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In vitro larvicidal and in vivo anthelmintic effects of Oxalis tetraphylla (Oxalidaceae) hydroalcoholic extract against Haemonchus contortus in lambs

  • B.J. González-Cruz (a1), M. Rodríguez-Labastida (a1), M. González-Cortázar (a2), A. Zamilpa (a2), M.E. López-Arellano (a1), L. Aguilar-Marcelino (a1), R. González-Garduño (a3), J.F.J. Torres-Acosta (a4), A. Olmedo-Juárez (a1) and P. Mendoza-de Gives (a1)...


The in vitro larvicidal and in vivo anthelmintic effects of Oxalis tetraphylla hydroalcoholic extract (HE), against Haemonchus contortus in experimentally infected lambs, were assessed. We used a microtitration plate method, comprising the following two stages. Stage 1: 20 μl of water containing 200 sheathed H. contortus infective larvae (ShHcl) were deposited in every well of three series; then, the series 2 and 3 wells were treated with 80 μl 1% ivermectin and O. tetraphylla HE at 20 mg/ml, respectively. Stage 2: the same procedure was performed replacing the ShHcl with exsheathed larvae (ExShHcl). Evaluations were performed after 24 and 48 h. The total numbers of dead and live larvae were counted. A second experiment evaluated the reduction in nematode egg populations in the faeces of lambs treated orally with the O. tetraphylla HE. The 27 lambs used were divided into Groups 1, 2 and 3 (n = 9), which were administered water (positive control), levamisole 1 m (7.5 mg/kg body weight (BW), as a unique dose) and O. tetraphylla HE (20 mg/kg BW), respectively. The plant HE was administered daily for 8 days. The in vitro assay showed 80.9% and 86.5% larval mortality of ShHcl after 24 and 48 h, respectively, while the corresponding mortality values for ExShHcl were 97 and 99%, respectively. The in vivo assay showed variability in the eggs/gram of faeces (epg) values; however, at the end of the trial, the average reduction in the epg values of the O. tetraphylla HE group was 45.6% (P < 0.05). Oxalis tetraphylla HE contains compounds that belong to the flavonol group with anthelmintic activity.


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Akerreta, S., Calvo, M.I. & Cavero, R.Y. (2010) Ethnoveterinary knowledge in Navarra (Iberian Peninsula). Journal of Ethnopharmacology 130, 369378.
Alawa, C.B.I., Adamu, A.M., Gefu, J.O., Ajanusi, O.J., Abdu, P.A. & Chiezey, N.P. (2010) In vivo efficacy of Vernonia amigdalina (Compositae) against natural helminth infection in Bunaji (Bos indicus) calves. Pakistan Veterinary Journal 30, 215218.
Ansa, P., Athul, P.V., Charan, A. & Afeefa, T.P. (2009) Anthelmintic activity of Macrotyloma uniflorm. Hygeia Journal for Drugs and Medicines 1, 2627.
Benson, H. (2012) Parasite loads of beef cattle in a rotationally grazed closed herd. MSc degree dissertation thesis, Murray State University, Kentucky, USA.
Bharati, A.K. & Sharma, B.L. (2012) Plants used as ethnoveterinary medicines in Sikkim Himalayas. Ethnobotany Research and Applications 10, 339356.
Bouix, J., Krupinski, J., Rzepecki, R. & Nowosad, B. (1998) Genetic resistance to gastrointestinal nematode parasites in Polish long-wool sheep. International Journal for Parasitology 28, 17971804.
Brickell, C. & Zuk, J.D. (1997) The American Horticultural Society A–Z encyclopedia of garden plants. New York, USA, DK Publishing.
Burger, W. (1991) Flora Costaricensis. Fieldiana, Botany. New Series, No. 28. Publication 1428. Chicago, Illinois, USA, Field Museum of Natural History.
Burggraaf, V.T., Boom, C.J., Sheath, G.W. & Brooky, A.R. (2009) The effect of rotational grazing by either calves, cows, lambs or ewes on the removal of herbage contaminated with gastro-intestinal parasite larvae around cattle faecal pats, New Zealand. Journal of Agricultural Research 52, 289297.
Coles, G.C., Jackson, F., Pomroy, W.E., Prichard, R.K., Himmelstjerna, V.S., Silvestre, A., Taylor, M.A. & Vercruysse, J. (2006) The detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology 136, 168185.
De Jesús-Gabino, A.F., Mendoza de Gives, P., Salinas-Sánchez, D.O., López-Arellano, M.E., Liébano-Hernández, E., Hernández-Velázquez, V.M. & Valladares-Cisneros, G. (2010) Anthelmintic effects of Prosopis laevigata n-hexanic extract against Haemonchus contortus in artificially infected gerbils (Meriones unguiculatus). Journal of Helminthology 84, 7175.
Eguale, T. & Giday, M. (2009) In vitro anthelmintic activity of three medicinal plants against Haemonchus contortus. International Journal of Green Pharmacy 3, 2934.
Fawzi, E.M., González-Sánchez, M.E., Corral, M.J., Cuquerella, M. & Alunda, J.M. (2014) Vaccination of lambs against Haemonchus contortus infection with a somatic protein (Hc23) from adult helminths. International Journal of Parasitology 44, 429436.
Fiaz-Qamar, M., Maqbool, A. & Ahmad, N. (2011) Economic looses due to haemonchosis in sheep and goats. Science International (Lahore) 23, 321324.
Garedaghi, Y., Hashemzadefarhang, H. & Esmaeli, A. (2013) Study on the prevalence and species composition of abomasal nematodes in small ruminants slaughtered at Behshahr Town. Iranian Journal of Veterinary Advance 3, 5559.
Hassan, H.U., Murad, W., Tariq, A. & Ahmad, A. (2014) Ethnoveterinary study of medicinal plants in Malakand Valley, District Dir (Lower), Khyber Pakhtunkhwa, Pakistan. Irish Veterinary Journal 67, 16.
Heckendorn, F., Häring, A.D., 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, 123134.
Hutchings, M.R., Knowler, K.J., McAnulty, R. & McEwan, J.C. (2007) Genetically resistant sheep avoid parasites to a greater extent than do susceptible sheep. Proceedings of the Royal Society of London, B 274, 18391844.
Iqbal, Z., Latee, M. & Gilani, A.H. (2010) In vivo anthelmintic activity of Azadirachta indica A. Juss seeds against gastrointestinal nematodes of sheep. Veterinary Parasitology 168, 342345.
Irum, S., Ahmed, H., Mukhtar, M., Mushtaq, M., Mirza, B., Donskow-Łysoniewska, K., Qayyum, M. & Simsek, S. (2015) Anthelmintic activity of Artemisia vestita Wall ex DC. and Artemisia maritima L. against Haemonchus contortus from sheep. Veterinary Parasitology 15, 451455.
Jabbar, A., Zaman, A.M., Iqbal, Z., Yaseen, M. & Shamim, A. (2007) Anthelmintic activity of Chenopodium album (L.) and Caesalpinia crista (L.) against trichostrongylid nematodes of sheep. Journal of Ethnopharmacology 114, 8691.
Lange, K.C., Olcott, D.D., Miller, J.E., Mosjidis, J.A., Terril, T.H., Burke, J.M. & Kearney, M.T. (2006) Effect of Sericea lespedeza (Lespedeza cuneata) fed as hay on natural and experimental Haemonchus contortus infections in lambs. Veterinary Parasitology 141, 273278.
Loudon, J. (2009) The horticulturist. 707 pp. London, Applewood Books.
Marshall, R., Gebrelul, S., Gray, L. & Ghebreiyessus, Y. (2012) Mixed species grazing of cattle and goats on gastrointestinal infections of Haemonchus contortus. American Journal of Animal Veterinary Science 7, 6166.
Naumann, H.D., Armstrong, S.A., Lambert, B.D., Muira, J.P., Tedeschid, L.O. & Kothmann, M.M. (2014) Effect of molecular weight and concentration of legume condensed tannins on in vitro larval migration inhibition of Haemonchus contortus. Veterinary Parasitology 199, 9398.
Paul, M., Torgerson, R.P., Höglund, J. & Furrer, R. (2014) Hierarchical modelling of faecal egg counts to assess anthelmintic efficacy. Journal of the Royal Statistical Society. Available at “arXiv (stat.AP)” (accessed 12 January 2014).
Periasamy, K., Pichler, R., Poli, M., Cristel, S., Cetra, B., Medus, D., Basar, M., Thiruvenkadan, A.K., Ramasamy, S., Ellahi, B.M., Mohamed, B., Teneva, A., Shamsuddin, M., García, P.M. & Diallo, A. (2014) Candidate gene approach for parasite resistance in sheep – variation in immune pathway genes and association with fecal egg count. PLoS One 9, e88337.
Pollard, D. (2009) Dose titration of Sericea lespedeza leaf meal on Haemonchus contortus infection in crossbred lambs. Doctoral dissertation, Faculty of the Louisiana State University and Agricultural and Mechanical College, USA
Prakash, V. & Bano, S. (2010) Symptoms and pathogenicity of Haemonchus contortus in sheep. Asian Journal of Animal Science 4,186187.
Roberts, B., Antonopoulos, A., Haslam, S.M., Dicker, A.J., McNeilly, T.N., Johnson, S.L., Dell, A., Knox, D.P. & Britton, C. (2013) Novel expression of Haemonchus contortus vaccine candidate aminopeptidase H11 using the free-living nematode Caenorhabditis elegans. Veterinary Research 44, 115.
Romero, L.C.E. (2000) Influencia del pastoreo en la concentración de fenoles totales y taninos condensados en Gliricidia sepium en el trópico seco. Livestock Research Rural Development 12, 410.
Saha, R.M., De Sarker, D. & Sen, A. (2014) Ethnoveternary practices among the tribal community of Malda district of West Bengal, India. Indian Journal of Traditional Knowledge 13, 359367.
Sayward, G. & Sayward, L. (2014) Effect of copper on both wool color and parasite load of Icelandic sheep. Ying Tri-Regional Science Fair 23 March 2014. Available at (accessed 23 March 2014).
Schuster-Gajzágó, I. (2004) Nutritional aspects of legumes. pp. 101114 in Fuleky, G. (Ed.) Cultivated plants, primarily as food sources, Vol 1. Encyclopedia of Life Support System (EOLSS), developed under the auspices of the UNESCO. Oxford, UK, Eolss Publishers.
Torres-Acosta, J.F.J., Mendoza-de-Gives, P., Aguilar-Caballero, A.J. & Cuéllar-Ordaz, J.A. (2012) Anthelmintic resistance in sheep farms: Update of the situation in the American continent. Veterinary Parasitology 189, 8996.
Von Son-de Fernex, E., Alonso-Díaz, M.A., Valles-de la Mora, B. & Capetillo-Leal, C.M. (2012) In vitro anthelmintic activity of five tropical legumes on the exsheathment and motility of Haemonchus contortus infective larvae. Experimental Parasitology 131, 413418.
Wagner, H., Bladt, S. & Zgainski, E.M. (1984) Plant drug analysis. Berlin, Germany, Springer-Verlag.
Yap, P., Utzinger, J., Hattendorf, J. & Steinman, P. (2014) Influence of nutrition on infection and re-infection with soil-transmitted helminths: a systematic review. Parasite & Vectors 7, 229.


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