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In vitro ovicidal and larvicidal activities of some saponins and flavonoids against parasitic nematodes of goats

Published online by Cambridge University Press:  21 May 2018

Acidália Carine Vieira Santos ,
Francianne Oliveira Santos ,
Hélimar Gonçalves Lima ,
Gisele Dias Da Silva ,
Rosangela Soares Uzêda ,
Êuder Reis Dias ,
Alexsandro Branco ,
Klauber Viana Cardoso ,
Jorge Mauricio David  and
Mariana Borges Botura
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Acidália Carine Vieira Santos
Affiliation:
Laboratório de Toxicologia, Hospital de Medicina Veterinária, Universidade Federal da Bahia, Av. Ademar de Barros, 500, Ondina, CEP: 40170-110, Salvador, BA, Brazil
Francianne Oliveira Santos
Affiliation:
Laboratório de Toxicologia, Hospital de Medicina Veterinária, Universidade Federal da Bahia, Av. Ademar de Barros, 500, Ondina, CEP: 40170-110, Salvador, BA, Brazil
Hélimar Gonçalves Lima
Affiliation:
Laboratório de Toxicologia, Hospital de Medicina Veterinária, Universidade Federal da Bahia, Av. Ademar de Barros, 500, Ondina, CEP: 40170-110, Salvador, BA, Brazil
Gisele Dias Da Silva
Affiliation:
Laboratório de Toxicologia, Hospital de Medicina Veterinária, Universidade Federal da Bahia, Av. Ademar de Barros, 500, Ondina, CEP: 40170-110, Salvador, BA, Brazil
Rosangela Soares Uzêda
Affiliation:
Departamento de Medicina Veterinária Preventiva e Produção Animal, Universidade Federal da Bahia, Av. Ademar de Barros, 500, Ondina, CEP: 40170-110, Salvador, BA, Brazil
Êuder Reis Dias
Affiliation:
Laboratório de Fitoquímica, Universidade Estadual de Feira de Santana, Av. Transnordestina s/n, CEP: 44036-900, Feira de Santana, BA, Brazil
Alexsandro Branco
Affiliation:
Laboratório de Fitoquímica, Universidade Estadual de Feira de Santana, Av. Transnordestina s/n, CEP: 44036-900, Feira de Santana, BA, Brazil
Klauber Viana Cardoso
Affiliation:
Instituto de Química, Universidade Federal da Bahia, Av. Ademar de Barros, 500, Ondina, CEP: 40170-110, Salvador, BA, Brazil
Jorge Mauricio David
Affiliation:
Instituto de Química, Universidade Federal da Bahia, Av. Ademar de Barros, 500, Ondina, CEP: 40170-110, Salvador, BA, Brazil
Mariana Borges Botura
Affiliation:
Laboratório de Toxicologia, Universidade Estadual de Feira de Santana, Av. Transnordestina s/n, CEP: 44036-900, Feira de Santana, BA, Brazil
Silvia Lima Costa
Affiliation:
Laboratório de Neuroquímica e Biologia Celular, Universidade Federal da Bahia, Av. Reitor Miguel Calmon, s/n, Vale do Canela, CEP: 40110-100, Salvador, BA, Brazil
Maria José Moreira Batatinha*
Affiliation:
Laboratório de Toxicologia, Hospital de Medicina Veterinária, Universidade Federal da Bahia, Av. Ademar de Barros, 500, Ondina, CEP: 40170-110, Salvador, BA, Brazil
*
Author for correspondence: Maria José Moreira Batatinha, E-mail: mjmb@ufba.br
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Abstract

This study assessed the anthelmintic activity of plant-derived compounds against gastrointestinal nematodes of goats using the egg hatch and larval motility assays. The compounds tested were saponins (digitonin and aescin) and their respective sapogenins (aglycones), hecogenin acetate and flavonoids (catechin, hesperidin, isocordoin and a mixture of isocordoin and cordoin). Additionally, cytotoxicity of active substances was analysed on Vero cell through 3-4,5-dimethylthiazol-2-yl,2,5diphenyltetrazolium bromide (MTT) and propidium iodide (PI) tests. Significant reduction on the egg hatching (P < 0.05) was seen only in the treatments with aescin (99%/EC50 = 0.67 mg mL−1) and digitonin (45%). The compounds that reduced the larval motility (P < 0.05) were digitonin (EC50 = 0.03 mg mL−1 and EC90 = 0.49 mg mL−1) and the hecogenin acetate (75%). The other sapogenins showed low anthelmintic activity. All the flavonoids showed low ovicidal (4–12%) and larvicidal (10–19%) effects. The aescin and digitonin showed low toxicity in PI test (viable cells >90%). Nevertheless, higher cytotoxicity was observed in the MTT assay, with IC50 of 0.20 mg mL−1 (aescin) and 0.0074 mg mL−1 (digitonin). Aescin and digitonin have a pronounced in vitro anthelmintic effect and the glycone portion of these saponins plays an important role in this activity.

Keywords

Anthelminticflavonoidsapogeninsaponintoxicity
Type
Research Article
Information
Parasitology , Volume 145 , Issue 14 , December 2018 , pp. 1884 - 1889
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Copyright
Copyright © Cambridge University Press 2018 

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References

Adamu, M, Naidoo, V and Eloff, JN (2013) Efficacy and toxicity of thirteen plant leaf acetone extracts used in ethnoveterinary medicine in South Africa on egg hatching and larval development of Haemonchus contortus. BMC Veterinary Research 9, 01–08.Google Scholar
Ahmad, VU, Baqai, FT and Ahmad, R (1995) A diosgenin tetrasaccharide from Cestrum nocturnum. Zeitschrift für Naturforschung B 50, 1104–1110.Google Scholar
Avato, P et al. (2006) Antimicrobial activity of saponins from Medicago sp.: structure–activity relationship. Phytotherapy Research 20, 454–457.Google Scholar
Baldissera, MD et al. (2014) In vitro and in vivo trypanocidal action of aescin and aescin liposomes against Trypanosoma evansi in experimental mice. Asian Pacific Journal of Tropical Biomedicine 4, 947–951.Google Scholar
Besier, RB et al. (2016) The pathophysiology, ecology and epidemiology of Haemonchus contortus infection in small ruminants. Advances in Parasitology 93, 95–143.Google Scholar
Borges, SL et al. (2015) Resistência anti-helmíntica em rebanhos caprinos nos biomas Caatinga e Mata Atlântica. Pesquisa Veterinária Brasileira 35, 643–648.Google Scholar
Böttger, S, Hofmann, K and Melzig, MF (2012) Saponins can perturb biologic membranes and reduce the surface tension of aqueous solutions: a correlation? Bioorganic & Medicinal Chemistry 20, 2822–2828.Google Scholar
Botura, MB et al. (2013) In vitro ovicidal and larvicidal activity of Agave sisalana Perr. (sisal) on gastrointestinal nematodes of goats. Veterinary Parasitology 192, 211–217.Google Scholar
Braz-Filho, R et al. (1986) S3β-O-β-D-glicopiranosilespinasterol, um novo glicosídeo esteroidal isolado de Amarthospermum schomburghinana (Miq) Baehni. Anais da Academia Brasileira de Ciências 58, 363–367.Google Scholar
Chen, L et al. (2015) The small-molecule TrkB agonist 7, 8-dihydroxyflavone decreases hippocampal newborn neuron death after traumatic brain injury. Journal Neuropathol and Experimental Neurology 74, 557–567.Google Scholar
Coles, GC et al. (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, 35–44.Google Scholar
Cooper, KM et al. (2011) Stability during cooking of anthelmintic veterinary drug residues in beef. Food Additives and Contaminants 28, 155–165.Google Scholar
Desrues, O et al. (2016) Impact of chemical structure of flavanol monomers and condensed tannins on in vitro anthelmintic activity against bovine nematodes. Parasitology 143, 444–454.Google Scholar
Doligalska, M et al. (2011) Triterpenoid saponins affect the function of P-glycoprotein and reduce the survival of the free-living stages of Heligmosomoides bakeri. Veterinary Parasitology 179, 144–151.Google Scholar
Farag, MA, Porzel, A and Wessjohann, LA (2015) Unraveling the active hypoglycemic agent trigonelline in Balanites aegyptiaca date fruit using metabolite fingerprinting by NMR. Journal of Pharmaceutical and Biomedical Analysis 115, 383–387.Google Scholar
Ferreira, LE et al. (2013) In vitro anthelmintic activity of aqueous leaf extract of Annona muricata L. (Annonaceae) against Haemonchus contortus from sheep. Experimental Parasitology 134, 327–332.Google Scholar
Fuchs, H et al. (2009) Saponins as tool for improved targeted tumor therapies. Current Drug Targets 10, 140–151.Google Scholar
Gilabert-Oriol, R et al. (2013) Real time analysis of membrane permeabilizing effects of oleanane saponins. Bioorganic & Medicinal Chemistry 21, 2387–2395.Google Scholar
Glensk, M et al. (2011) Aescin determination in seeds and capsules of three pure and hybrid Aesculus species. Chemistry of Natural Compounds 47, 142–144.Google Scholar
Gomes, DC et al. (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 Scholar
Gruza, MM et al. (2013) Preparation, purification and regioselective functionalization of protoescigenin – the main aglycone of escin complex. Molecules 18, 4389–4402.Google Scholar
Gülden, M, Schreiner, J and Seibert, H (2015) In vitro toxicity testing with microplate cell cultures: impact of cell binding. Toxicology 332, 41–51.Google Scholar
Hansen, MB, Nielsen, SE and Berg, K (1989) Re-examination and further top of the development needs and rapid dye method for measuring cell growth/cell kill. Journal of Immunological Methods 119, 203–210.Google Scholar
Hoste, H and Torres-Acosta, JFJ (2011) Non chemical control of helminths in ruminants: adapting solutions for changing worms in a changing world. Veterinary Parasitology 180, 144–154.Google Scholar
Hubert, J and Kerboeuf, D (1992) A microlarval development assay for the detection of anthelmintic resistance in sheep nematodes. Veterinary Record 130, 442–446.Google Scholar
Kerboeuf, D, Riou, M and Guégnard, F (2008) Flavonoids and related compounds in parasitic disease control. Mini-Reviews in Medicinal Chemistry 8, 116–128.Google Scholar
Klaassen, CD and Watkins, JB (2010) Casarett e Doull Essentials of Toxicology, 2nd Edn. USA: MCGRAW-HILL PROFESSI.Google Scholar
Klongsiriwet, C et al. (2015) Synergistic inhibition of Haemonchus contortus exsheathment by flavonoid monomers and condensed tannins. International Journal for Parasitology: Drugs and Drug Resistance 5, 127–134.Google Scholar
Krstin, S, Peixoto, HS and Wink, M (2015) Combinations of alkaloids affecting different molecular targets with the saponin digitonin can synergistically enhance trypanocidal activity against Trypanosoma brucei brucei. Antimicrobial Agents and Chemotherapy 59, 7011–7017.Google Scholar
Kumar, S and Pandey, AK (2013) Chemistry and biological activities of flavonoids: an overview. The Scientific World Journal 2013, 1–16.Google Scholar
Muhr, P, Likussar, W and Schubert-Zsilavecz, M (1996) Structure investigation and proton and carbon-13 assignments of digitonin and cholesterol using multidimensional NMR techniques. Magnetic Resonance in Chemistry 34, 137–142.Google Scholar
Nchu, F et al. (2011) Anthelmintic and cytotoxic activities of extracts of Markhamia obtusifolia Sprague (Bignoniaceae). Veterinary Parasitology 183, 184–188.Google Scholar
Paris, I et al. (2011) Autophagy protects against aminochrome-induced cell death in substantia Nigra-derived cell line. Toxicological Sciences 121, 376–388.Google Scholar
Parmar, VS et al. (1992) 13C nuclear magnetic resonance studies on 3-methylbut-2-enylated 1, 3-diphenylprop-2-enones. Spectrochimica Acta Part A: Molecular Spectroscopy 48, 617–620.Google Scholar
Platonova, A et al. (2015) Role of cytoskeleton network in anisosmotic volume changes of intact and permeabilized A549 cells. Biochimica et Biophysica Acta 1848, 2337–2343.Google Scholar
Press, JB et al. (2000) Structure/function relationships of immunostimulating saponins. Studies in Natural Products Chemistry 24, 131–174.Google Scholar
Puttonen, KA et al. (2008) Different viabilities and toxicity types after 6-OHDA and Ara-C exposure evaluated by four assays in five cell lines. Toxicology in Vitro 22, 182–189.Google Scholar
Rieger, AM et al. (2011) Modified annexin V/propidium iodide apoptosis assay for accurate assessment of cell death. Journal of Visualized Experiments 50, 1–4.Google Scholar
Santos, FO et al. (2017) In vitro anthelmintic and cytotoxicity activities the Digitaria insularis (Poaceae). Veterinary Parasitology 245, 48–54.Google Scholar
Singh, R et al. (2016) Detection of anthelmintic resistance in sheep and goat against fenbendazole by faecal egg count reduction test. Journal of Parasitic Diseases 40, 1–4.Google Scholar
Sirtori, CR (2001) Aescin: pharmacology, pharmacokinetics and therapeutic profile. Pharmacological Research 44, 183–193.Google Scholar
Thakur, M et al. (2011) Chemistry and pharmacology of saponins: special focus on cytotoxic properties. Botanics: Targets and Therapy 1, 19–29.Google Scholar
Ueno, H and Gonçalves, PC (1998) Manual Para Diagnóstico das Helmintoses de Ruminantes. Tokyo: Japan International Cooperation Agency.Google Scholar
Vercruysse, J et al. (2001) Anthelmintic efficacy of international harmonisation guidelines. Veterinary Parasitology 96, 171–193.Google Scholar
Vermes, I, Haanen, C and Reutelingsperger, C (2000) Flow cytometry of apoptotic cell death. Journal of Immunological Methods 243, 167–190.Google Scholar
Vliegenthart, JFG, Dorland, L and Halbeek, HV (1983) High-resolution, 1H-nuclear magnetic resonance spectroscopy as a tool in the structural analysis of carbohydrates related to glycoproteins. Advances in Carbohydrate Chemistry and Biochemistry 41, 209–374.Google Scholar
Wang, Y et al. (2007) Exploration of the correlation between the structure, hemolytic activity, and cytotoxicity of steroid saponins. Bioorganic & Medicinal Chemistry 15, 2528–2532.Google Scholar
Wulff, G and Tschesche, R (1969) Über triterpene-XXVI: Über die struktur der rosskastaniensaponnie (aescin) und die aglykone verwandter glykoside. Tetrahedron 25, 415–436.Google Scholar
Yang, et al. (2006) Antifungal activity of C-27 steroidal saponins. Antimicrobial Agents and Chemotherapy 50, 1710–1714.Google Scholar
Ye, Y, Xing, H and Chen, X (2013) Anti-inflammatory and analgesic activities of the hydrolyzed sasanquasaponins from the defatted seeds of Camellia oleífera. Archives Pharmacal Research 36, 941–951.Google Scholar
Yuan, S et al. (2017) Escin induces apoptosis in human renal cancer cells through G2/M arrest and reactive oxygen species-modulated mitochondrial pathways. Oncology Reports 37, 1002–1010.Google Scholar