinococcosis in central Mexico. Acta Tropica 92, 231236.CrossRefGoogle Scholar
Moazeni, M. and Roozitalab, A. (2012). High scolicidal effect of Zataria multiflora on protoscoleces of hydatid cyst: an in vitro study. Comparative Clinical Pathology 21, 99104.CrossRefGoogle Scholar
Monalisa, J., Swati, M., Swetalina, J. and Sudhanshu, S. (2013). Nanotechnology- future prospect in recent medicine: a review. International Journal of Basic and Clinical Pharmacology 2, 353359.Google Scholar
Monteiro, D. U., Botton, S. A., Tonin, A. A., Azevedo, M. I., Graichen, D. A. S., Noal, C. B. and de la Rue, M. L. (2014). Echinococcus canadensis (G7) and Echinococcus granulosus sensu stricto (G1) in swine of southern Brazil. Veterinary Parasitology 202, 335338.CrossRefGoogle ScholarPubMed
Nakao, M., Lavikainen, A., Yanagida, T. and Ito, A. (2013). Phylogenetic systematics of the genus Echinococcus (Cestoda: Taeniidae). International Journal for Parasitology 43, 10171029.CrossRefGoogle ScholarPubMed
Peláez, V., Kugler, C., Correa, D., Del Carpio, M., Guangiroli, M., Molina, J., Marcos, B. and Lopez, E. (2000). PAIR as percutaneous treatment of hydatid liver cysts. Acta Tropica 75, 197202.CrossRefGoogle ScholarPubMed
Pensel, P. E., Maggiore, M. A., Gende, L. B., Eguaras, M. J., Denegri, M. G. and Elissondo, M. C. (2014). Efficacy of essential oils of Thymus vulgaris and Origanum vulgare on Echinococcus granulosus . Interdisciplinary Perspectives on Infectious Diseases 1, 12.Google Scholar
Petrigh, R. S. and Fugassa, M. H. (2013). DNA extraction and a cost-effective detection method for Echinococcus granulosus protoscoleces. Veterinary Parasitology 198, 410413.CrossRefGoogle Scholar
Puryan, K., Karadayi, K., Topcu, O., Canbay, E., Sumer, Z., Turan, M., Karayalcin, K. and Sen, M. (2005). Chlorhexidine gluconate: an ideal scolicidal agent in the treatment of intraperitoneal hydatidosis? World Journal of Surgery 29, 227230.CrossRefGoogle ScholarPubMed
Putheti, R. R., Okigbo, R. N., Madhusoodhan, S. and Chavanpatil, S. (2008). Nanotechnology importance in the pharmaceutical industry. African Journal of Pure and Applied Chemistry 2, 2731.Google Scholar
Romig, T., Ebi, D. and Wassermann, M. (2015). Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Veterinary Parasitology 213, 7684.CrossRefGoogle ScholarPubMed
Sagave, L., Gressler, L. T., Flores, F. C., Silva, C. B., Vargas, A. P. C., Lovato, M., Sangioni, L. A., Pötter, L. and Botton, S. A. (2015). Atividade de nanoformulações de Melaleuca alternifolia e terpinen-4-ol em isolados de Rhodococcus equi . Arquivo Brasileiro de Medicina Veterinária e Zootecnia 67, 221226.CrossRefGoogle Scholar
Schaffazick, S. R., Guterres, S. S., Freitas, L. L. and Pohlmann, A. R. (2003). Caracterização e estabilidade físico-química de sistemas poliméricos nanoparticulados para administração de fármacos. Química Nova 26, 726737.CrossRefGoogle Scholar
Sharma, M., Sehgal, R., Fomda, B. A., Malhotra, A. and Malla, N. (2013). Molecular characterization of Echinococcus granulosus cysts in north Indian patients: identification of G1, G3, G5 and G6 genotypes. PLOS Neglected Tropical Diseases 7, e2262.CrossRefGoogle Scholar
Silva, A. M., Caldeira, J. and Nunes, J. N. (2001). P.A.I.R. – alternativa terapêutica do quisto hidático do fígado. Portuguese Journal of Gastroenterology 8, 113120.Google Scholar
Smego, R. A. and Sebanego, P. (2005). Treatment options for hepatic cystic echinococcosis. International Journal of Infectious Diseases 9, 6976.CrossRefGoogle ScholarPubMed
Walton, S. F., McKinnon, M., Pizzutto, S., Dougall, A., Williams, E. and Currie, B. J. (2004). Acaricidal activity of Melaleuca alternifolia (tea tree) oil. Archives of Dermatology 140, 563566.CrossRefGoogle ScholarPubMed
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