Essential Oils and Their Bioactive Compounds in the Control of Gastrointestinal Nematodes of Small Ruminants
DOI:
https://doi.org/10.22456/1679-9216.81804Abstract
Background: Gastrointestinal nematodes are one of the major health and economic problem of sheep and goats in the world. The control of these nematodes is carried out conventionally with synthetic anthelminths, which favored the selection of gastrointestinal nematode (GIN) populations multiresistant to anthelmintics. The emergence of anthelmintic resistance has stimulated the search for new alternatives to control small ruminant GIN, standing out the use of plants and their bioactives compounds, such as essential oils (EO). The objective of this review was to present the main characteristics and anthelmintic activity of EO, their isolated compounds and drug delivery systems in the control of GIN.
Review: Essential oils are a complex blend of bioactive compounds with volatile, lipophilic, usually odoriferous and liquid substances. EO are composed of terpenes, terpenoids, aromatic and aliphatic constituents. EO has various pharmacological activities of interest in preventive veterinary medicine such as antibacterials, antifungals, anticoccicids, insecticides and anthelmintics. In vitro and in vivo tests are used to validate the anthelmintic activity of EO on GIN. In vitro tests are low cost screening tests that allow the evaluation of the anthelmintic activity of a large amount of bioactive compounds on eggs, first (L1) and third stage larvae (L3), and adult nematodes. The antiparasitic effect of EO is related to its main compound or to the interaction of the compounds. These bioactive compounds penetrate the cuticle of the nematodes by transcuticular diffusion, altering the mechanisms of locomotion, besides causing cuticular lesions. Following in vitro evaluation, the acute and sub-chronic toxicity test should be performed to assess the toxicity of the bioactive compounds and to define the dose to be used in in vivo tests. In vivo tests are more reliable because the anthelmintic effectiveness of bioactive compounds is evaluated after the metabolization process. The metabolization process of the bioactive compounds can generate metabolites that exhibit or not anthelmintic effectiveness. The in vivo tests assessing the anthelmintic effectiveness of bioactive compounds in sheep and goats are the fecal egg count reduction test and the controlled test. OE promoted reduction of egg elimination in faeces which may be related to cuticular and reproductive alterations in GIN, and reduction of parasite burden in in vivo tests. Due to the promising results obtained with OE in the in vivo tests, interest has been aroused in using nanotechnology as an alternative to increase the bioavailability of OE and consequently, potentializing its anthelmintic effect, reducing the dose and toxicity of the biocompounds. In addition to nanotechnology, the isolation and chemical modification of compounds isolated from OE have been employed to obtain new molecules with anthelmintic action and understand the mechanism of action of EO on the small ruminant GIN.
Conclusion: The use of EO and their compound bioactive in the control of resistant populations of GIN is a promising alternative. The adoption of strategies in which natural products can replace synthetic anthelmintics, such as in dry periods and use synthetic anthelmintics in the rainy season when the population in refugia in the pasture is high, thus reducing the dissemination of GIN resistant populations. As perspective, the evaluation of pharmacokinetics and pharmacodynamics of these natural products should be performed so that one defines treatment protocols that optimize the anthelmintic effect.
Downloads
References
Acharya J., Hildreth M.B. & Neil R. 2014. In vitro screening of forty medicinal plant extracts from the United States Northern Great Plains for anthelmintic activity against Haemonchus contortus. Veterinary Parasitology. 201(1-2): 7581.
Akkari H., Ezzine O., Dhahri S., B’chir F., Rekik M., Hajaji S., Darghouth M.A., Jamâa M.L.B. & Gharbi M. 2015. Chemical composition, insecticidal and in vitro anthelmintic activityes of Ruta chalepensis (Rutaceae) essential oil. Industrial Crops and Products. 74: 745-751.
Álvarez-Sánchez M.A., Pérez García J., Bartley D., Jackson F. & Rojo-Vázquez F.A. 2005. The larval feeding inhibition assay for the diagnosis of nematode anthelmintic resistance. Experimental Parasitology. 110(1): 56-61.
Andre W.P.P., Ribeiro W.L.C., Cavalcante G.S., Santos, J.M.L., Macedo I.T.F., Paula H.C.B., Freitas R.M., Morais S.M., Melo J.V. & Bevilaqua C.M.L. 2016. Comparative efficacy and toxic effects of carvacryl acetate and carvacrol on sheep gastrointestinal nematodes and mice. Veterinary Parasitology. 218: 52-58.
André W.P.P., Cavalcante G.S., Ribeiro W.L.C., Santos J.M.L., Macedo I.T.F., Paula H.C.B., Morais S.M., Melo J.V. & Bevilaqua C.M.L. 2017. Anthelmintic effect of thymol and thymol acetate on sheep gastrointestinal nematodes and their toxicity in mice. Revista Brasileira de Parasitologia Veterinária. 22(3): 323-330.
Bakkali F., Averbeck S., Averbeck D. & Idaomar M. 2008. Biological effects of essencial oils – A review. Food and Chemical Toxicology. 46(2): 446-475.
Besier R.B., Kahn L.P., Sargison N.D. & Van Wyk J.A. 2016. The pathophysiology, ecology and epidemiology of Haemonchus contortus infection in small ruminants. Advances in Parasitology. 93: 2-39.
Camurça-Vasconcelos A.L.F., Bevilaqua C.M.L., Morais S.M., Maciel M.V., CostaC.T.C., Macedo I.T.F., Oliveira L.M.B., Braga R.R., Silva R.A., Vieira L.S. & Navarro A.M.C. 2008. Anthelmintic activity of Lippia sidoides essential oil on sheep gastrointestinal nematodes. Veterinary Parasitology. 154(1-2): 167-170.
Camurça-Vasconcelos A.L.F., Bevilaqua C.M.L., Morais S.M., Maciel M.V., Costa C.T.C., Macedo I.T.F., Oliveira L.M.B., Braga R.R., Silva R.A. & Vieira L.S. 2007. Anthelmintic activity of Croton zehntneri and Lippia sidoides essential oils. Veterinary Parasitology. 148(3-4): 288-294.
Camurça-Vasconcelos A.L.F., Morais S.M., Santos L.F.L., Rocha M.F.G. & Bevilaqua C.M.L. 2005. Validação de plantas medicinais com atividade anti-helmíntica. Revista Brasileira de Plantas Medicinais. 7(3): 97-106
Castilho C.V.V., Fantatto R.R., Gaínza Y.A., Bizzo H.R., Barbi N., Leitão S.G. & Chagas A.C.S. 2017. In vitro activity of the essential oil from Hesperozygis myrtoides on Rhipicephalus (Boophilus) microplus and Haemonchus contortus. Revista Brasileira de Farmacognosia. 27: 70-76.
Chagas A.C.S., Oliveira M.C.S., Giglioti R., Santana R.C.M., Bizzo H.R., Gama P.E. & Chaves F.C.M. 2016. Efficacy of 11 Brazilian essential oils on lethality of the cattle tick Rhipicephalus (Boophilus) microplus. Ticks and Tick-borne Diseases. 7(3): 427-432.
Chan-Pérez J.I., Torres-Acosta J.F.F., Sandoval-Castro C.A., Hoste H., Castañeda-Ramírez G.S., Vilarem G. & Mathieu C. 2016. In vitro susceptibility of ten Haemonchus contortus isolates from different geographical origins towards acetone:water extracts of two tannin rich plants. Veterinary Parasitology. 217: 53-60.
Chan-Pérez J.I., Torres-Acosta J.F.F., Sandoval-Castro C.A., Castañeda-Ramírez G.S., Vilarem G., Mathieu C. & Hoste H. 2017. Susceptibility of ten Haemonchus contortus isolates from different geographical origins towards acetone:water extracts of polyphenol-rich plants. Part 2: Infective L3 larvae. Veterinary Parasitology. 240: 11-16.
Cleff M.B., Meinerz A.R.M., Madrid I., Fonseca A.O., Alves G.H., Meireles M.C.A. & Rodrigues M.R.A. 2012. Perfil de suscetibilidade de leveduras do gênero Candida isoladas de animais ao óleo essencial de Rosmarinus officinalis L. Revista Brasileira de Plantas Medicinais. 14(1): 43-49.
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 (WAAVP) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology. 44(1-2): 35-44.
Conder G.A., Johnson S.S., Hall A.D., Fleming M.W., Mills M.D. & Guimond P.M. 1992. Growth and development of Haemonchus contortus in jirds, Meriones unguiculatus. Journal of Parasitology. 78(3): 492-497.
Cruz B.C., Buzzulini C., Lopes W.D.Z., Maciel W.G, Bichuette M.A., Felippelli G., Teixeira W.F.P., Soares V.E., Gomes L.V.C., Prando L., Campos G.P. & Costa A.J. 2015. Effects of different spray formulations on the reproductive parameters of engorged Rhipicephalus (Boophilus) microplus females detached from experimentally infested. Preventive Veterinary Medicine. 122(1-2): 70-75.
Domingues L.F., Giglioti R., Feitosa K.A., Fantatto R.R., Rabelo M.D., Oliveira M.C.S., Bechara G.H., Oliveira G.P., Barioni Junior W. & Chagas A.C.S. 2013. In vitro and in vivo evaluation of the activity of pineapple (Ananas comosus) on Haemonchus contortus in Santa Inês sheep. Veterinary Parasitology. 197(1-2): 263-270.
Donsì F., Annunziata M., Sessa M. & Ferrari G. 2011. Nanoencapsulation of essential oils to enhance their antimicrobial activity in foods. Food Science and Technology. 44(9): 1908-1914.
Eguale T., Tadesse D. & Giday M. 2011. In vitro anthelmintic activity of crude extracts of five medicinal plants against egg-hatching and larval development of Haemonchus contortus. Journal of Ethnopharmacology. 137(1): 108-113.
Epe C. & Kaminsky R. 2013. New advancement in anthelmintic drugs in veterinary medicine. Trends in Parasitology. 29(3): 129-134.
Ferreira L.E., Benincasa B.I., Fachin A.L., França S.C., Contini S.S.H.T., Chagas A.C.S. & Beleboni R.O. 2016. Thymus vulgaris L. essential oil and its main component thymol: Anthelmintic effects against Haemonchus contortus from sheep. Veterinary Parasitology. 288: 70-76.
Gaínza Y.A., Domingues L.F., Perez O.P., Rabelo M.D., López E.R. & Chagas A.C.S. 2015. Anthelmintic activity in vitro of Citrus sinensis and Melaleuca quinquenervia essential oil from Cuba on Haemonchus contortus. Industrial Crops and Products. 76: 647-652.
Gaínza Y.A., Fantatto R.R., Chaves F.C.M., Bizzo H.R., Esteves S.N. & Chagas A.C.S. 2016. Piper aduncum against Haemonchus contortus isolates: cross resistance and the research of natural bioactive compounds. Revista Brasileira de Parasitologia Veterinária. 25(4): 383-393.
Gamboa G.V.U., Palma S.D., Lifschitz A., Ballent M., Lanusse C., Passirani C., Benoit J.P. & Allemandi D.A. 2016. Ivermectin-loaded lipid nanocapsules: toward the development of a new antiparasitic delivery system for veterinary applications. Parasitology Research. 115(5): 1945-1953.
Gaudin E., Simon M., Quijada J., Schelcher F., Sutra J.F., Lespine A. & Hoste H. 2016. Efficacy of sainfoin (Onobrychis viciifolia) pellets against multi resistant Haemonchus contortus and interaction with oral ivermectin: Implications for on-farm control. Veterinary Parasitology. 227: 122-129.
Giarratana F., Muscolino D., Beninati C., Giuffrida A. & Panebianco A. 2014. Activity of Thymus vulgaris essential oil against Anisakis larvae. Experimental Parasitology. 142: 7-10.
Githiori J.B., Athanasiadou S. & Thamsborg S.M. 2006. Use of plants in novel approaches for control of gastrointestinal helminths in livestock with emphasis on small ruminants. Veterinary Parasitology. 139(4): 308-320.
Gobbo-Neto L. & Lopes N.P. 2007. Plantas medicinais: fatores de influência no conteúdo de metabolitos secundários. Quimica Nova. 30(2): 374-381.
Grando T.H., Baldissera, M.D., Gressler, L.T., Sá M.F., Bortoluzzi B.N., Schafer, A.S., Ebling R.C., Raffin R.P., Santos R.C.V., Stefani L.M., Vaucher R., Leal M.L.R. & Monteiro S.G. 2016. Melaleuca alternifolia anthelmintic activity in gerbils experimentally infected by Haemonchus contortus. Experimental Parasitology. 170: 177-183.
Grando T.H., Sá M.F., Baldissera M.D., Oliveira C.B., Souza M.E., Raffin R.P., Santos R.C.V., Domingues R., Minho A.P., Leal M.L.R. & Monteiro S.G. 2016. In vitro activity of essential oils of free and nanostructured Melaleuca alternifolia and of terpinen-4-ol on eggs and larvae of Haemonchus contortus. Journal of Helminthology. 90(3): 377-382.
Gupta R., Gabrielsen B. & Ferguson S.M. 2005. Nature’s Medicines: Traditional Knowledge and Intellectual Property Management. Case Studies from the National Institutes of Health (NIH), USA. Current Drug Discovery Technology. 2(4): 203-219.
Heckendorn F., Häring D.A., Maurer V., Senn M. & Hertzberg H. 2007. Individual administration of three tanniferous forage plants to lambs artificially infected with Haemonchus contortus and Cooperia curticei. Veterinary Parasitology. 146(1-2): 123-134.
Hoste H., Jackson F., Athanasiadou S., Thansborg S.M. & Hoskin S.O. 2006. The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends in Parasitology. 22(6): 253-261.
Hoste H., Torres-Acosta J.F.J., Quijada J., Chan-Perez I., Dakheel M.M., Kommuru D.S., Mueller-Harvey I. & Terrill T.H. 2016. Interactions Between Nutritionand Infections With Haemonchus contortus and Related Gastrointestinal Nematodes in Small Ruminants. Advances in Parasitology. 93: 239-351.
Hoste H. & Torres-Acosta J.F.J. 2011. Non chemical control of helminths in ruminants: adapting solutions for changing worms in a changing world. Veterinary Parasitology. 180(1-2): 144-154.
Hounzangbe-Adote M.S., Paolini V., Fouraste I., Moutairou K. & Hoste H. 2005. In vitro effects of four tropical plants on three life-cycle stages of the parasitic nematode, Haemonchus contortus. Research in Veterinary Science. 78(2): 155-160.
Hubert J. & Kerboeuf D. 1992. A microlarval development assay for the detection of anthelmintic resistance in sheep nematodes. Veterinary Record. 130(20): 442–446.
Iqbal Z., Lateef M., Jabbar A., Muhammad G. & Khan M.N. 2005. Anthelmintic activity of Calotropis procera (Ait.) Ait. F. flowers in sheep. Journal of Ethnopharmacology. 102(2): 256-261.
Jitviriyanon S., Phanthong P., Lomarat P., Bunyapraphatsara N., Porntrakulpipat S. & Paraksa N. 2016. In vitro study of anti-coccidial activity of essential oils from indigenous plants against Eimeria tenella. Veterinary Parasitology. 228: 96-102.
Katiki L.M., Barbieri A.M.E., Araujo R.C., Veríssimo C.J., Louvandini H. & Ferreira J.F.S. 2017. Synergistic interaction of ten essential oils against Haemonchus contortus in vitro. Veterinary Parasitology. 243: 47-51.
Katiki L.M., Chagas A.C.S., Takahira R.K., Juliani H.R., Ferreira J.F.S. & Amarante A.F.T. 2012. Evaluation of Cymbopogon schoenanthus essential oil in lambs experimentally infected with Haemonchus contortus. Veterinary Parasitology. 186(3-4): 312-318.
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. Veterinary Parasitology. 183(1-2): 103-108.
Kearney P.E., Murray P.J., Hoy J.M., Hohenhaus M. & Kotze A. 2016. The ‘Toolbox’ of strategies for managing Haemonchus contortus in goats: What’s in and what’s out. Veterinary Parasitology. 220: 93-107.
Kotze A.C. & Prichard R.K. 2016. Anthelmintic Resistance in Haemonchus contortus: History, Mechanisms and Diagnosis. Advances in Parasitology. 93: 398-420.
Lanusse C., Lifschitz A. & Alvarez L. 2015. Basic and clinical pharmacology contribution to extend anthelmintic molecules lifespan. Veterinary Parasitology. 212(1-2): 35-46.
Lei J., Leser M. & Enan E. 2010. Nematicidal activity of two monoterpenoids and SER-2 tyramine receptor of Caenorhabditis elegans. Biochemical Pharmacology. 79(7): 1062-1071.
Lima A.S., Carvalho, J.F., Peixoto, M.G., Blank, A.F., Borges L.M.F. & Costa-Júnior L.M. 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(1): 73-77.
Lopes S.G. & Costa-Junior L.M. 2015. Controle de helmintos gastrintestinais utilizando plantas no Brasil. In: Costa Junior L. & Amarante A. (Eds). Controle de Helmintos de ruminantes no Brasil. Jundiaí: Paco Editora, pp.261-304.
Lynagh T., Cromer B.A., Dufour V. & Laube B. 2014. Comparative pharmacology of flatworm and roundworm glutamate-gated chloride channels: Implications for potential anthelmintics. International Journal for Parasitology: Drugs and Drug Resistance. 4(3): 244-255.
Macedo I.T.F. 2012. Atividade anti-helmíntica de óleos essenciais de plantas do nordeste brasileiro.120f. Fortaleza, CE. Tese (Doutorado em Ciências Veterinárias) - Programa de Pós-graduação em Ciências Veterinárias, Universidade Estadual do Ceará.
Macedo I.T.F., Bevilaqua C.M.L., Oliveira L.M.B., Camurça-Vasconcelos A.L.F., Vieira L.S., Oliveira F.R., Queiroz-Junior E.M, Tomé A.R. & Nascimento N.R.F. 2010. Anthelmintic effect of Eucalyptus staigeriana essential oil against gastrointestinal nematodes. Veterinary Parasitology. 173(1-2): 93-98.
Macedo I.T.F., Bevilaqua C.M.L., Oliveira L.M.B., Camurça-Vasconcelos A.L.F., Vieira L.S. & Amóra S.S.A. 2011. Evaluation of Eucalyptus citriodora essential oil on goat gastrointestinal nematodes. Revista Brasileira de Parasitologia Veterinária. 20(3): 223-227.
Macedo I.T.F., Bevilaqua C.M.L., Oliveira L.M.B., Camurça-Vasconcelos A.L.F., Morais S.M., Machado L.K.A. & Ribeiro W.L.C. 2012. In vitro activity of Lantana camara, Alpinia zerumbet, Mentha villosa and Tagetes minuta decoctions on Haemonchus contortus eggs and larvae. Veterinary Parasitology. 190(3-4): 504-509.
Macedo I.T.F., Bevilaqua C.M.L., Oliveira L.M.B., Camurça-Vasconcelos A.L.F., Vieira L.S., Oliveira F.R., Queiroz-Junior E.M., Portela B.G., Barros R.S. & Chagas A.C.S. 2009. Atividade ovicida e larvicida in vitro do óleo essencial de Eucalyptus globulus sobre Haemonchus contortus. Revista Brasileira de Parasitologia Veterinária. 18(3): 62-66.
Macedo I.T.F., Oliveira L.M.B., Camurça-Vasconcelos A.L.F., Ribeiro W.L.C., Santos J.M.L., Morais S.M.M., Paula H.C.B. & Bevilaqua C.M.L. 2013. In vitro effects of Coriandrum sativum, Tagetes minuta, Alpinia zerumbet and Lantana camara essential oils on Haemonchus contortus. Revista Brasileira de Parasitologia Veterinaria. 22(4): 463-469.
Macedo I.T.F., Oliveira L.M.B., Ribeiro W.L.C., Santos J.M.L., Silva K.C., Araújo Filho J.V., Camurça-Vasconcelos A.L.F. & Bevilaqua C.M.L. 2015. Anthelmintic activity of Cymbopogon citratus against Haemonchus contortus. Revista Brasileira de Parasitologia Veterinária. 24(3): 268-275.
Marie-Magdeleine C., Hoste H., Mahieu M., Varo H. & Archimede H. 2009. In vitro effects of cucurbita moschata seed extracts on Haemonchus contortus. Veterinary Parasitology. 161(1-2): 99-105.
Marie-Magdeleine C., Udino L., Philibert L., Bocage B. & Archimede H. 2014. In vitro effects of Musa paradisiacal extracts on four developmental stages of Haemonchus contortus. Research in Veterinary Science. 96(1): 127-132.
Martínez-Ortíz-de-Montellano C., Arroyo-López C., Fourquaux I., Torres-Acosta J.F.J., Sandoval-Castro C.A. & Hoste H. 2013. Scanning electron microscopy of Haemonchus contortus exposed to tannin-rich plants under in vivo and in vitro conditions. Experimental Parasitology. 133(3): 281-286.
Mesquita M.A., Silva Júnior J.B., Panassol A.M., Oliveira E.F., Camurça-Vasconcelos A.L.F., Paula H.C.B. & Bevilaqua C.M.L. 2013. Anthelmintic activity of Eucalyptus staigeriana encapsulated oil on sheep gastrointestinal nematodes. Parasitology Research. 112(9): 3161-3165.
Miresmailli S. & Isman M.B. 2014. Botanical insecticides inspired by plant-herbivore chemical interactions. Trends in Plant Sciences. 19(1): 29-35.
Molan A.L. & Faraj A.M. 2010. The effects of condensed tannins extracted from different plant species on egg hatching and larval development of Teladorsagia circumcincta (Nematoda: Trichostrongylidae). Folia Parasitologica. 57(1): 62-68.
Monteiro M.V.B., Bevilaqua C.M.L., Morais S.M., Machado L.K.A., Camurça-Vasconcelos A.L.F., Ribeiro W.L.C. & Mesquita M.A. 2011. Anthelmintic activity of Jatropha curcas L. seeds on Haemonchus contortus. Veterinary Parasitology. 182(2-4): 259-263.
Mugnaini L., Nardoni S., Pinto L., Pistelli L., Leonardi M., Pisseri F. & Mancianti F. 2012. In vitro and in vivo antifungal activity of some essential oils against feline isolates of Microsporum canis. Journal de Mycologie Médicale. 22(2): 179-184.
Mullen K.A.E., Lee A.R., Lyman R.L., Mason S.E., Washburn S.P. & Anderson K.L. 2014. An in vitro assessment of the antibacterial activity of plant-derived oils. Journal of Dairy Science. 97(9): 5587-5591.
Oka Y., Nacar S., Putievsky E., Ravid U., Yaniv Z. & Spiegel Y. 2000. Nematicidal activity of essential oils and their components against the root-knot nematode. Phytopathology. 90(7): 710-715.
Oliveira L.M.B, Bevilaqua C.M.L., Macedo I.T.F., Morais S.M., Monteiro M.V.B., Campello C.C., Ribeiro W.L.C. & Batista E.K.F. 2011. Effect of six tropical tanniferous plant extracts on larval exsheathment of Haemonchus contorus. Revista Brasileira de Parasitologia Veterinária. 20(2): 155-160.
Oliveira L.M.B., Bevilaqua C.M.L., Morais S.M., Camurça-Vasconcelos A.L.F. & Macedo I.T.F. 2011. Plantas taniníferas e o controle de nematóides gastrintestinais de pequenos ruminantes. Ciência Rural. 41(11): 1967-1974.
Oliveira G.L., Vieira T.M., Nunes V.F., Ruas M.O., Duarte E.R., Moreira D.L., Kaplan M.A.C. & Martins E.R. 2014. Chemical composition and efficacy in the egg-hatching inhibition of essential oil of Piper aduncum against Haemonchus contortus from sheep. Revista Brasileira de Farmacognosia. 24(3): 288-292.
Pandey A.K., Singh P. & Tripathi N.N. 2014. Chemistry and bioactivities of essential oils of some Ocimum species: an overview. Asian Pacific Journal of Tropical Biomedicine. 4(9): 682-694.
Pavela R. 2015. Essential oils for the development of eco-friendly mosquito larvicides: A review. Industrial Crops and Products. 76: 174-187.
Peixoto M.G., Costa-Júnior L.M., Blank F.A., 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. Veterinary Parasitology. 210(1-2): 118-122.
Peres L.E.P. 2004. Metabolismo Secundário. Piracicaba: Escola Superior de Agricultura Luiz de Queiroz (ESALQ)/ Universidade de São Paulo, pp.1-10.
Pessoa L.M., Morais S.M., Bevilaqua C.M.L. & Luciano J.HS. 2012. Anthelmintic activity of essential oil of Ocimum gratissimum Linn. and eugenol against Haemonchus contortus. Veterinary Parasitology. 109(1-2): 59-63.
Qi H., Wang W.X., Dai J.L. & Zhu L. 2015. In vitro Zanthoxylum simulans essential oil against Haemonchus contortus. Veterinary Parasitology. 211(3-4): 223-227.
Raut J.S. & Karuppayil S.M. 2014. A status review on the medicinal properties of essential oils. Industrial Crops and Products. 62: 250-264.
Remmal A., Achahbar S., Bouddine L., Chami N. & Chami F. 2011. In vitro destruction of Eimeria oocysts by essential oils. Veterinary Parasitology. 182(2-4): 121-126.
Ribeiro J.C., Ribeiro W.L.C., Camurça-Vasconcelos A.L.F., Macedo I.T.F., Santos J.M.L., Paula H.C.B., Araújo Filho J.V., Magalhães R.D. & Bevilaqua C.M.L. 2014. Efficacy of free and nanoencapsulated Eucalyptus citriodora essential oils on sheep gastrointestinal nematodes and toxicity for mice. Veterinary Parasitology. 204(3-4): 243-248.
Ribeiro W.L.C., Andre W.P.P., Cavalcante G.S., Araújo Filho J.V., Santos J.M.L., Macedo I.T.F., de Melo J.V., de Morais S.M. & Bevilaqua C.M.L. 2017. Effects of Spigelia anthelmia decoction on sheep gastrointestinal nematodes. Small Ruminant Research. 153: 146-152.
Ribeiro W.L.C., Camurça-Vasconcelos A.L.F., Macedo I.T.F., Santos J.M.L., Ribeiro J.C., Pereira V.A., Viana D.A., Paula H.C.B. & Bevilaqua C.M.L. 2015. In vitro effects of Eucalyptus staigeriana nanoemulsion on Haemonchus contortus and toxicity in rodents. Veterinary Parasitology. 212(3-4): 444-447.
Ribeiro W.L.C., Camurça-Vasconcelos A.L.F., Santos J.M.L., Macedo I.T.F., Ribeiro J.C., Oliveira E.F., Paula H.C.B. & Bevilaqua C.M.L. 2017. The use of Eucalyptus staigeriana nanoemulsion in the control of sheep haemonchosis. Pesquisa Veterinária Brasileira. 37(3): 221-226.
Ribeiro W.L.C., Macedo I.T.F., Santos J.M.L., Oliveira E.F., Camurça-Vasconcelos A.L.F., Paula H.C.B. & Bevilaqua C.M.L. 2013. Activity of chitosan-encapsulated Eucalyptus staigeriana essential oil on Haemonchus contortus. Experimental Parasitology. 135(1): 24-29.
Ritter R.A., Monteiro M.V.M., Monteiro F.O.B., Rodrigues S.T., Soares M.L.S., Silva J.C.R., Palha M.D.C., Biondi G.F., Rahal S.C. & Tourinho M.M. 2012. Ethnoveterinary knowledge and practices at Colares Island, Pará state, eastern Amazon, Brazil. Journal of Ethnopharmacology. 144(2): 346-352.
Rossi C.A., Soares M., Luchese F.C. & Santurio J.M. 2015. Uso de óleos essenciais no controle dos sinais clínicos das diarreias neonatais em leitões nascidos de fêmeas com diferentes ordens de parto. Ciência Animal Brasileira. 16(1): 93-102.
Santos J.M.L., Monteiro J.P., Ribeiro, W.L.C., Macedo, I.T.F., Araújo Filho J.V., Andre W.P.P., Araújo P.R.M., Vasconcelos J.F., Freitas E.P., Camurça-Vasconcelos A.L.F., Vieira L.S. & Bevilaqua C.M.L. 2017. High levels of benzimidazole resistance and β-tubulin isotype 1 SNP F167Y in Haemonchus contortus populations from Ceará State, Brazil. Small Ruminant Research. 147: 1-5.
Simões C.M.O. & Spitzer V. 2004. Óleos voláteis. In: Simões C.M.O. (Ed). Farmacognósia: da planta ao medicamento. 5.ed. Porto Alegre/Florianópolis: Editora da UFRGS/Editora da UFSC, pp.467-495.
Squires J.M., Foster J.G., Lindsay D.S., Caudell D.L. & Zajac A.M. 2010. Efficacy of an orange oil emulsion as an anthelmintic against Haemonchus contortus in gerbils (Meriones unguiculatus) and in sheep. Veterinary Parasitology. 172(1-2): 95-99.
Taylor M.A., Hurt K.R. & Goodyear K.L. 2002. Anthelmintic resistance detection methods. Veterinary Parasitology. 103(3): 183-94.
Wood I.B., Amaral N.K., Bairden K., Duncan J.L., Kassai T., Malone-Junior J.B., Pankavich J.A., Reinecke R.K., Slocombe O., Taylor S.M. & Vercruysse J. 1995. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) second edition of guidelines for evaluating the efficacy of anthelmintics in ruminants (bovine, ovine, caprine). Veterinary Parasitology. 58(3): 181-213.
Zhu L., Dai J.L., Yang L. & Qiu J. 2013. In vitro ovicidal and larvicidal activity of the essential oil of Artemisia lancea against Haemonchus contortus (Strongylida). Veterinary Parasitology. 195(1-2): 112-117.
Zhu L., Dai J., Yang L. & Qiu J. 2013. Anthelmintic activity of Arisaema franchetianum and Arisaema lobatum essential oils against Haemonchus contortus. Journal of Ethnopharmacology. 148(1): 311-316.
Published
How to Cite
Issue
Section
License
This journal provides open access to all of its content on the principle that making research freely available to the public supports a greater global exchange of knowledge. Such access is associated with increased readership and increased citation of an author's work. For more information on this approach, see the Public Knowledge Project and Directory of Open Access Journals.
We define open access journals as journals that use a funding model that does not charge readers or their institutions for access. From the BOAI definition of "open access" we take the right of users to "read, download, copy, distribute, print, search, or link to the full texts of these articles" as mandatory for a journal to be included in the directory.
La Red y Portal Iberoamericano de Revistas Científicas de Veterinaria de Libre Acceso reúne a las principales publicaciones científicas editadas en España, Portugal, Latino América y otros países del ámbito latino
