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Anthelmintic activity of botanical extracts against sheep gastrointestinal nematodes, Haemonchus contortus

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Abstract

The source of chemical anthelmintics (levamisole, flubendazole, and thiabendazole) had limited the success of gastrointestinal nematodiasis control in sheep and goats and thus awakened interest in the study of medicinal plant extracts as alternative sources of anthelmintics. The egg hatching and larvicidal effect of indigenous plant extracts were investigated against the sheep parasite, Haemonchus contortus. The purpose of the present study was to assess the efficacy of leaf, bark, and seed ethyl acetate, acetone and methanol extracts of Andrographis paniculata (Burm.f.) Wall. ex Nees., Anisomeles malabarica (L.) R. Br., Annona squamosa L., Datura metel L., and Solanum torvum Swartz were tested against the parasitic nematode of small ruminants H. contortus using egg hatch assay (EHA) and larval development assay (LDA). The assays were run in 24-well cell culture plates at room temperature with five replicates. All plant extracts showed moderate parasitic effects after 48 and exposure for egg hatching and LDA, respectively; however, 100% egg hatching and larvicidal inhibition were found in the methanol extracts of A. paniculata, A. squamosa, D. metel, and S. torvum at 25 mg/ml and the effect was similar to positive control of Albendazole (0.075 mg/ml) and Ivermectin (0.025mg/ml) against H. contortus, respectively. The EHA result showed the ED50 of methanol extracts of A. paniculata and D. metel, which were 2.90 and 3.08 mg/ml, and in larval development assay, the ED50 was 4.26and 3.86 mg/ml, respectively. These effects remain to be confirmed through in vivo studies.

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References

  • Allonby EW, Urquhart M (1975) The epidemiology and pathogenic significance of haemonchosis in Merino Folk in Eastern Africa. Vet Parasitol 1:1001–1007

    Article  Google Scholar 

  • Alonso-Díaz MA, Torres-Acosta JF, Sandoval-Castro CA, Aguilar-Caballero AJ, Hoste H (2008) In vitro larval migration and kinetics of exsheathment of Haemonchus contortus larvae exposed to four tropical tanniniferous plant extracts. Vet Parasitol 153:313–319

    Article  PubMed  Google Scholar 

  • Asase A, Oteng-Yeboah AA, Odamtten GT, Simmonds MSJ (2005) Ethnobotanical study of some Ghanaian anti-malarial plants. J Ethnopharmacol 99:273–279

    Article  PubMed  Google Scholar 

  • Assis LM, Bevilaqua CML, Morais SM, Vieira LS, Costa CTC, Souza JAL (2003) Ovicidal and larvicidal activity in vitro of Spigelia anthlmia Linn. Extracts on Haemonchus contortus. Vet Parasitol 117:43–49

    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 131:531–538

    Article  CAS  Google Scholar 

  • Bizimenyera ES, Githiori JB, Eloff JN, Swan GE (2006) In-vitro activity of Peltophourum africanum Sond. (Fabaceae) extracts on the egg hatching and larval development of the parasitic nematode Trichostrongylus colubrifrmis. Vet Parasitol 142(3–4):336–343

    Article  PubMed  CAS  Google Scholar 

  • Bonde K (2001) The genus Datura: from research subject to powerful hallucinogen. Journal of Ethanobotanical Leaflet 29:335–336 http://www.lycaeum.org/leda/docs/16212.shtml?ID=16212

    Google Scholar 

  • Coles GC, Bauer C, Borgsteede F, Geerts S, Klei TR, Taylor MA, Waller PJ (1992) World association for advancement in veterinary parasitology (WAAVP) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol 44:35–43

    Article  PubMed  CAS  Google Scholar 

  • Costa CTC, Bevilaqua CML, Camurca-vasconcelos ALF, Maciel MV, Morais SM, Castor CMS, Braga RR, Oliverira LMB (2008) In vitro ovicidal and larvacidal activity of Azadiracha indica extracts on Haemonchus contrtus. Small RumRes 74:284–287

    Article  Google Scholar 

  • Dua VK, Ojha VP, Roy R, Joshi BC, Valecha N, Usha Devi C, Bhatnagar MC, Sharma VP, Subbarao SK (2004) Anti-malarial activity of some xanthones isolated from the roots of Andrographis paniculata. J Ethnopharmacol 95:247–251

    Article  PubMed  CAS  Google Scholar 

  • Dua VK, Verma G, Dash AP (2009) In vitro antiprotozoal activity of some xanthones isolated from the roots of Andrographis paniculata. Phytother Res 23:126–128

    Article  PubMed  CAS  Google Scholar 

  • Eguale T, Tilahun G, Debella A, Feleke A, Makonnen E (2007) In vitro and in vivo anthelmintics activity of crude extracts of Coriandrum sativum against Haemonchus contortus. J Ethnopharmacol 110(3):428–433

    Article  PubMed  CAS  Google Scholar 

  • Elango G, Rahuman AA, Bagavan A, Kamaraj C, Zahir AA, Venkatesan C (2009) Laboratory study on larvicidal activity of indigenous plant extracts against Anopheles subpictus and Culex tritaeniorhynchus. Parasitol Res 104:1381–1388

    Article  PubMed  CAS  Google Scholar 

  • Geary TM, Sangster NC, Thompson DP (1999) Frontiers in anthelmintic pharmacology. Vet Parasitol 84:275–295

    Article  PubMed  CAS  Google Scholar 

  • Geethangili M, Rao YK, Fang SH, Tzeng YM (2008) Cytotoxic constituents from Andrographis paniculata induce cell cycle arrest in jurkat cells. Phytother Res 22:1336–1341

    Article  PubMed  CAS  Google Scholar 

  • Githiori JB, Athansiadou S, Thamsborg SM (2006) Use of plants novel approaches for control of gastro-intestinal helminths in livestock with emphasis on small ruminants. Vet Parasitol 139:308–320

    Article  PubMed  Google Scholar 

  • Goswami BK, Vijayalakshmi K (1987) Studies on the effect of some plant and non-edible oil seed cake extracts on larval hatching of Meloidogyne incognita. Assam Agri Uni 8:62–64

    Google Scholar 

  • Herd R (1996) Impactos ambientais associados aos compostos endectocidas. In: Padilha T (ed) Controle dosnematódeos gastrintestinais em ruminantes. EMBRAPA-CNPGL, Coronel Pacheco, pp 95–111

    Google Scholar 

  • Hördegen P, Cabaret J, Hertzberg H, Langhans W, Maurer V (2006) In vitro screening of six anthelmintic plant products against larval Haemonchus contortus with a modified methyl-thiazolyl-tetrazolium reduction assay. J Ethnopharmacol 108:85–89

    Article  PubMed  Google Scholar 

  • Hounzangbe-Adote FI, Mountairou K, Hoste H (2005) In-vitro effects of four tropical plants on three life cycle stages of parasitic nematode Haemonchus contortus. Res Vet Sci 78:155–160

    Article  PubMed  CAS  Google Scholar 

  • Hubert J, Kerboeuf D (1984) A new method for culture of larvae used in diagnosis of ruminant gastrointestinal strongylosis: comparison with faecal cultures. Can J Com Med 48:63–71

    CAS  Google Scholar 

  • Kamaraj C, Rahuman AA (2010) Efficacy of anthelmintic properties of medicinal plant extracts against Haemonchus contortus. Res Vet Sci. doi:10.1016/j.rvsc.2010.09.018

    PubMed  Google Scholar 

  • Kamaraj C, Bagavan A, Rahuman AA, Zahir AA, Elango G, Pandiyan G (2009) Larvicidal potential of medicinal plant extracts against Anopheles subpictus Grassi and Culex tritaeniorhynchus Giles (Diptera: Culicidae). Parasitol Res 104:1163–1171

    Article  PubMed  CAS  Google Scholar 

  • Kamaraj C, Rahuman AA, Bagavan A, Mohamed MJ, Elango G, Rajakumar G, Zahir AA, Santhoshkumar T, Marimuthu S (2010) Ovicidal and larvicidal activity of crude extracts of Melia azedarach against Haemonchus contortus (Strongylida). Parasitol Res 106:1071–1077

    Article  PubMed  Google Scholar 

  • Kotze AC, O’Grady J, Emms J, Toovey AF, Hughes S, Jessop P, Bennel M, Vercoe PE, Revell DK (2009) Exploring the anthelmintic properties of Australian native shrubs with respect to their potential role in livestock grazing systems. Parasitology 136:1065–1080

    Article  PubMed  CAS  Google Scholar 

  • Kusirisin W, Jaikang C, Chaiyasut C, Narongchai P (2009) Effect of polyphenolic compounds from Solanum torvum on plasma lipid peroxidation, superoxide anion and cytochrome P450 2E1 in human liver microsomes. Med Chem 5:583–588

    Article  PubMed  CAS  Google Scholar 

  • Lacey E, Redwin JM, Gill JH, Demargheriti VM, Waller PJ (1990) A larval development assay for the simultaneous detection of broad spectrum anthelmintic resistance. In: Boray JC, Martin PJ, Roush RT (eds) Resistance of parasites to antiparasitic drugs. MSD Agvet, Rajway, pp 177–184

    Google Scholar 

  • Liu YT, Wang F, Wang GX, Han J, Wang Y, Wang YH (2010) In vivo anthelmintic activity of crude extracts of Radix angelicae pubescentis, Fructus bruceae, Caulis spatholobi, Semen aesculi, and Semen pharbitidis against Dactylogyrus intermedius (Monogenea) in goldfish (Carassius auratus). Parasitol Res 106(5):1233–1239

    Article  PubMed  Google Scholar 

  • López-Aroche U, Salinas-Sánchez DO, Mendoza de Gives P, López-Arellano ME, Liébano-Hernández E, Valladares-Cisneros G, Arias-Ataide DM, Hernández-Velázquez V (2008) In vitro nematicidal effects of medicinal plants from the Sierra de Huautla, Biosphere Reserve, Morelos, Mexico against Haemonchus contortus infective larvae. J Helminthol 82:25–31

    Article  PubMed  Google Scholar 

  • Maciel MV, Morais SM, Bevilaqua CM, Camurça-Vasconcelos AL, Costa CT, Castro CM (2006) Ovicidal and larvicidal activity of Melia azedarach extracts on Haemonchus contortus. Vet Parasitol 140:98–104

    Article  PubMed  CAS  Google Scholar 

  • Maphosa V, Masika PJ, Bizimenyera ES, Eloff JN (2010) In vitro anthelminthic activity of crude aqueous extracts of Aloe ferox, Leonotis leonurus and Elephantorrhiza elephantina against Haemonchus contortus. Trop Anim Health Prod 42(2):301–307

    Article  PubMed  Google Scholar 

  • McCorkle M, Mathias E, van Schillhorn Veen TW (1996) Ethnoveterinary research and development. IT studies in indigenous knowledge and development intermediate technology publications. Southampton Row, London, pp 1–23

    Google Scholar 

  • Melo ACFL, Reis IF, Bevilaqua CML, Vieira LS, Echevarria FAM, Melo LM (2003) Nemato’ deos resistentes a anti-helmı’nticos emrebanhos de ovinos e caprinos no estado do Ceara, Brasil. Cienc Rural 33:339–344

    Article  Google Scholar 

  • Mishra K, Dash AP, Swain BK, Dey N (2009) Anti-malarial activities of Andrographis paniculata and Hedyotis corymbosa extracts and their combination with curcumin. Malar J 8:26–34

    Article  PubMed  Google Scholar 

  • Murugan K, Babu R, Sivaramakrishnan S (1999) Toxic effect of plants on Spodoptera litura Fab. Insect Env 4:135

    Google Scholar 

  • Nik AN, Rahman N, Furuta T, Kojima S, Takane K, Mohd MA (1999) Antimalarial activity of extracts of Malaysian medicinal plants. J Ethnopharmacol 64:249–254

    Article  Google Scholar 

  • Oduor-Owino P (1993) Effects of aldicarb, Datura stramonium, Datura metel and Tagetes minuta on the pathogenicity of root-knot nematodes in Kenya. Crop Prot 12:315–317

    Article  CAS  Google Scholar 

  • Oliveira LM, Bevilaqua CM, Costa CT, Macedo IT, Barros RS, Rodrigues AC, Camurça-Vasconcelos AL, Morais SM, Lima YC, Vieira LS, Navarro AM (2009) Anthelmintic activity of Cocos nucifera L. against sheep gastrointestinal nematodes. Vet Parasitol 159:55–59

    Article  PubMed  CAS  Google Scholar 

  • Pardhasaradhi BV, Reddy M, Ali AM, Kumari AL, Khar A (2005) Differential cytotoxic effects of Annona squamosa seed extracts on human tumour cell lines: role of reactive oxygen species and glutathione. J Biosci 302:237–244

    Article  Google Scholar 

  • Parrotta JA (2001) Healing plants of India. CABI Publishing, Wallingford, p 917

    Google Scholar 

  • Raghavendra K, Singh SP, Sarala K, Subbarao DAP (2009) Laboratory studies on mosquito larvicidal efficacy of aqueous & hexane extracts of dried fruit of Solanum nigrum Linn. Indian J Med Res 130:74–77

    PubMed  CAS  Google Scholar 

  • Rahuman AA, Gopalakrishnan G, Venkatesan P, Geetha K (2008) Isolation and identification of mosquito larvicidal compound from Abutilon indicum (Linn.) Sweet. Parasitol Res 102:981–988

    Article  PubMed  Google Scholar 

  • Rates SMK (2001) Plants as source drugs. Toxicon 39:603–613

    Article  PubMed  CAS  Google Scholar 

  • Roberts FHS, O’Sullivan PJ (1950) Methods for egg counts and larval cultures for strongyles infecting the gastrointestinal tract of cattle. Aus J Agri Res 1:99–102

    Article  Google Scholar 

  • Schoenian S (2003) Integrated parasite management. Maryland Cooperative extension. Maryland Small Ruminant www.sheepandgoat.com/articles/IPM.html.

  • Sharma RN, Bhosale AS, Joshi VN, Hebbalkar DS, Tungikar VB, Gupta AS, Patwardhan SA (1981) Lavandula gibsonii: a plant with insectistatic potential. Phytoparasit 9:101–109

    Article  Google Scholar 

  • Singha PK, Roy S, Dey S (2007) Protective activity of andrographolide and arabinogalactan proteins from Andrographis paniculata Nees. against ethanol-induced toxicity in mice. J Ethnopharmacol 111:13–21

    Article  PubMed  CAS  Google Scholar 

  • Souza MMC, Bevilaqua CML, Morais SM, Costa CTC, Silva ARA, Filho RB (2008) Anthelmintic acetogenin from Annona squamosa L. Seeds. An Acad Brasi Cienc 80:271–277

    Article  CAS  Google Scholar 

  • Srinivasan P, Sudha A, Bharathajothi P, Rameshthangam P, Manikandan R, Arulvasu C (2010) Effects of anti-inflammatory and anti-pyretic activity of Anisomeles malabarica R.BR. J Pharm Res 7:1598–1601

    Google Scholar 

  • Sugati SS, Sudjaswadi W, Rini S, Wien W (1999) Andrographis paniculata (Burm.f.) Wallich ex Nees. In: de Padua LS, Bunyapraphatsara N, Lemmens RHMJ (eds) PROSEA—Plant Resources of Southeast Asia No. 12(1). Medicinal and Poisonous Plants 1. Backhuys Publishers, Leiden, pp 119–123

    Google Scholar 

  • Tadesse D, Eguale T, Giday M, Mussa A (2009) Ovicidal and larvicidal activity of crude extracts of Maesa lanceolata and Plectranthus punctatus against Haemonchus contortus. J Ethnopharmacol 122:240–244

    Article  PubMed  Google Scholar 

  • Vieira LS, Cavalcante ACR, Pereira MF, Dantas LBA, Ximenes LJF (1999) Evaluation of anthelmintic efficacy of plants available in Ceará State, North-east Brazil, for the control of goat gastrointestinal nematodes. Rev Méd Vét 150:447–452

    Google Scholar 

  • Wu TS, Chern HJ, Damu AG, Kuo PC, Su CR, Lee EJ, Teng CM (2008) Flavonoids and ent-labdane diterpenoids from Andrographis paniculata and their antiplatelet aggregatory and vasorelaxing effects. J Asian Nat Prod Res 10:17–24

    Article  PubMed  CAS  Google Scholar 

  • Zahir AA, Rahuman AA, Kamaraj C, Bagavan A, Elango G, Sangaran A, Senthil Kumar B (2009) Laboratory determination of efficacy of indigenous plant extracts for parasites control. Parasitol Res 105(2):453–461

    Article  PubMed  Google Scholar 

  • Zaridah MZ, Idid SZ, Omar AW, Khozirah S (2001) In vitro antifilarial effects of three plant species against adult worms of subperiodic Brugia malayi. J Ethnopharmacol 78:79–84

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to C. Abdul Hakeem College Management, Dr. S. Mohammed Yousuff, Principal, Dr. K. Abdul Subhan, Associate Professor and HOD of Zoology Department, and Dr. Sait Sahul Hameed, Associate Professor in Zoology, for the facilities and support.The authors wish to thank Dr. A. Sangaran, Department of Parasitology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai, India for identification of parasite.

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Kamaraj, C., Rahuman, A.A., Elango, G. et al. Anthelmintic activity of botanical extracts against sheep gastrointestinal nematodes, Haemonchus contortus . Parasitol Res 109, 37–45 (2011). https://doi.org/10.1007/s00436-010-2218-y

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