Skip to main content
Erschienen in: Comparative Clinical Pathology 1/2018

25.10.2017 | Original Article

Lysiloma acapulcensis leaves contain anthelmintic metabolites that reduce the gastrointestinal nematode egg population in sheep faeces

verfasst von: Manases González-Cortazar, Alejandro Zamilpa, María Eugenia López-Arellano, Liliana Aguilar-Marcelino, David Emanuel Reyes-Guerrero, Sara Olazarán-Jenkins, Gabriel Ramírez-Vargas, Agustín Olmedo-Juárez, Pedro Mendoza-de-Gives

Erschienen in: Comparative Clinical Pathology | Ausgabe 1/2018

Einloggen, um Zugang zu erhalten

Abstract

One metabolite against lamb gastrointestinal nematodes (GIN) was identified from extracts of Lysiloma acapulcensis leaves. Firstly, an aqueous extract of L. acapulcensis leaves and two fractions, organic and aqueous, were evaluated at different concentrations against Haemonchus contortus eggs and histotrophic larvae. In other experiment, 35 Pelibuey GIN-infected lambs were randomly divided into five groups, as follows: (1) ivermectin (0.2 mg/kg BW); (2) control (untreated); (3) rutin (10 mg/kg BW, as a flavonoid comparison control); (4) L. acapulcensis leaves ethyl acetate fraction (EtAc-F, 25 mg/kg BW); and (5) L. acapulcensis leaves (dried and grinded, 5 g/kg BW). The EtAc-F fraction caused 94.8% egg-hatching inhibition (P < 0.05, 6.25 mg/ml). Likewise, at 50 mg/ml, this fraction resulted in 100% larval mortality. In the second experiment, the highest eggs per gram (EPG) of faeces reduction caused by ivermectin was 80.2% (ȳ = 61.8%); meanwhile, rutin showed a highest EPG reduction = 66.2% (ȳ = 37.5%). Similarly, EtAc-F fraction showed 62.9% EPG highest reduction (ȳ = 32.5%). On the other hand, lambs fed with L. acapulcensis leaves showed a maximum EPG reduction = 50.1% (ȳ = 29.4%). Chromatography analysis (HPLC; NRM) of EtAc-F fraction revealed the presence of myricitrin as a major compound. Lysiloma acapulcensis leaves EtAc-F exhibited the highest in vitro activity against H. contortus eggs and larvae. The low efficacy of ivermectin suggests the presence of anthelmintic resistance. Lysiloma acapulcensis leaves and fractions can be considered in future experiments searching for a sustainable alternative of GIN control.
Fußnoten
1
Note: rutin is a flavonoid with anthelmintic activity and it was included in this study as a control of comparison. The dose of this metabolite was estimated based on a bioavailability study in neonatal calves after oral administration of quercetin, aglycone, or rutin (Maceij et al. 2015).
 
Literatur
Zurück zum Zitat Arece J, Mahieu M, Archiméde H, Aumont G, Fernández M, González E, Cáceres O, Menéndez-Buxadera A (2004) Comparative efficacy of six anthelmintics for the control of nematodes in sheep in Matanzas, Cuba. Small Rumin Res 5(1–2):61–67CrossRef Arece J, Mahieu M, Archiméde H, Aumont G, Fernández M, González E, Cáceres O, Menéndez-Buxadera A (2004) Comparative efficacy of six anthelmintics for the control of nematodes in sheep in Matanzas, Cuba. Small Rumin Res 5(1–2):61–67CrossRef
Zurück zum Zitat Barrau E, Fabre N, Fouraste I, Hoste H (2005) Effect of bioactive compounds from Sainfoin (Onobrychis viciifolia Scop.) on the in vitro larval migration of Haemonchus contortus: role of tannins and flavonol glicosides. Parasitology 131:531–538CrossRefPubMed Barrau E, Fabre N, Fouraste I, Hoste H (2005) Effect of bioactive compounds from Sainfoin (Onobrychis viciifolia Scop.) on the in vitro larval migration of Haemonchus contortus: role of tannins and flavonol glicosides. Parasitology 131:531–538CrossRefPubMed
Zurück zum Zitat Camacho LM, Rojo R, Salem AZM, Provenza FD, Mendoza GD, Avilés F, Montañez-Valdez OD (2010) Effect of season on chemical composition and in situ degradability in cows and in adapted and unadapted goats of three Mexican browse species. Anim Feed Sci Technol 155:206–212CrossRef Camacho LM, Rojo R, Salem AZM, Provenza FD, Mendoza GD, Avilés F, Montañez-Valdez OD (2010) Effect of season on chemical composition and in situ degradability in cows and in adapted and unadapted goats of three Mexican browse species. Anim Feed Sci Technol 155:206–212CrossRef
Zurück zum Zitat Castillo-Mitre GF, Olmedo-Juárez A, Rojo-Rubio R, González-Cortazar M, Mendoza-de Gives P, Hernández-Beteta EE, Reyes-Guerrero DE, López-Arellano ME, Vazquez-Armijo JF, Ramírez-Vargas G, Zamilpa A (2017) Caffeoyl and coumaroyl derivatives from Acacia cochliacantha exhibit ovicidal activity against Haemonchus contortus. J Ethnopharmacol 204:125–131CrossRefPubMed Castillo-Mitre GF, Olmedo-Juárez A, Rojo-Rubio R, González-Cortazar M, Mendoza-de Gives P, Hernández-Beteta EE, Reyes-Guerrero DE, López-Arellano ME, Vazquez-Armijo JF, Ramírez-Vargas G, Zamilpa A (2017) Caffeoyl and coumaroyl derivatives from Acacia cochliacantha exhibit ovicidal activity against Haemonchus contortus. J Ethnopharmacol 204:125–131CrossRefPubMed
Zurück zum Zitat Craig H, Wastling M, Knox D (2006) A preliminary proteomic survey of the in vitro excretory/secretory products of fourth-stage larval and adult Teladorsagia circumcincta. Parasitology 132:535–543CrossRefPubMed Craig H, Wastling M, Knox D (2006) A preliminary proteomic survey of the in vitro excretory/secretory products of fourth-stage larval and adult Teladorsagia circumcincta. Parasitology 132:535–543CrossRefPubMed
Zurück zum Zitat Dupuy J, Larrieu G, Sutra JF, Lespine A, Alvineire M (2003) Enhancement of moxidectin bioavailability in lamb by natural flavonoid: quercertin. Vet Parasitol 112:337–347CrossRefPubMed Dupuy J, Larrieu G, Sutra JF, Lespine A, Alvineire M (2003) Enhancement of moxidectin bioavailability in lamb by natural flavonoid: quercertin. Vet Parasitol 112:337–347CrossRefPubMed
Zurück zum Zitat Encalada-Mena L, Tuyub-Solis H, Ramírez-Vargas G, Mendoza-de Gives P, Aguilar-Marcelino L, López-Arellano ME (2014) Phenotypic and genotypic characterization of Haemonchus contortus spp. and other gastrointestinal nematodes resistant to benzimidazole in infective calves from tropical regions of Campeche state, Mexico. Vet Parasitol 205:266–254CrossRef Encalada-Mena L, Tuyub-Solis H, Ramírez-Vargas G, Mendoza-de Gives P, Aguilar-Marcelino L, López-Arellano ME (2014) Phenotypic and genotypic characterization of Haemonchus contortus spp. and other gastrointestinal nematodes resistant to benzimidazole in infective calves from tropical regions of Campeche state, Mexico. Vet Parasitol 205:266–254CrossRef
Zurück zum Zitat Ferreira LE, Castro PMN, Chagas ACS, Franҫa SC, Beleboni RO (2013) In vitro anthelmintic activity of aqueous leaf extract of Annona muricata L. (Annonaceae) against Haemonchus contortus from sheep. Exp Parasitol 134:327–332CrossRefPubMed Ferreira LE, Castro PMN, Chagas ACS, Franҫa SC, Beleboni RO (2013) In vitro anthelmintic activity of aqueous leaf extract of Annona muricata L. (Annonaceae) against Haemonchus contortus from sheep. Exp Parasitol 134:327–332CrossRefPubMed
Zurück zum Zitat Grazziela JA, Coelho-dos-Reis A, Gomes O, Bertolini DE, Martins ML, Almeida MR, Martins CS, Carvalho LD, Souza JG, Vilela JMC, Andrade M, Barbosa-Stancioli EF (2011) Evaluation of the effects of quercertin and kaempherol on the surface of MT-2 cells visualized by atomic force microscopy. J Virol Methods 174:47–52CrossRef Grazziela JA, Coelho-dos-Reis A, Gomes O, Bertolini DE, Martins ML, Almeida MR, Martins CS, Carvalho LD, Souza JG, Vilela JMC, Andrade M, Barbosa-Stancioli EF (2011) Evaluation of the effects of quercertin and kaempherol on the surface of MT-2 cells visualized by atomic force microscopy. J Virol Methods 174:47–52CrossRef
Zurück zum Zitat Howell SB, Burke JM, Miller JE, Terrill TH, Valencia E, Williams MJ, Williamson LH, Zajac AM, Kaplan RM (2008) Prevalence of anthelmintic resistance on sheep and goat farms in the southeastern United States. J Am Vet Med Assoc 233:1913–1919CrossRefPubMed Howell SB, Burke JM, Miller JE, Terrill TH, Valencia E, Williams MJ, Williamson LH, Zajac AM, Kaplan RM (2008) Prevalence of anthelmintic resistance on sheep and goat farms in the southeastern United States. J Am Vet Med Assoc 233:1913–1919CrossRefPubMed
Zurück zum Zitat Jasso-Díaz G, Torres-Hernández G, Zamilpa A, Becerril-Pérez C, Ramírez-Bribesca JE, Hernández-Mendo O, Sánchez-Arroyo H, González-Cortazar M, Mendoza de Gives P (2017) In vitro assessment of Argemone mexicana, Taraxacumj officinale, Ruta chalepensis and Tagetes filifolia against Haemonchus contortus nematode eggs and infective (L3) larvae. Microb Pathog 109:162–168CrossRefPubMed Jasso-Díaz G, Torres-Hernández G, Zamilpa A, Becerril-Pérez C, Ramírez-Bribesca JE, Hernández-Mendo O, Sánchez-Arroyo H, González-Cortazar M, Mendoza de Gives P (2017) In vitro assessment of Argemone mexicana, Taraxacumj officinale, Ruta chalepensis and Tagetes filifolia against Haemonchus contortus nematode eggs and infective (L3) larvae. Microb Pathog 109:162–168CrossRefPubMed
Zurück zum Zitat Klongsiriwet C, Quijada J, Williams AR, Muller-Harvey I, Williamson EM, Hoste H (2015) Synergistic inhibition of Haemonchus contortus exsheathment by flavonoid monomers and condensed tannins. Int J Parasitol Drugs Drug Resist 5:127–134CrossRefPubMedPubMedCentral Klongsiriwet C, Quijada J, Williams AR, Muller-Harvey I, Williamson EM, Hoste H (2015) Synergistic inhibition of Haemonchus contortus exsheathment by flavonoid monomers and condensed tannins. Int J Parasitol Drugs Drug Resist 5:127–134CrossRefPubMedPubMedCentral
Zurück zum Zitat López-Arellano ME, Flores J, Mendoza de Gives P, Vázquez V, Liébano E, Bravo A, Herrera D, Godines E, Várgas P, Zamudio F (2006) Use of Bacillus thuringiensis toxin as an alternative method of control against Haemonchus contortus. Ann New York Acad Sci 1081:347–354CrossRef López-Arellano ME, Flores J, Mendoza de Gives P, Vázquez V, Liébano E, Bravo A, Herrera D, Godines E, Várgas P, Zamudio F (2006) Use of Bacillus thuringiensis toxin as an alternative method of control against Haemonchus contortus. Ann New York Acad Sci 1081:347–354CrossRef
Zurück zum Zitat Maceij J, Schäff CT, Kanitz E, Tuchscher BRM, Wolffram S, Hammon HM (2015) Bioavailability of the flavonol quercetin in neonatal calves after oral administration of quercetin aglycone or rutin. J Dairy Sci 98:3909–3917 Maceij J, Schäff CT, Kanitz E, Tuchscher BRM, Wolffram S, Hammon HM (2015) Bioavailability of the flavonol quercetin in neonatal calves after oral administration of quercetin aglycone or rutin. J Dairy Sci 98:3909–3917
Zurück zum Zitat Martinez-Ortíz-de-Montellano C, Arroyo-López C, Fourquaux I, Torres-Acosta JFJ, Sandoval-Castro CA, Hoste H (2013) Scanning electron microscopy of Haemonchus contortus exposed to tannin-rich plants under in vivo and in vitro conditions. Exp Parasitol 133:281–286CrossRefPubMed Martinez-Ortíz-de-Montellano C, Arroyo-López C, Fourquaux I, Torres-Acosta JFJ, Sandoval-Castro CA, Hoste H (2013) Scanning electron microscopy of Haemonchus contortus exposed to tannin-rich plants under in vivo and in vitro conditions. Exp Parasitol 133:281–286CrossRefPubMed
Zurück zum Zitat Muñiz-Lagunes A, González-Garduño R, López-Arellano ME, Ramírez-Valverde R, Ruíz-Flores A, García-Muñiz G, Ramírez-Vargas G, Mendoza-de Gives P, Torres-Hernández G (2015) Anthelmintic resistance in gastrointestinal nematodes from grazing beef cattle in Campeche state, Mexico. Trop Anim Health Prod 47:1049–1054CrossRefPubMed Muñiz-Lagunes A, González-Garduño R, López-Arellano ME, Ramírez-Valverde R, Ruíz-Flores A, García-Muñiz G, Ramírez-Vargas G, Mendoza-de Gives P, Torres-Hernández G (2015) Anthelmintic resistance in gastrointestinal nematodes from grazing beef cattle in Campeche state, Mexico. Trop Anim Health Prod 47:1049–1054CrossRefPubMed
Zurück zum Zitat Olmedo-Juárez A, Rojo RR, Arece GJ, Salem AZM, Kholif AM, Morales AE (2014) In vitro activity of Pithecellobium dulce and Lysiloma acapulcensis on the exogenous development of sheep gastrointestinal strongyles. Ital J Anim Sci 13:303–330CrossRef Olmedo-Juárez A, Rojo RR, Arece GJ, Salem AZM, Kholif AM, Morales AE (2014) In vitro activity of Pithecellobium dulce and Lysiloma acapulcensis on the exogenous development of sheep gastrointestinal strongyles. Ital J Anim Sci 13:303–330CrossRef
Zurück zum Zitat Olmedo-Juárez A, Rojo RR, Arece GJ, Mohamed AZM, Morales AE, Albarrán PB, Aarón HLR, Vázquez AJF (2015) Lysiloma acapulcensis extract on digestibility and ruminal fermentation of a diet for sheep. Eco Rec Agropec 2(5):173–182 Olmedo-Juárez A, Rojo RR, Arece GJ, Mohamed AZM, Morales AE, Albarrán PB, Aarón HLR, Vázquez AJF (2015) Lysiloma acapulcensis extract on digestibility and ruminal fermentation of a diet for sheep. Eco Rec Agropec 2(5):173–182
Zurück zum Zitat Orihuela A, Vázquez-Prats VM (2009) Los Parásitos y sus Huéspedes. Un Enfoque Etológico, Ed., LIMUSA, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, México. 88 p Orihuela A, Vázquez-Prats VM (2009) Los Parásitos y sus Huéspedes. Un Enfoque Etológico, Ed., LIMUSA, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, México. 88 p
Zurück zum Zitat Palacios-Landín J, Mendoza de Gives P, Salinas-Sanchez DO, López-Arellano ME, Liebano-Hernandez E, Hernández-Velázquez VM, Valladares-Cisneros MG (2015) In vitro and in vivo nematicidal activity of Allium sativum and Tagetes erecta extracts against Haemonchus contortus. Türk Parazitol Derg 39:260–264CrossRef Palacios-Landín J, Mendoza de Gives P, Salinas-Sanchez DO, López-Arellano ME, Liebano-Hernandez E, Hernández-Velázquez VM, Valladares-Cisneros MG (2015) In vitro and in vivo nematicidal activity of Allium sativum and Tagetes erecta extracts against Haemonchus contortus. Türk Parazitol Derg 39:260–264CrossRef
Zurück zum Zitat Ramünke S, Melville L, Rinaldi L, Hertzberg H, de Waal T, von Samson-Himmelstjerna G, Crihgoli G, Mavrot F, Skuce P, Krücken J, Demeler J (2016) Benzimidazole resistance survey for Haemonchus, Teladorsagia and Trichostrongylus in three European coutries using pyrosequencing including the development of new assay for Trichostrongylus. Int J Parasitol Drugs Drug Resist 6:230–240CrossRefPubMedPubMedCentral Ramünke S, Melville L, Rinaldi L, Hertzberg H, de Waal T, von Samson-Himmelstjerna G, Crihgoli G, Mavrot F, Skuce P, Krücken J, Demeler J (2016) Benzimidazole resistance survey for Haemonchus, Teladorsagia and Trichostrongylus in three European coutries using pyrosequencing including the development of new assay for Trichostrongylus. Int J Parasitol Drugs Drug Resist 6:230–240CrossRefPubMedPubMedCentral
Zurück zum Zitat Rivera JC, Yépez-Mulia L, Hernández-Campos A, Moreno-Esparaza R, Castillo R, Navarrete-Vázquez G, Fuentes-Noriega I, Jung-Cook H (2007) Biopharmaceutic evaluation of novel anthelminthic (1H-bencimidazol-5(6)-yl) carboxamide derivatives. Int J Pharm 343:159–165CrossRefPubMed Rivera JC, Yépez-Mulia L, Hernández-Campos A, Moreno-Esparaza R, Castillo R, Navarrete-Vázquez G, Fuentes-Noriega I, Jung-Cook H (2007) Biopharmaceutic evaluation of novel anthelminthic (1H-bencimidazol-5(6)-yl) carboxamide derivatives. Int J Pharm 343:159–165CrossRefPubMed
Zurück zum Zitat Rogerio AP, Kanashiro A, Fontanari C, Da Silva EV, Lucisano-Valim YM, Soares EG, Faccioli LH (2007) Anti-inflammatory activity of quercetin and isoquercitrin in experimental murine allergic asthma. Inflamm Res 56(10):402–408CrossRefPubMed Rogerio AP, Kanashiro A, Fontanari C, Da Silva EV, Lucisano-Valim YM, Soares EG, Faccioli LH (2007) Anti-inflammatory activity of quercetin and isoquercitrin in experimental murine allergic asthma. Inflamm Res 56(10):402–408CrossRefPubMed
Zurück zum Zitat Sargison ND (2016) Keys to solving health problems in small ruminants: anthelmintic resistance as a threat to sustainable nematode control. Small Rumin Res 142:11–15CrossRef Sargison ND (2016) Keys to solving health problems in small ruminants: anthelmintic resistance as a threat to sustainable nematode control. Small Rumin Res 142:11–15CrossRef
Zurück zum Zitat SAS, Institute (2006) SAS User’s guide: statistics. Ver 9.0. SAS Institute, Cary SAS, Institute (2006) SAS User’s guide: statistics. Ver 9.0. SAS Institute, Cary
Zurück zum Zitat von Son-de Fernex E, Alonso-Díaz MA, Mendoza-de-Gives P, Valles-de la Mora B, González-Cortazar M, Zamilpa A, Castillo-Gallegos E (2015) Elucidation of Leucaena leucocephala anthelmintic-like phytochemicals and the ultrastructural damage generated to eggs of Cooperia spp. Vet Parasitol 214:89–95CrossRef von Son-de Fernex E, Alonso-Díaz MA, Mendoza-de-Gives P, Valles-de la Mora B, González-Cortazar M, Zamilpa A, Castillo-Gallegos E (2015) Elucidation of Leucaena leucocephala anthelmintic-like phytochemicals and the ultrastructural damage generated to eggs of Cooperia spp. Vet Parasitol 214:89–95CrossRef
Zurück zum Zitat Steel RGD, Torrie JH (1985) Bioestadística: Principios y procedimientos. McGraw-Hill, México, pp 181–184 Steel RGD, Torrie JH (1985) Bioestadística: Principios y procedimientos. McGraw-Hill, México, pp 181–184
Zurück zum Zitat Vargas-Magaña JJ, Torres-Acosta JF, Aguilar-Caballero AJ, Sandoval-Castro CA, Hoste H, Chan-Perez JL (2014) Anthelmintic activity of acetone-water extracts against Haemonchus contortus eggs: interactions between tannins and other plant secondary compounds. Vet Parasitol 206:322–327CrossRefPubMed Vargas-Magaña JJ, Torres-Acosta JF, Aguilar-Caballero AJ, Sandoval-Castro CA, Hoste H, Chan-Perez JL (2014) Anthelmintic activity of acetone-water extracts against Haemonchus contortus eggs: interactions between tannins and other plant secondary compounds. Vet Parasitol 206:322–327CrossRefPubMed
Zurück zum Zitat Wagner H, Bladt S (1998) Plant drug analysis in: a thin layer chromatography, Atlas, 2nd edn. Springer, Germany Wagner H, Bladt S (1998) Plant drug analysis in: a thin layer chromatography, Atlas, 2nd edn. Springer, Germany
Zurück zum Zitat van Wyk JA, Mayhew E (2013) Morphological identification of parasitic nematode infective larvae of small ruminants and cattle: a practical lab guide. Ondesterpoort J Vet Res 80(1):1–14 van Wyk JA, Mayhew E (2013) Morphological identification of parasitic nematode infective larvae of small ruminants and cattle: a practical lab guide. Ondesterpoort J Vet Res 80(1):1–14
Zurück zum Zitat Yin F, Li Z, Si J, Chang Q, Li Z, Pan R (2014) Separation and purification of Myricitrin from Bayberry tree bark by high-speed counter-current chromatography. J Liq Chromatogr Relat Technol 36(11):1503–1512 Yin F, Li Z, Si J, Chang Q, Li Z, Pan R (2014) Separation and purification of Myricitrin from Bayberry tree bark by high-speed counter-current chromatography. J Liq Chromatogr Relat Technol 36(11):1503–1512
Zurück zum Zitat Yu CS, Lai KC, Yang JS, Chiang JH, Lu CC, Wu CL, Lin JP, Liao CL, Tang NY, Wood WG, Chung JG (2009) Quercetin inhibited murine leukemia WEHI-3 cells in vivo and promoted immune response. Phytother Res 24(2):163–168 Yu CS, Lai KC, Yang JS, Chiang JH, Lu CC, Wu CL, Lin JP, Liao CL, Tang NY, Wood WG, Chung JG (2009) Quercetin inhibited murine leukemia WEHI-3 cells in vivo and promoted immune response. Phytother Res 24(2):163–168
Metadaten
Titel
Lysiloma acapulcensis leaves contain anthelmintic metabolites that reduce the gastrointestinal nematode egg population in sheep faeces
verfasst von
Manases González-Cortazar
Alejandro Zamilpa
María Eugenia López-Arellano
Liliana Aguilar-Marcelino
David Emanuel Reyes-Guerrero
Sara Olazarán-Jenkins
Gabriel Ramírez-Vargas
Agustín Olmedo-Juárez
Pedro Mendoza-de-Gives
Publikationsdatum
25.10.2017
Verlag
Springer London
Erschienen in
Comparative Clinical Pathology / Ausgabe 1/2018
Print ISSN: 1618-5641
Elektronische ISSN: 1618-565X
DOI
https://doi.org/10.1007/s00580-017-2577-1

Weitere Artikel der Ausgabe 1/2018

Comparative Clinical Pathology 1/2018 Zur Ausgabe

Neu im Fachgebiet Pathologie

Open Access 15.04.2024 | Biomarker | Schwerpunkt: Next Generation Pathology

Molekularpathologische Untersuchungen im Wandel der Zeit

11.04.2024 | Pathologie | Schwerpunkt: Next Generation Pathology

Vergleichende Pathologie in der onkologischen Forschung

Open Access 08.04.2024 | GIST | CME

Gastrointestinale Stromatumoren

Wo stehen wir?

03.04.2024 | Zielgerichtete Therapie | Schwerpunkt: Next Generation Pathology

Personalisierte Medizin in der Onkologie