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Nematicidal activity of leaf extract of Moringa oleifera Lam. against Haemonchus contortus and Nacobbus aberrans

Published online by Cambridge University Press:  23 February 2022

S.Y. Páez-León
Affiliation:
Area de Helmintología, CENID-Salud Animal e Inocuidad, INIFAP, Carretera Federal Cuernavaca-Cuautla No. 8534, Col. Progreso, CP 62550. Jiutepec, Morelos, Mexico Universidad Politécnica del Estado de Morelos, Boulevard Cuauhnáhuac #566, Col. Lomas del Texcal, CP 62550, Jiutepec, Morelos, Mexico
M. Carrillo-Morales
Affiliation:
Universidad Politécnica del Estado de Morelos, Boulevard Cuauhnáhuac #566, Col. Lomas del Texcal, CP 62550, Jiutepec, Morelos, Mexico
O. Gómez-Rodríguez
Affiliation:
Colegio de Postgraduados, Campus Montecillo, Km. 36.5, México 136 5, Montecillo, CP 56230, Montecillo, Mexico
G. López-Guillén
Affiliation:
Campo Experimental Rosario Izapa, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias (INIFAP), Tuxtla Chico, Chiapas, C. P. 30780, Mexico
G.S. Castañeda-Ramírez
Affiliation:
Area de Helmintología, CENID-Salud Animal e Inocuidad, INIFAP, Carretera Federal Cuernavaca-Cuautla No. 8534, Col. Progreso, CP 62550. Jiutepec, Morelos, Mexico
E. Hernández-Núñez
Affiliation:
Centro de Investigaciones y de Estudios Avanzados del Instituto Politécnico Nacional, Departamento de Recursos del Mar, Unidad Mérida, Carretera antigua a Progreso Km. 6, CP 97310, Mérida, Yucatán, Mexico
A. Wong-Villarreal
Affiliation:
División Agroalimentaria; Universidad Tecnológica de la Selva, Entronque Toniná Km. 0.5, CP 29950, Ocosingo, Chiapas, Mexico
L. Aguilar-Marcelino*
Affiliation:
Area de Helmintología, CENID-Salud Animal e Inocuidad, INIFAP, Carretera Federal Cuernavaca-Cuautla No. 8534, Col. Progreso, CP 62550. Jiutepec, Morelos, Mexico
*
Author for correspondence: L. Aguilar-Marcelino, E-mail: [email protected]

Abstract

In the present study, the nematicidal activity of a Moringa oleifera ethyl acetate leaf extract against the eggs and larvae of Haemonchus contortus and Nacobbus aberrans, nematodes of agricultural importance, was evaluated. The experimental design for the evaluation of the effects against both nematodes consisted of eight treatments (n = 4). Distilled water, Tween (4%) and a commercial anthelmintic agent (ivermectin, 5 mg/mL) were used as controls, and for treatments 4–8, the concentrations of the extract were 20, 10, 5, 2.5 and 1.25 mg/mL, respectively. Readings were taken at 12 h and 24 h for N. aberrans and 48 h and 72 h for H. contortus post-treatment under an optical microscope (10× and 40×). The data obtained were analysed by analysis of variance through a completely randomized factorial design using the SAS V9 program. The results show that, for H. contortus egg hatching, 85.88% inhibition was obtained at a concentration of 20 mg/mL at 48 h, while for third-stage larva (L3) mortality, the highest percentage was 68.19% at 1.25 mg/mL at 72 h. In the case of N. aberrans, the greatest inhibition of egg hatching was 90.69% at 5 mg/mL at 12 h post-treatment, and for larval mortality, it was 100% at 10 mg/mL at 24 h post-treatment. The main major compounds identified by qualitative analysis and by gas chromatography coupled to mass spectrometry were 9,12,15-octadecatrienoic acid, (Z,Z,Z)-, n-hexadecanoic acid and 2,4-di-tert-butylphenol, and the minor compounds included phytol, γ-sitosterol and α-tocopheryl acetate. It was demonstrated that the ethyl acetate leaf extract of M. oleifera Lam. shows great potential for combating agricultural nematodes.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Abbott, KA, Taylor, M and Stubbings, LA (2012) Sustainable Worm Control Strategies for Sheep—A technical manual for veterinary surgeons and advisers. SCOPS, UK. 58p. www.scops.org.uk.Google Scholar
Ali, R, Rooman, M, Mussarat, S, Norin, S, Ali, S, Adnan, M and Khan, SN (2021) A systematic review on comparative analysis, toxicology, and pharmacology of medicinal plants against Haemonchus contortus. Frontiers in Pharmacology 12, 644027.10.3389/fphar.2021.644027CrossRefGoogle ScholarPubMed
Alvindia, DdG and Mangoba, MAA (2020) Biological activities of Moringa oleífera Lam. against anthracnose of mango caused by Colletotrichum gloesporioides Penz. Archives of Phytopathology and Plant Protection 53, 659672.10.1080/03235408.2020.1791479CrossRefGoogle Scholar
Audu, SA, Mohammed, I and Kaita, HA (2007) Phytochemical screening of the leaves of Lophira lanceolata (ochanaceae). Life Science Journal 4(4), 7579.Google Scholar
Bakare, SB and Ghareeb, MA (2019) Chemical profile, antimicrobial and antioxidant activities of Moringa oleifera Lam leaves grown in Saudi Arabia. Mens Agitat 14, 4552.Google Scholar
Barreto, MB, Freitas, JVBD, Silveira, ER, Bezerra, AME, Nunes, EP and Gramosa, NV (2009) Constituintes químicos voláteis e não-voláteis de Moringa oleifera Lam., Moringaceae. Revista Brasileira de Farmacognosia 19, 893897.10.1590/S0102-695X2009000600018CrossRefGoogle Scholar
Bauer, B, Pomroy, WE, Gueydon, J, Gannac, S, Scott, I and Pfister, K (2010) Comparison of the FLOTAC technique with the McMaster method and the Baermann technique to determine counts of Dictyocaulus eckerti L1 and strongylid eggs in faeces of red deer (Cervus elaphus). Parasitology Research 107, 555560.10.1007/s00436-010-1893-zCrossRefGoogle Scholar
Cabardo, DE and Portugaliza, HP (2017) Actividad antihelmíntica de extractos acuosos y etanólicos de semillas de Moringa oleifera contra huevos de Haemonchus contortus y larvas de tercer estadio. Revista Internacional de Ciencia Y Medicina Veterinarias 5(1), 3034.Google Scholar
Doménech-Asensi, G, Durango- Villaadiego, AM and Ros- Berruezo, G (2017) Moringa oleifera: revisión sobre aplicaciones y usos en alimentos. Archivos Latinoamericanos de Nutrición 67(2), 8697.Google Scholar
Fujimoto, T, Abe, H, Mizukubo, T and Seo, S (2021) Phytol, a constituent of chlorophyll, induces root-knot nematode resistance in Arabidopsis via the ethylene signaling pathway. Molecular Plant-Microbe Interactions 34(3), 279285.10.1094/MPMI-07-20-0186-RCrossRefGoogle ScholarPubMed
Gómez-Valdez, L (2016). Potencial nematicida de un metabolito secundario producido por Serratia sp. (Enterobacteriales: Enterobacteriaceae) sobre Nacobbus aberrans (Tylenchida: Pratylenchidae). Centro de Zoología Aplicada. Universidad Nacional de Córdoba.Google Scholar
González-Garduño, R, Torres-Hernández, G, López-Arellano, ME and Mendoza-de-Gives, P (2012) Resistencia antihelmíntica de nematodos parásitos en ovinos. Revista de Geografía Agrícola 48-49, 6374.Google Scholar
Guaycha-Pérez, N, Jaramillo-Jaramillo, C, Cuenca-Buele, S, Tocto-León, J and Márquez-Hernández, I (2017) Estudios farmacognósticos y toxicológicos preliminares de hojas, tallo y raíz de Moringa (Moringa oleifera Lam). Revista Ciencia UNEM 10(22), 6068.10.29076/issn.2528-7737vol10iss22.2017pp60-68pCrossRefGoogle Scholar
Jackson, F and Hoste, H (2010) In vitro methods for the primary screening of plant products for direct activity against ruminant gastrointestinal nematodes. pp. 2545 in Vercoe, PE, Makkar, HPS and Schlink, AC (Eds) In vitro screening of plant resource for extra-nutritional attributes in ruminants: Nuclear and related methodologies. Dordrecht (Netherlands), Springer.10.1007/978-90-481-3297-3_3CrossRefGoogle Scholar
Khandelwal, S, Rishi, A and Khurana, SM (2014) Estimación de metabolitos primarios y secundarios de hojas de tres plantas medicinales. Revista Internacional de Investigación de Farmacia 5, 783785.Google Scholar
Kimbaris, AC, Siatis, NG, Daferera, DJ, Tarantilis, PA, Pappas, CS and Polissiou, MG (2006) Comparison of distillation and ultrasound-assisted extraction methods for the isolation of sensitive aroma compounds from garlic (Allium sativum). Ultrasonic Sonochem 13(1), 5460.10.1016/j.ultsonch.2004.12.003CrossRefGoogle Scholar
Koul, O and Walia, S (2009) Comparing impacts of plant extracts and pure allelochemicals and implications for pest control. pp. 130 in CAB reviews: perspectives in agriculture, veterinary science, nutrition and natural resources. Wallingford, UK, CAB International Publishing.Google Scholar
Liébano, HE, López-Arellano, ME, Mendoza-de-Gives, P and Aguilar-Marcelino, L (2011). Manual de diagnóstico para la identificación de larvas de nematodos gastrointestinales en rumiantes. Special Handbook No. 2. pp. 1-48. Morelos, México, INIFAP.Google Scholar
Linares-Rivero, C, Quiñones-Gálvez, J, Pérez-Martínez, AT, Carvajal-Ortiz, CC, Rivas-Paneca, M, Cid-Valdéz, GA, Pérez-Gómez, L, La-Rosa-González, S and Capdesuñer-Ruiz, YK (2018) Obtención de extractos fenólicos foliares de Moringa oleifera Lam mediante el uso de diferentes métodos de extracción. Biotecnología Vegetal 18(1), 4756.Google Scholar
Mancilla-Montelongo, G, Castañeda-Ramírez, GS, Torres-Acosta, JF, Sandoval-Castro, C and Borges-Argáez, R (2019) Evaluation of cinnamic acd and six analogues against eggs and larvae of Haemonchus contortus. Veterinary Parasitology 270, 2530.10.1016/j.vetpar.2019.05.009CrossRefGoogle Scholar
Marie-Magdeleine, C, Udino, L, Philibert, L, Bocage, B and Archimede, H (2010) Efectos in vitro de extractos de hojas de yuca (Manihot esculenta) en cuatro etapas de desarrollo de Haemonchus contortus. Veterinary Parasitology 173, 8592.10.1016/j.vetpar.2010.06.017CrossRefGoogle Scholar
Mayoral-Peña, Z, Piña-Vázquez, DM, Gómez-Sánchez, M, Salazar-Olivo, LA, Aguilar-Tipacamú, G and Arellano-Carbajal, F (2017) El nematodo caenorhabditis elegans como modelo para evaluar el potencial antihelmíntico de extractos de plantas. Revista mexicana de Ciencias Pecuarias 8(3), 279289.10.22319/rmcp.v8i3.4504CrossRefGoogle Scholar
Mbogning-Tayo, G, Wabo-Poné, J, Komtangi, MC, Yondo, J, Ngangout, AM and Mbida, M (2014) Anthelminthic activity of Moringa oleifera leaf extracts evaluated in vitro on four developmental stages of Haemonchus contortus from goats. American Journal of Plant Sciences 05, 17021710.10.4236/ajps.2014.511185CrossRefGoogle Scholar
Ministry of Agriculture, Fisheries and Food (MAFF) (1986) Manual of veterinary parasitological laboratory techniques. 3rd edn, ADAS, HMSO, UK. 160 pp.Google Scholar
Nogueira, BRS, Alencar, SJ, Santos, PV, et al. (2017) Research advances on the multiple uses of Moringa oleifera: a sustainable alternative for socially neglected population. Asian Pacific Journal of Tropical Medicine 10(7), 621630.Google Scholar
Pant, DR, Pant, ND, Saru, DB, Yadav, UN and Khanal, DP (2017) Phytochemical screening and study of antioxidant, antimicrobial, antidiabetic, anti-inflammatory and analgesic activities of extracts from stem wood of Pterocarpus marsupium Roxburgh. Journal of Intercultural Ethnopharmacology 6(2), 170176.10.5455/jice.20170403094055CrossRefGoogle ScholarPubMed
Pineda-Alegría, JA, Sánchez, J, González-Cortazar, M, Zamilpa, A, López-Arellano, M, Cuevas-Padilla, E, Mendoza-de-Gives, P and Aguilar-Marcelino, L (2017) The edible mushroom Pleurotus djamor produces metabolites with lethal activity against the parasitic nematode Haemonchus contortus. Journal of Medicinal Food 20, 11841192.10.1089/jmf.2017.0031CrossRefGoogle ScholarPubMed
Pineda-Alegría, JA, Sánchez, JE, González-Cortazar, M, von Son-de Fernex, E, González-Garduño, R, Mendoza-de Gives, P, Zamilpa, A and Aguilar-Marcelino, L (2020) In vitro nematocidal activity of commercial fatty acids and β-sitosterol against Haemonchus contortus. Journal of Helminthology 94, e135.10.1017/S0022149X20000152CrossRefGoogle ScholarPubMed
Puerto-Abreu, M, Arece-García, J, López-Leyva, Y, Roche, Y, Molina, M, Sanavria, A and da Fonseca -Adivaldo, H (2014) Efecto in vitro de extractos acuosos de Moringa oleifera y Gliricida sepium en el desarrollo de las fases exógenas de estrongílidos gastrointestinales de ovinos. Revista de Salud Animal 36(1), 2834.Google Scholar
Rocha, L, Lemos, G, Vieira, I, Braz-Filho, R, Freitas, SP, Glória, LS and Santos, CP (2020) Chemical characterization and in vitro biological activity of Cymbopogon citratus extracts against Haemonchus spp. and Trichostrongylus spp. nematodes from sheep. Parasitology 147(13), 15591568.10.1017/S0031182020001432CrossRefGoogle ScholarPubMed
Rodríguez-Chávez, JL, Franco-Navarro, F and Delgado, G (2019) Actividad nematicida in vitro de cadinenos naturales y semisintéticos de Heterotheca inuloides contra el nematodo parásito de las plantas Nacobbus aberrans (Tylenchida: Pratylenchidae). Pest Management Science 75(6), 17341742.10.1002/ps.5294CrossRefGoogle Scholar
Rodríguez-Vivas, RI, Arieta-Román, RJ, Pérez-Cogollo, LC, Rosado-Aguilar, JA, Ramírez-Cruz, GT and Basto-Estrella, G (2010) Uso de lactonas macrocíclicas para el control de la garrapata Rhipicepholus (Boophilus) microplus en el ganado bovino. Archivos de Medicina Veterinaria 42, 115123.10.4067/S0301-732X2010000300002CrossRefGoogle Scholar
Rodríguez-Vivas, RI, Rosado-Aguilar, JA, Ojeda-Chi, MM, Pérez-Cogollo, LC, Trinidad-Martínez, I and Bollo-González, ME (2014) Control integrado de garrapatas en la ganadería bovina. Ecosistemas Y Recursos Agropecuarios 1, 295308.Google Scholar
Romero-Benavides, JC, Ruano, AL, Silva-Rivas, R, Castillo-Ventimilla, P, Vivanco-Jaramillo, S and Bailon-Moscoso, N (2017) Medicinal plants used as anthelmintics: ethnomedical, pharmacological, and phytochemical studies. European Journal of Medicinal Chemistry 129(31), 209217.10.1016/j.ejmech.2017.02.005CrossRefGoogle ScholarPubMed
Salas-Zapata, R, Velásquez-Vélez, R, Herrera-Ospina, LV, Ríos-Osorio, L and Polanco-Echeverry, D (2016) Prevalencia de nematodos gastrointestinales En sistemas de producción Ovina y Caprina bajo confinamiento, semiconfinamiento y pastoreo En municipios de Antioquia, Colombia. Revista de Investigaciones Veterinarias Del Perú 27(2), 344354.10.15381/rivep.v27i2.11647CrossRefGoogle Scholar
SAS 9.2 (2009) Statistical analysis system, SAS Institute Inc, Cary, NC, USA.Google Scholar
Sepúlveda-Vázquez, J, Torres-Acosta, JF, Sandoval-Castro, CA, Martínez-Puc, JF and Chan-Pérez, JI (2018) La importancia de los metabolitos secundarios en el control de nematodos gastrointestinales en ovinos con énfasis en Yucatán, México. Journal of the Selva Andina Animal Science 5(2), 7995.10.36610/j.jsaas.2018.050200079CrossRefGoogle Scholar
Shaikh, JR and Patil, MK (2020) Qualitative tests for preliminary phytochemical screening: an overview. International Journal of Chemical Studies 8(2), 603608.10.22271/chemi.2020.v8.i2i.8834CrossRefGoogle Scholar
Sousa, A, Souza, P, Gifoni, JM, Dias, LP, Freitas, C, Oliveira, J and Vasconcelos, IM (2019) Scanning electron microscopy reveals deleterious effects of Moringa oleifera seed exuded proteins on root-knot nematode Meloidogyne incognita eggs. International Journal of Biological Macromolecules 154, 12371244.10.1016/j.ijbiomac.2019.10.278CrossRefGoogle ScholarPubMed
Torres-Acosta, JFJ, Chan-Pérez, I, López-Arellano, ME, et al. (2015) Diagnóstico de resistencia a los antiparasitarios en rumiantes. pp. 355403 in Rodriguez-Vivas, RI (Ed) Técnicas para el diagnóstico de parásitos con importancia en salud pública y veterinaria. México, AMPAVE-CONASA.Google Scholar
Vargas-Magaña, JJ, Torres-Acosta, JF, Aguilar-Caballero, AJ, Sandoval-Castro, CA, Hoste, H and Chan-Pérez, JA (2014) Anthelmintic activity of acetone-water extracts against Haemonchus contortus eggs: interactions between tannins and other plant secondary compounds. Veterinary Parasitoly 206(3–4), 322327.10.1016/j.vetpar.2014.10.008CrossRefGoogle ScholarPubMed
Vats, S and Gupta, T (2017) Evaluation of bioactive compounds and antioxidant potential of hydroethanolic extract of Moringa oleifera Lam. from Rajasthan, India. Physiology and Molecular Biology Plants 23, 239248.10.1007/s12298-016-0407-6CrossRefGoogle ScholarPubMed
Velázquez-Zavala, M, Peón-Escalante, IE, Zepeda-Bautista, R and Jiménez-Arellanes, MA (2016) Moringa (Moringa oleifera Lam.): potential uses in agriculture, industry and medicine. Revista Chapingo Serie Horticultura 22(2), 95116.10.5154/r.rchsh.2015.07.018CrossRefGoogle Scholar
Villar-Luna, E, Zavaleta-Mejía, E, Rojas-Martínez, RI, Gómez-Rodríguez, O, Reyes-Trejo, B and Hernández-Anguiano, AM (2009) Respuesta hipersensitiva en el follaje de Chile CM-334 resistente a Phytophthora capsici infectado con Nacobbus aberrans. Nematropica 39, 143155.Google Scholar
Vimalkumar, CS, Hosagaudar, VB, Suja, SR, Vilash, V, Krishnakumar, NM and Latha, PG (2014) Comparative preliminary phytochemical analysis of ethanolic extracts of leaves of Olea dioica Roxb., infected with the rust fungus Zaghouania oleae (E.J. Butler) Cummins and non-infected plants. Journal of Pharmacognosy and Phytochemistry 3(4), 6972.Google Scholar
Vrain, TC (1977) A technique for the collection of larvae of Meloidogyne spp. and a comparison of eggs and larvae as inocula. Journal of Nematology 9, 249.Google Scholar