Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-29T01:34:24.945Z Has data issue: false hasContentIssue false
  • English
  • Français

Chemical characterization and in vitro biological activity of Cymbopogon citratus extracts against Haemonchus spp. and Trichostrongylus spp. nematodes from sheep

Published online by Cambridge University Press:  03 August 2020

Letícia Oliveira da Rocha ,
Gloria Cristina da Silva Lemos ,
Ivo José Curcino Vieira ,
Raimundo Braz-Filho ,
Silvério de Paiva Freitas ,
Leonardo Siqueira Glória  and
Clóvis de Paula Santos Open the ORCID record for Clóvis de Paula Santos [Opens in a new window]
Letícia Oliveira da Rocha
Affiliation:
Laboratório de Biologia Celular e Tecidual, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Av. Alberto Lamego, 2000, Parque Califórnia, Campos dos Goytacazes, RJ28013-602, Brazil
Gloria Cristina da Silva Lemos
Affiliation:
Laboratório de Fitotecnia, Centro de Ciências Tecnológicas e Agropecuárias, Universidade Estadual do Norte Fluminense, Av. Alberto Lamego, 2000, Parque Califórnia, Campos dos Goytacazes, RJ, 28013-602, Brazil
Ivo José Curcino Vieira
Affiliation:
Laboratório de Ciências Químicas, Centro de Ciências Tecnológicas, Universidade Estadual do Norte Fluminense, Av. Alberto Lamego, 2000, Parque Califórnia, Campos dos Goytacazes, RJ, 28013-602, Brazil
Raimundo Braz-Filho
Affiliation:
Pesquisador Emérito-FAPERJ, DQO-IQ – Universidade Federal Rural do Rio de Janeiro (UFRRJ)/LCQUI – CCT – Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF) Rodovia BR 465, Km 07, s/n Zona Rural, Seropédica - RJ, 23890-000 Brazil e Av. Alberto Lamego, 2000, Parque Califórnia, Campos dos Goytacazes, RJ, 28013-602, Brazil
Silvério de Paiva Freitas
Affiliation:
Laboratório de Fitotecnia, Centro de Ciências Tecnológicas e Agropecuárias, Universidade Estadual do Norte Fluminense, Av. Alberto Lamego, 2000, Parque Califórnia, Campos dos Goytacazes, RJ, 28013-602, Brazil
Leonardo Siqueira Glória
Affiliation:
Laboratório de Zootecnia, Centro de Ciências Tecnológicas e Agropecuárias, Universidade Estadual do Norte Fluminense, Av. Alberto Lamego, 2000, Parque Califórnia, Campos dos Goytacazes, RJ, 28013-602, Brazil
Clóvis de Paula Santos*
Affiliation:
Laboratório de Biologia Celular e Tecidual, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Av. Alberto Lamego, 2000, Parque Califórnia, Campos dos Goytacazes, RJ28013-602, Brazil
*
Author for correspondence: Clóvis de Paula Santos, E-mails: [email protected], [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Medicinal plants have been the focus of several studies due to their nematicide properties which can be used to control nematodes in sheep. No study has examined the morphological effects of Cymbopogon citratus on nematodes. Thus, this study evaluated the chemical composition, nematicidal activity and effects of C. citratus extracts on the morphology of eggs and infective larvae (L3) of sheep. Aqueous and methanolic extracts and fractions of C. citratus were obtained and analysed in vitro. The C. citratus extracts were effective against Haemonchus spp. and Trichostrongylus spp. larvae and eggs. Ten fractions were obtained from C. citratus, six of which had high ovicidal activity at 1000 μg mL−1, and two fractions had high activity at all tested concentrations. The phytochemical analysis identified the presence of compounds such as terpenoids, various ketones, esters, and fatty acids. The ultrastructural analysis showed deformations of the cuticle and wilting along the body of the nematodes at all concentrations. The muscular layer, intestinal cells and the mitochondria profile showed damage compared to the typical pattern. Ultra-thin sections of eggs treated with methanolic fractions of C. citratus presented modifications. This study showed the biological activity and effects of C. citratus on the gastrointestinal nematodes in sheep.

Keywords

Cymbopogon citratusgastrointestinal nematodessheepsmall ruminants
Type
Research Article
Information
Parasitology , Volume 147 , Issue 13 , November 2020 , pp. 1559 - 1568
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abegaz, B, Yohannes, PG and Dieter, RK (1983) Constituents of the essential oil of Ethiopian Cymbopogon citratus Stapf. Journal of Natural Products 46, 424–426.CrossRefGoogle Scholar
Ademola, IO and Eloff, JN (2011) Anthelmintic activity of acetone extract and fractions of Vernonia amygdalina against Haemonchus contortus eggs and larvae. Tropical Animal Health and Production 43, 521–527.CrossRefGoogle ScholarPubMed
Ahmed, M, Laing, MD and Nsahlai, IV (2013) In vitro Anthelmintic activity of crude extracts of selected medicinal plants against Haemonchus contortus from sheep. Journal of Helminthology 87, 174–179.CrossRefGoogle ScholarPubMed
Ahmed, M, Laing, MD and Nsahlai, IV (2014) In vivo Effect of selected medicinal plants against gastrointestinal nematodes of sheep. Tropical Animal Health and Production 46, 411–417. .CrossRefGoogle ScholarPubMed
Almeida, MA, Botura, MB, Santos, MM, Domingues, LF, Costa, SL and Batatinha, MJM (2003) Efeitos dos extratos aquosos de folhas de Cymbopogon citratus (DC.) stapf (capim-santo) e de Digitaria insularis (L.) fedde (capim-açu) sobre cultivos de larvas de nematóides gastrintestinais de caprinos. Revista Brasileira de Parasitol Veterinária 129, 125–129.Google Scholar
Andre, WPP, Ribeiro, WLC, Cavalcante, GS, Santos, JML, Macedo, ITF, de Paula, HCB, Freitas, RM, Morais, SM, Melo, JV and Bevilaqua, CML (2016) Comparative efficacy and toxic effects of carvacryl acetate and carvacrol on sheep gastrointestinal nematodes and mice. Veterinary Parasitology 218, 52–58.CrossRefGoogle ScholarPubMed
Armstrong, SA, Klein, DR, Whitney, TR, Scott, CB, Muird, JP, Lambert, BD and Craig, TM (2013) Effect of using redberry juniper (Juniperus pinchotii) to reduce Haemonchus contortus in vitro motility and increase ivermectin efficacy. Veterinary Parasitology 197, 271–276.CrossRefGoogle ScholarPubMed
Barbosa, LCA, Pereira, UA, Martinazzo, AP, Maltha, CRA, Teixeira, RR and Melo, EC (2008) Evaluation of the chemical composition of Brazilian commercial Cymbopogon citratus (D.C.) Stapf samples. Molecules 13, 1864–1874.CrossRefGoogle Scholar
Barbosa, P, Lima, AS, Vieira, P, Dias, LS, Tinoco, MT, Barroso, JG, Pedro, LG, Figueiredo, AC and Mota, M (2010) Nematicidal activity of essential oils and volatiles derived from Portuguese aromatic flora against the pinewood nematode, Bursaphelenchus xylophilus. Journal of Nematology 42, 8–16.Google ScholarPubMed
Bassolé, IH, Lamien-Meda, A, Bayala, B, Obame, LC, Ilboudo, AJ, Franz, C, Novak, J, Nebié, RC and Dicko, MH (2011) Chemical composition and antimicrobial activity of Cymbopogon citratus and Cymbopogon giganteus essential oils alone and in combination. Phytomedicine: International Journal of Phytotherapy and Phytopharmacology 18, 1070–1074.Google ScholarPubMed
Bird, AF and Bird, J (1991) The Structure of Nematodes. San Diego, New York: Academic Press.Google Scholar
Bizimenyera, ES, Githiori, JB, Eloff, JN and Swan, GE (2006). In vitro activity of Peltophorum africanum Sond. (Fabaceae) extracts on the egg hatching and larval development of the parasitic nematode Trichostrongylus colubriformis. Veterinary Parasitology 142, 336–346.10.1016/j.vetpar.2006.06.013CrossRefGoogle ScholarPubMed
Bonadiman, SF, Ederli, NB, Soares, AKP, Moraes Neto, AHA, Santos, CP and DaMatta, RA (2006) Occurrence of Libyostrongylus sp. (Nematoda) in ostriches (Struthio camelus Linnaeus, 1758) from the north region of the state of Rio de Janeiro, Brazil. Veterinary Parasitology 37, 175–179.CrossRefGoogle Scholar
Botura, MB, dos Santos, JD, da Silva, GD, de Lima, HG, de Oliveira, JVA, de Almeida, MAO, Batatinha, MJM and Branco, A (2013) In vitro Ovicidal and larvicidal activity of Agave sisalana Perr. (sisal) on gastrointestinal nematodes of goats. Veterinary Parasitology 192, 211–217.CrossRefGoogle ScholarPubMed
Brunet, S, Fourquaux, I and Hoste, H (2011) Ultrastructural changes in the third-stage, infective larvae of ruminant nematodes treated with sainfoin (Onobrychis viciifolia) extract. Parasitology International 60, 419–424.CrossRefGoogle ScholarPubMed
Cavalcante, GS, Morais, SM, Andre, WPP, Ribeiro, WLC, Rodrigues, ALM, De Lira, FCML, Viana, JM and Bevilaqua, CML (2016) Chemical composition and in vitro activity of Calotropis procera (Ait.) latex on Haemonchus contortus. Veterinary Parasitology 226, 22–25.CrossRefGoogle ScholarPubMed
Chagas, ACS (2004) Controle de Parasitas utilizando extratos vegetais. Revista Brasileira de Parasitologia Veterinária 13, 156–160.Google Scholar
Chisowa, EH, Hall, DR and Farman, DI (1998) Volatile constituents of the essential oil of Cymbopogon citratus Stapf grown in Zambia. Flavour and Fragrance Journal 13, 29–30.3.0.CO;2-S>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, 35–44.CrossRefGoogle ScholarPubMed
Decraemer, W, Karanastasi, E, Brown, D and Backeljau, T (2003) Review of the ultrastructure of the nematode body cuticle and its phylogenetic interpretation. Biological Review 78, 465–510.CrossRefGoogle ScholarPubMed
Eguale, T and Giday, M (2009) In vitro Anthelmintic activity of three medicinal plants against Haemonchus contortus. International Journal of Green Pharmacy 3, 29–34.CrossRefGoogle Scholar
Fabiyi, OA, Olatunji, GA, Adebayo, MO and Atolani, O (2018) Effect of thermal degraded products of Cymbopogon citratus on the In Vitro survival of Meloidogyne incognita eggs and juveniles. Ceylon Journal of Science 47, 235–239.CrossRefGoogle Scholar
Giovanelli, F, Mattellini, M, Fichi, G, Flamini, G and Perrucci, S (2018) In vitro Anthelmintic activity of four plant-derived compounds against sheep gastrointestinal Nematodes. Veterinary Sciences 5, 78.CrossRefGoogle ScholarPubMed
Gomes, DC, Lima, HG, Vaz, AV, Santos, NS, Santos, FO, Dias, ER, Botura, MB, Branco, A and Batatinha, MJM (2016) In vitro Anthelmintic activity of the Zizyphus joazeiro bark against gastrointestinal nematodes of goats and its cytotoxicity on vero cells. Veterinary Parasitology 226, 10–16.Google ScholarPubMed
Gordon, HM and Whitlock, HV (1939) A new technique for counting nematode eggs in sheep faeces. Journal of the Council for Scientific and Industrial Research 12, 50–52.Google Scholar
Gupta, BK and Jam, N (1978) Cultivation and utilization of genus Cymbopogon In Indian. Indian Perfumer 22, 55–68.Google Scholar
Hansen, J and Perry, B (1994) The Epidemiology, Diagnosis and Control of Helminth Parasites of Ruminants. Nairobi, Kenya: International Laboratory for Research on Animal Diseases.Google Scholar
Hernando, G, Turani, O and Bouzat, C (2019) Caenorhabditis elegans muscle Cys-loop receptors as novel targets of terpenoids with potential anthelmintic activity. PLoS Neglected Tropical Diseases 13, e0007895.Google ScholarPubMed
Hounzangbe-Adote, MS, Paolini, V, Fouraste, I, Moutairou, K and Hoste, H (2005) In vitro Effects of four tropical plants on three life-cycle stages of the parasitic nematode, Haemonchus contortus. Research Veterinary Science 78, 155–160.CrossRefGoogle ScholarPubMed
Kamaraj, C, Rahuman, AA, Elango, G, Bagavan, A and Zahir, AA (2011) Anthelmintic activity of botanical extracts against sheep gastrointestinal nematodes, Haemonchus contortus. Parasitology Research 109, 37–45.CrossRefGoogle ScholarPubMed
Leathwick, DM and Besier, RB (2014) The management of anthelmintic resistance in grazing ruminants in Australasia—strategies and experiences. Veterinary Parasitology 204, 44–54.CrossRefGoogle ScholarPubMed
Macedo, ITF, Bevilaqua, CML, Oliveira, LMB, Camurça-Vasconcelos, ALF, Vieira, LS, Oliveira, FR, Queiroz-Junior, EM, Tomé, AR and Nascimento, NRF (2010) Anthelmintic effect of Eucalyptus staigeriana essential oil against goat gastrointestinal nematodes. Veterinary Parasitology 173, 93–98.CrossRefGoogle ScholarPubMed
Macedo, IT, Oliveira, LM, Ribeiro, WL, Santos, JM, Silva, KD, AraújoFilho, JV, CamurçaVasconcelos, AL and Bevilaqua, CM (2015) Anthelmintics activity of Cymbopongon citratus Against Haemonchus contortus. Revista Brasileira de Parasitologia Veterinária 24, 268–275.Google ScholarPubMed
Macedo, IT, Oliveira, LMB, André, WPP, Araújo Filho, JV, Santos, JML, Rondon, FCM, Ribeiro, WLC, Camurça-Vasconcelos, ALF, Oliveira, EF, de Paula, HCB and Bevilaqua, CML (2019) Anthelmintic effect of Cymbopogon citratus essential oil and its nanoemulsion on sheep gastrointestinal nematodes. Revista Brasileira de Parasitologia Veterinária 28, 522–527.CrossRefGoogle ScholarPubMed
Maestrini, M, Tava, A, Mancini, S, Salari, F and Perrucci, S (2019) In vitro Anthelmintic activity of saponins derived from Medicago Spp. Plants against donkey gastrointestinal nematodes. Veterinary Sciences 6, 35.CrossRefGoogle ScholarPubMed
Maestrini, M, Tava, A, Mancini, S, Tedesco, D and Perrucci, S (2020) In vitro Anthelmintic activity of saponins from Medicago spp. against sheep gastrointestinal nematodes. Molecules 25, 242.CrossRefGoogle ScholarPubMed
Martínez-Ortíz-de-Montellano, C, Arroyo-López, C, Fourquaux, I, Torres-Acosta J, FJ, Sandoval-Castro, CA and Hoste, H (2013) Scanning electron microscopy of Haemonchus contortus exposed to tannin-rich plants under in vivo and in vitro conditions. Experimental Parasitology 133, 281–286.CrossRefGoogle ScholarPubMed
McLeod, RS (1995) Costs of major parasites to the Australian livestock industries. International Journal for Parasitology 25, 1363–1367.CrossRefGoogle ScholarPubMed
Mohamed Hanna, AR, Sallaam, YI, El-Leity, AS and Safaa, EA (2012) Lemongrass (Cymbopogon citratus) essential oil as affected by drying methods. Annals of Agricultural Sciences 57, 113–116.CrossRefGoogle Scholar
Oka, Y, Nacar, S, Putievsky, E, Ravid, U, Yaniv, Z and Spiegel, Y (2000) Nematicidal activity of essential oils and their components against the root-knot nematode. Phytopathology 90, 710–715.CrossRefGoogle ScholarPubMed
Pineda-Alegria, JA, Sanchez-Vazquez, JE, Gonzalez-Cortazar, M, Zamilpa, A, Lopez-Arellano, ME, Cuevas-Padilla, EJ, Mendoza-de-Gives, P and Aguilar-Marcelino, L (2017) The edible mush- room Pleurotus Djamor produces metabolites with lethal activity against the parasitic nematode Haemonchus contortus. Journal of Medical Food 20, 1184–1192.CrossRefGoogle Scholar
Ritter, RA, Monteiro, MVB, Monteiro, FOB, Rodrigues, ST, Soares, ML, Silva, JCR, Md, Palha, Biondi, GF, Rahal, SC and Tourinho, MM (2012) Ethnoveterinary knowledge and practices at Colares Island, Pará state, eastern Amazon, Brazil. Journal of Ethnopharmacology 144, 346–352.CrossRefGoogle ScholarPubMed
Saddiq, A and Khayyat, S (2010) Chemical and antimicrobial studies of monoterpene: Citral. Pesticide Biochemistry and Physiology 98, 89–93.CrossRefGoogle Scholar
Salgado, JA and Santos, CP (2016) Overview of anthelmintic resistance of gastrointestinal nematodes of small ruminants in Brazil. Revista Brasileira de Parasitologia Veterinária 25, 3–17.CrossRefGoogle ScholarPubMed
Santos, ACV, Santos, FO, Lima, HG, Silva, GDD, Uzêda, RS, Dias, ÊR, Branco, A, Cardoso, KV, David, JM, Botura, MB, Costa, SL and Batatinha, MJM (2018) In vitro Ovicidal and larvicidal activities of some saponins and flavonoids against parasitic nematodes of goats. Parasitology 145, 1884–1889.CrossRefGoogle ScholarPubMed
Santos, FO, Cerqueira, APM, Branco, A, Batatinha, MJM and Botura, MB (2019) Anthelmintic activity of plants against gastrointestinal nematodes of goats: a review. Parasitology 146, 1233–1246.CrossRefGoogle Scholar
Silva, WW, Brito, AFS, Marinho, FA, Rodrigues, OG and Athayde, ACR (2005) Ação do extrato alcoólico do capim santo (Cymbopogon citratus (DC) Stapf) sobre nematóides gastrintestinais de ovinos. Agropecuária Científica no Semi Árido 1, 46–49.Google Scholar
Sindan, (2018) Available at http://www.sindan.org.br/sd/base.aspx?controle=8 (Accessed in March 2020).Google Scholar
Souza, W (2007) Técnicas de microscopia eletrônica aplicadas às Ciências Biológicas. Rio de Janeiro: Sociedade Brasileira de Microscopia.Google Scholar
Tajidin, NE, Ahmad, SH, Rosenani, AB, Azimah, H and Munirah, M (2012) Chemical composition and citral content in lemongrass (Cymbopogon citratus) essential oil at three maturity stages. African Journal of Biotechnology 11, 2685–2693.CrossRefGoogle Scholar
Torres, RC and Ragadio, AG (1996) Chemical composition of the essential oil of Philippine Cymbopogon citratus (DC) Stapf. Philippine Journal of Science 125, 147–156.Google 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, 39–553.Google Scholar
Van Wyk, JA, Cabaret, J and Michael, LM (2004) Morphological identification of nematode larvae of small ruminants and cattle simplified. Veterinary Parasitology 119, 277–306.CrossRefGoogle ScholarPubMed
Villaseñor, IM, Angelada, J, Canlas, AP and Echegoyen, D (2002) Bioactivity studies on β-sitosterol and its glucoside. Phytotherapy Research 16, 417–421.CrossRefGoogle ScholarPubMed
Yoshihara, E, Minho, AP, Tabacow, VBD, Cardim, ST and Yamamura, MH (2015) Ultrastructural changes in the Haemonchus contortus cuticle exposed to Acacia mearnsii extract. Semina: Ciências Agrárias 36, 3763–3768.Google Scholar
Zhu, L, Dai, J, Yang, L and Qiu, J (2013) Anthelmintic activity of Arisaema franchetianum and Arisaema lobatum essential oils against Haemonchus contortus. Journal of Ethnopharmacology 148, 311–316.CrossRefGoogle ScholarPubMed
Supplementary material: File

Rocha et al. supplementary material

Figures S1-S2

Download Rocha et al. supplementary material(File)
File 144.8 KB