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In vivo anthelmintic activity of Anogeissus leiocarpus Guill & Perr (Combretaceae) against nematodes in naturally infected sheep

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Abstract

The identification of new anthelmintic drugs becomes a priority because of the availability of a handful of drugs, cost of treatments, and recent emergence of drug resistance. Medicinal plants are a good source of bioactive compounds for development of drugs. In this study, in vivo efficacy of Anogeissus leiocarpus was assessed in sheep naturally infected with gastrointestinal nematodes. Fecal examination, serological analyses, and necropsy were carried out to determine the egg and worm-burden reduction. The administration of ethanolic extract (single oral dose of 80 mg/kg) of A. leiocarpus induced a moderate fecal egg reduction (81 %) and adult worm-burden reduction (87 %) against Haemonchus contortus and Trichostrongylus colubriformis (82 %). The plant exhibited high efficacy against adult Strongyloïdes papillosus (100 %), Gaigeria pachyscelis (90 %), Cooperia curticei (100 %), and Oesophagostomum columbianum (95 %) but low efficacy against Trichostrongylus axei (67 %) and Trichuris globulosa (79 %). All these helminthes were sensitive to fenbendazole, except O. columbianum which showed a decrease susceptibility (17 %). The plant extract also improved certain biological parameters by increasing bodyweight from 0.7 ± 2.9 to 3.3 ± 1.9 % and improving hematocrit of 6.9 ± 1.6 % 3-week posttreatment. It emerges from the results that the plant possesses significant effectiveness on diarrhea; all treated animals gave normal feces. This study has shown that A. leiocarpus could find an application in the control of multiparasitism in small ruminants.

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References

  • Abdel-Ghaffar F, Semmler M, Al-Rasheid KAS, Strassen B, Fischer K, Aksu G, Klimpel S, Mehlhorn H (2011) The effects of different plant extracts on intestinal cestodes and on trematodes. Parasitol Res 108:979–984

    Article  PubMed  Google Scholar 

  • Achi YL, Zinsstag J, Yeo N, Dea V, Dorchies P (2003) Epidémiologie des helminthoses des moutons et des chèvres du Nord de La Côte d’Ivoire. Rev Med Vet 154:179–188

    Google Scholar 

  • Ademola IO, Eloff JN (2011) In vitro anthelmintic effect of Anogeissus leiocarpus (DC.) Guill. & Perr. leaf extracts and fractions on developmental stages of Haemonchus contortus. Afr J Tradit Complement Altern Med 8:134–139

    PubMed  CAS  Google Scholar 

  • Agaie BM, Onyeyili PA, Muhammad BY, Ladan MJ (2007) Acute toxicity effects of the aqueous leaf extract of Anogeissus leiocarpus in rats. Afr J Biotechnol 6:886–889

    Google Scholar 

  • Al-Rofaai A, Rahman WA, Abdulghani M (2013) Sensitivity of two in vitro assays for evaluating plant activity against the infective stage of Haemonchus contortus strains. Parasitol Res 112:893–898

    Article  PubMed  CAS  Google Scholar 

  • Anonymous (2003) Rapport national sur l’état des ressources zoogénétiques. Ministère de la production république de Côte d’lvoire animale et des ressources halieutiques 80 p

  • Athanasiadou S, Kyriazakis I, Jackson F, Coop RL (2001) Direct anthelmintic effects of condensed tannins towards different gastro-intestinal nematodes of sheep: in vitro and in vivo studies. Vet Parasitol 99:205–219

    Article  PubMed  CAS  Google Scholar 

  • 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 glycosides. Parasitol 131:1–8

    Article  Google Scholar 

  • Bentounsi B, Khaznadar A, Cabaret J (2012) Resistance of Trichostrongylus spp. (Nematoda) to benzimidazole in Algerian cattle herds grazed with sheep. Parasitol Res 110:1021–1023

    Article  PubMed  Google Scholar 

  • Besier B (2007) New anthelmintics for livestock: the time is right. Trends Parasitol 23:21–24

    Article  PubMed  CAS  Google Scholar 

  • Brady HA, Nichols WT (2009) Drug resistance in equine parasites: an emerging global problem. J Equine Vet Sci 29:285–295

    Article  Google Scholar 

  • Cabaret J (2004) Genetic and phenotypic diversity in benzimidazole resistant trichostrongyle isolates from ruminants hosts: tools for control of resistance? In: Nematode Parasites Symposium: genetic diversity, virulence genes, diagnosis and control methods

  • CSAO-OCDE/CEDEAO (2008) Élevage et marché régional au Sahel et en Afrique de l’Ouest: Potentialités et défis. Eds Club du Sahel et de l’Afrique de l’Ouest/OCDE, Paris, France, 179 p

  • Coles GC, Bauer C, Borgsteede FHM, Geerts S, Klei TR, Taylor MA, 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. Vet Parasitol 44:35–44

    Article  PubMed  CAS  Google Scholar 

  • Coles GC, Jackson F, Pomroy WE, Prichard RK, von Samson-Himmelstjerna G, Silvestre A, Taylor MA, Vercruysse J (2006) The detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol 31:167–185

    Article  Google Scholar 

  • Cringoli G, VenezianoV RL, Sauvé C, Rubino R, Fedele V, Cabaret J (2007) Resistance of trichostrongyles to benzimidazoles in Italy: a first report in a goat farm with multiple and repeated introductions. Parasitol Res 101:577–58

    Article  PubMed  CAS  Google Scholar 

  • Dalziel JM (1937) The useful plants of West tropical Africa Crown agents for overseas Governments. Milbank, London, UK, pp 202–204

    Google Scholar 

  • Debela E (2002) Epidemiology of Gastrointestinal helminthiasis of Rift valley goats under traditional husbandry system in Adami Tulu District, Ethiopia. Ethiop J Sci 25:35–44

    Google Scholar 

  • Diehl MS, Kamanzi Atindehou K, TERE H, Betschart B (2004) Prospect of anthelmintic plants in the Ivory Coast using ethnobotanical criteria. J Ethnopharmacol 95:277–284

    Article  PubMed  CAS  Google Scholar 

  • Gordon HM, Whitlock HV (1939) A new technique for counting nematodes eggs in sheep faeces. J Counc Sci Ind Res Aust 12:50–52

    Google Scholar 

  • Graber M, Perrotin G (1983) Helminthes et helminthoses des ruminants domestiques d’Afrique tropicale. Paris, France, Ed. Le Point vétérinaire, 162 p

  • Hammond JA, Fielding D, Bishop SC (1997) Prospects for plant anthelmintics in tropical veterinary medicine. Vet Res Com 21:13–28

    Google Scholar 

  • Kabore A, Belem AMG, Tamboura HH, Traore A, Sawadogo L (2009) In vitro anthelmintic effect of two medicinal plants (Anogeissus leiocarpus and Daniellia oliveri) on Haemonchus contortus, an abosomal nematode of sheep in Burkina Faso. Afr J Biotechnol 8:4690–4695

    Google Scholar 

  • Kaufmann J (1996) Parasitic infections of domestic animals: a diagnostic manual. Birkhäuser Verlag, Basel, 423 p

  • Klimpel S, Abdel-Ghaffar F, Al-Rasheid KAS, Aksu G, Fischer K, Mehlhorn H (2011) The effects of different plant extracts on nematodes. Parasitol Res 108:1047–1054

    Article  PubMed  Google Scholar 

  • Komoin-Oka C, Zinsstag J, Pandey VS, Fofana F, N’depo A (1999) Epidémiologie des parasites des ovins de la zone sud forestière de la Côte d’Ivoire. Rev Elev Méd Vét Pays trop 52:39–46

    Google Scholar 

  • Koné WM, Kamanzi Atindehou K, Traoré D, Betschart B (2005) Anthelminthic activity of medicinal plants use in Northern Côte d’Ivoire against helminthiasis. Pharm Biol 43:72–78

    Article  Google Scholar 

  • Koné WM, Vargas M, Keiser J (2012) Anthelmintic activity of medicinal plants used in Côte d’Ivoire for treating parasitic diseases. Parasitol Res 110:2351–2362

    Article  PubMed  Google Scholar 

  • Mann A, Barnabas BB, Daniel II (2010) The effect of methanolic extracts of Anogeissus leiocarpus and Terminalia avicennioides on the growth of some food–borne microorganisms. Aust J Basic Appl Sci 4:6041–6045

    CAS  Google Scholar 

  • Mann A, Yahaya Y, Banso A, Ajayi GO (2008) Phytochemical and antibacterial screening of Anogeissus leiocarpus against some microorganisms associated with infectious wounds. Afr J Microbiol Res 2:060–062

    Google Scholar 

  • Mehlhorn H, Al-Quraishy S, Al-Rasheid KAS, Jatzlau A, Abdel-Ghaffar F (2011) Addition of a combination of onion (Allium cepa) and coconut (Cocos nucifera) to food of sheep stops gastrointestinal helminthic infections. Parasitol Res 108:1041–1046

    Article  PubMed  Google Scholar 

  • Murray M, Murray PK, Mcintyre WIM (1977) An improved parasitological technique for diagnosis of African trypanosomiasis. Trans. R Soc Trop Med Hyg 71:325–326

    Article  CAS  Google Scholar 

  • Niezen JH, Waghorn GC, Charleston WA (1998) Establishment and fecundity of Ostertagia circumcincta and Trichostrongylus colubriformis in lambs fed lotus (Lotus pedunculatus) or perennial ryegrass. Vet Parasitol 78:13–21

    Article  PubMed  CAS  Google Scholar 

  • Okpekon T, Yolou S, Gleye C, Roblot F, Loiseau P, Bories C, Grellier P, Frappier F, Laurens A, Hocquemiller R (2004) Antiparasitic activities of medicinal plants used in Ivory Coast. J Ethnopharmacol 90:91–97

    Article  PubMed  CAS  Google Scholar 

  • Paolini V, Fouraste I, Hoste H (2004) In vitro effects of three woody plant and sainfoin extracts on 3rd-stage larvae and adult worms of three gastro-intestinal nematodes. Parasitol 129:69–77

    Article  CAS  Google Scholar 

  • Pessoa LM, Morais SM, Bevilaqua CM, Luciano JH (2002) Anthelmintic activity of essential oil of Ocimum gratissimum Linn. and eugenol against Haemonchus contortus. Vet Parasitol 109:59–63

  • Powers KG, Wood IB, Eckert J, Gibson T, Smith HJ (1982) World Association for the Advancement Veterinary Parasitology (W.A.A.V.P.) guidelines for evaluating the efficacy of anthelmintics in rumi nants (bovine and ovine). Vet Parasitol 10:265–284

    Article  PubMed  CAS  Google Scholar 

  • Reinecke RK (1973) The larval anthelmintic test in ruminants. Tech Commun Dept Agric Tech Serv S Afr 106:1–20

    Google Scholar 

  • Reinecke RK (1980) Chemotherapy in the control of helminthiasis. Vet Parasitol 6:255–292

    Article  Google Scholar 

  • Rendell DK (2010) Anthelmintic resistance in cattle nematodes on 13 south-west Victorian properties. Aust Vet J 88:504–509

    Article  PubMed  CAS  Google Scholar 

  • Shuaibu MN, Wuyep PA, Yanagi T, Hirayama K, Tanaka T, Kouno I (2008) The use of microfluorometric method for activity-guided isolation of antiplasmodial compound from plant extracts. Parasitol Res 102:1119–1127

    Article  PubMed  CAS  Google Scholar 

  • Smith RA, Pontiggia L, Waterman C, Lichtenwalner M, Wasserman J (2009) Comparison of motility, recovery, and methyl-thiazolyltetrazolium reduction assays for use in screening plant products for anthelmintic activity. Parasitol Res 105:1339–1343

    Article  PubMed  Google Scholar 

  • Suarez VH, Cristel SL, Busetti MR (2009) Epidemiology and effects of gastrointestinal nematode infection on milk productions of dairy ewes. Parasite 16:141–147

    Article  PubMed  CAS  Google Scholar 

  • Sykes AR (1994) Parasitism and production in farm animals. Anim Prod 59:155–172

    Article  Google Scholar 

  • Sykes AR, Coop RL (1977) Intake and utilization of food by growing sheep with abomasal damage caused by daily dosing with Ostertagia circumcincta larvae. J Agric Sci 88:671–677

    Article  Google Scholar 

  • Terrill TH, Larsen M, Samples O, Husted S, Miller JE, Kaplan RM, Gelaye S (2004) Capability of the nematode-trapping fungus Duddingtonia flagrans to reduce infective larvae of gastrointestinal nematodes in goat feces in the southeastern United States: dose titration and dose time interval studies. Vet Parasitol 120:285–296

    Google Scholar 

  • Touré G, Ouattara Z, Yapy-Gnaore V, Yo T, Tanoh KG (2005) Sheep Commercialization in Bouake, Côte d’Ivoire: price variations at the small ruminants market. Revue Élev Méd vét Pays trop 58:95–101

    Google Scholar 

  • Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW (1996) Veterinary parasitology, 2nd edn. Blackwell, Oxford

  • Valderrábano J, Calvete C, Uriarte J (2010) Effect of feeding bioactive forages on infection and subsequent development of Haemonchus contortus in lamb faeces. Vet Parasitol 172:89–94

    Article  PubMed  Google Scholar 

  • Várady M, Papadopoulos E, Dolinská M, Königová A (2011) Anthelmintic resistance in parasites of small ruminants: sheep versus goats. Helminthologia 48:137–144

    Article  Google Scholar 

  • Waller PJ (1997) Anthelmintic resistance. Vet Parasitol 72:391–412

    Article  PubMed  CAS  Google Scholar 

  • Westlake WJ (1971) A one-sided version of the Tukey-Duckworth Test. Technometrics 13:901–903

    Article  Google Scholar 

  • Wolstenholme AJ, Fairweather I, Prichard RK, Samson-Himmelstjerna G, Sangster NC (2004) Drug resistance in veterinary helminths. Trends Parasitol 20:469–476

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors sincerely thank the “Programme Stratégique d’Appui à la Recherche Scientifique (PASRES, Project No. 21)” for financial support and the “Centre Suisse de Recherches Scientifiques en Côte d’Ivoire (CSRS)” for technical assistance. The authors acknowledge support from the consortium Afrique One “Ecosystem and Population Health: Expanding Frontiers in Health,” which is funded by the Wellcome Trust (WT087535MA). Thanks are also due to Dr. Esso Emmanuel and Mr. Yao Konan for statistical assistance.

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The authors declare that they have no conflict of interest.

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Correspondence to Witabouna Mamidou Koné.

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Soro, D., Koné, W.M., Bonfoh, B. et al. In vivo anthelmintic activity of Anogeissus leiocarpus Guill & Perr (Combretaceae) against nematodes in naturally infected sheep. Parasitol Res 112, 2681–2688 (2013). https://doi.org/10.1007/s00436-013-3435-y

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