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Investigation of anthelmintic activity of the acetone extract and constituents of Typha capensis against animal parasitic Haemonchus contortus and free-living Caenorhabditis elegans

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Abstract

This study aimed to determine in vitro anthelmintic activity of plant extracts of eleven plant species used traditionally in South Africa to treat various disorders including symptoms related to nematode infections, and to isolate bioactive compounds from the most active plant extract. Crude plant extracts were tested on different life-cycle stages of Haemonchus contortus. The cytotoxicity of the most active extracts, fractions and compounds was evaluated on Vero cells and the most potent extract, fractions and compounds were tested for their ability to kill the parasitic H. contortus and the free-living nematode Caenorhabditis elegans. Typha capensis acetone extract had the strongest egg hatching inhibitory effect with an EC50 of 184.94 μg/mL, and this extract also halted larval development of H. contortus with an EC50 of 83.30 μg/mL compared to the positive control (albendazole) with an EC50 of 2.66 μg/mL. Typha capensis crude extract and its butanol fraction had promising anthelmintic activity against both parasitic H. contortus and free-living C. elegans. Two compounds isolated from T. capensis, namely, isorhamnetin-3-O-β-d-glucoside and isorhamnetin 3-O-rutinoside, had antioxidant activity with IC50 values of 3.16 μg/mL and 0.96 μg/mL respectively, and good anthelmintic activity against H. contortus with IC50 values of 55.61 μg/mL and 145.17 μg/mL respectively. Identification of bioactive compounds from the T. capensis crude extract supports development of this extract as a complementary or alternative treatment against haemonchosis. However, further research is necessary to confirm the anthelmintic efficacy of the plant, including in vivo studies.

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Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Abdillahi HS, Van Staden J (2012) South African plants and male reproductive healthcare: conception and contraception. J Ethnopharm 143:475–480

    Article  CAS  Google Scholar 

  • Acamovic T, Brooker JD (2005) Biochemistry of plant secondary metabolites and their effects in animals. Pro Nut Soc 64:403–412

    Article  CAS  Google Scholar 

  • Adamu M, Naidoo V, Eloff JN (2013) Efficacy and toxicity of thirteen leaf acetone extracts used in ethnoveterinary medicine in South Africa on egg hatching and larval development of Haemonchus contortus. BMC Vet Res 9:38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Akbay P, Basaran AA, Undeger U, Basaran N (2003) In vitro immunomodulatory activity of flavonoid glycosides from Urtica dioica L. Phyt Res 17:34–37

    Article  CAS  Google Scholar 

  • Akin-Idowu PE, Ademoyegun OT, Olagunju YO, Aduloju AO, Adebo UG (2017) Phytochemical content and antioxidant activity of five grain amaranth species. Am J Food Sci Technol 5:249–255

    CAS  Google Scholar 

  • Akkari H, B'chir F, Hajaji S, Rekik M, Sebai E, Hamza H, Darghouth MA, Gharbi M (2016) Potential anthelmintic effect of Capparis spinosa (Capparidaceae) as related to its polyphenolic content and antioxidant activity. Vet Med 61:308-316

  • Arroyo-Lopez C, Manolaraki F, Saratsis A, Saratsi K, Stefanakis A, Skampardonis V, Voutzourakis N, Hoste H, Sotiraki S (2014) Anthelmintic effect of carob pods and sainfoin hay when fed to lambs after experimental trickle infections with Haemonchus contortus and Trichostrongylus colubriformis. Par 21:71–80

    Google Scholar 

  • Barry TN, McNabb WC (1999) The implications of condensed tannins on the nutritive value of temperate forages fed to ruminants. Brit J Nutr 81:263–272

    Article  CAS  PubMed  Google Scholar 

  • Blaxer M, Koutsovoulos G (2015) The evolution of parasitism in Nematoda. Par 142:26–39

    Google Scholar 

  • Bondia-Pons I, Savolainen O, Törrönen R, Martinez JA, Poutanen K, Hanhineva K (2014) Metabolic profiling of Goji berry extracts for discrimination of geographical origin by non-targeted liquid chromatography coupled to quadruple time-of-flight mass spectrometry. Food Res Int 63:132–138

    Article  CAS  Google Scholar 

  • Brenner S (1974) The Genetics of Caenorhabditis elegans. Genetics 77(1):71–94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burns AR, Wallace IM, Wildenhain J, Tyers M, Giaever G, Bader GD, Nislow C, Cutler SR, Roy PJ (2010) A predictive model for drug bioaccumulation and bioactivity in Caenorhabditis elegans. Nature Chem Biol 6:549–557

    Article  CAS  Google Scholar 

  • Burns AR, Luciani GM, Musso G, Bagg R, Yeo M, Zhang Y, Rajendran L, Glavin J, Hunter R, Redman E, Stasiuk S (2015) Caenorhabditis elegans is a useful model for anthelmintic discovery. Nat Com 6:7485–7496

    Article  CAS  Google Scholar 

  • Chapman J, Hall P (2000) Dictionary of Natural Products on CD-ROM. London

  • Chapman J, Hall P (2017) Dictionary of Natural Products on CD-ROM. Release 9:1, London

  • Coles GC, Bauer C, Borgsteede FHM, Geerts S, Klei TR, Taylor MA, Waller PJ (1992) World Association for the Advancement of Veterinary Parasitology (WAAVP) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol 44:35–44

    Article  CAS  PubMed  Google Scholar 

  • Debella A (2002) Manual for phytochemical screening of medicinal plants. Eth Health Nutr Res Inst, Addis Ababa, Ethiopia, pp. 35–47

  • Dehaghani ZA, Asghari G, Dinani MS (2017) Isolation and identification of nicotiflorin and narcissin from the aerial parts of Peucedanum aucheri Boiss. J Agri Sci Tech 7:45–51

    CAS  Google Scholar 

  • Eloff JN (1998) Which extractant should be used for the screening and isolation of antimicrobial components from plants? J Ethnopharm 60:1–8

    Article  CAS  Google Scholar 

  • Fouche G, Sakong BM, Adenubi OT, Pauw E, Leboho T, Wellington KW (2016) Anthelmintic activity of acetone extracts from South African plants used on egg hatching of Haemonchus contortus. Onderst J Vet Res 83:A1164

    CAS  Google Scholar 

  • Frezal L, Felix MA (2015) The natural history of model organisms: Caenorhabditis elegans outside the Petri dish. Elife, 4, e05849

  • Gaínza YA, Domingues LF, Perez OP, Rabelo MD, López ER, de Souza Chagas AC (2015) Anthelmintic activity in vitro of Citrus sinensis and Melaleuca quinquenervia essential oil from Cuba on Haemonchus contortus. Ind Cr Prod 76:647–652

    Article  CAS  Google Scholar 

  • Geary TG, Thompson DP (2001) Caenorhabditis elegans: how good a model for veterinary parasites? Vet Parasitol 101:371–386

    Article  CAS  PubMed  Google Scholar 

  • Gyamfi MA, Yonamine M, Aniya Y (1999) Free-radical scavenging action of medicinal herbs from Ghana: Thonningia sanguinea on experimentally-induced liver injuries. General Pharmacology: The Vas Sys 32(661):667

    Google Scholar 

  • Hammoda HM, Kassem FF, Radwan MM, Wanas AS, Darwish RS, El Sohly MA, Habib AAM (2016) Phytochemical investigation of Senecio vulgaris L. Planta Med. 82, PC82

  • Hila MB, Mosbah H, Zanina N, Ben Nejma A, Ben Jannet H, Aouni M, Selmi B (2016) Characterisation of phenolic antioxidants in Scabiosa arenaria flowers by LC–ESI-MS/MS and NMR. J Pharm Pharmacol 68:932–940

    Article  CAS  Google Scholar 

  • Hodgkin J, Doniach T (1997) Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146:149–164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubert J, Kerboeuf D (1992) A microlarval development assay for the detection of anthelmintic resistance in sheep nematodes. Vet Rec 130:442–446

    Article  CAS  PubMed  Google Scholar 

  • Idris OA, Wintola OA, Afolayan AJ (2017) Phytochemical and antioxidant activities of Rumex crispus L. in treatment of gastrointestinal helminths in Eastern Cape Province, South Africa. Asian Pac J Trop Biomed 12:1071–1078

    Article  Google Scholar 

  • Jin HG, Ko HJ, Chowdhury MA, Lee DS, Woo ER (2016) A new indole glycoside from the seeds of Raphanus sativus. Arch Pharm Res 39:755–761

    Article  CAS  PubMed  Google Scholar 

  • Joy V, Peter MPJ, Yesu Raj J, Ramesh, (2012) Medicinal values of avaram (Cassia auriculata Linn.): a review. Int J Curr Pharm Res 4:1–3

    Google Scholar 

  • Kagan J, Mabry TJ (2012) Isorhamnetin 3-O-rutinoside, the flavonoid pigment in Batis maritima. Phytochem 8:125–126

    Google Scholar 

  • Kaur M, Singh G, Mohan C (2013) Barringtonia acutangula: a traditional medicinal plant. Int J Pharm Sci Rev Res 33:168–171

    Google Scholar 

  • Kim YK, Na KS, Myint AM, Leonard BE (2017) The role of pro-inflammatory cytokines in neuroinflammation, neurogenesis and the neuroendocrine system in major depression. Pro Neu-Psy Bio Psy 64:277–284

    Google Scholar 

  • Klongsiriwet C, Quijada J, Williams AR, Mueller-Harvey I, Williamson EM, Hoste H (2015) Synergistic inhibition of Haemonchus contortus exsheathment by flavonoid monomers and condensed tannins. Int J Parasitol Drug Resist 5:127–134

    Article  Google Scholar 

  • Kose LS, Moteetee A, Van Vuuren S (2015) Ethnobotanical survey of medicinal plants used in the Maseru district of Lesotho. Ethnopharm 140:184–200

    Article  Google Scholar 

  • Kumarasingha R, Preston S, Yeo TC, Lim DS, Tu CL, Palombo EA, Shaw JM, Gasser RB, Boag PR (2016) Anthelmintic activity of selected ethno-medicinal plant extracts on parasitic stages of Haemonchus contortus. Par Vect 9:187

    Article  CAS  Google Scholar 

  • Lee JL, Mukhtar H, Bickers DR, Kopelovich L, Athar M (2005) Cyclooxygenases in the skin: pharmacological and toxicological implications. Toxicol Appl Pharmacol 192:294–306

    Article  CAS  Google Scholar 

  • Lemieux GA, Liu J, Mayer N, Bainton RJ, Ashrafi K, Werb Z (2011) A whole-organism screen identifies new regulators of fat storage. Nat Chem Biol 7:206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lespine A, Ménez C, Bourguinat C, Prichard RK (2012) P-glycoproteins and other multidrug resistance transporters in the pharmacology of anthelmintics: prospects for reversing transport-dependent anthelmintic resistance. Int J Parasitol Drug Res 2:58–75

    Article  CAS  Google Scholar 

  • Leung CK, Wang Y, Malany S, Deonarine A, Nguyen K, Vasile S, Choe KP (2013) An ultra high-throughput, whole-animal screen for small molecule modulators of a specific genetic pathway in Caenorhabditis elegans. PloS One 8:e62166

  • Lorimer SD, Perry NB, Foster LM, Burgess EJ, Douch PG, Hamilton MC, Donaghy MJ, McGregor RA (1996) A nematode larval motility inhibition assay for screening plant extracts and natural products. J Agr Food Chem 44:2842–2845

    Article  CAS  Google Scholar 

  • Max RA (2010) Effect of repeated wattle tanning drenches on worms burdens, faecal egg counts and egg hatchability during naturally acquired nematode infections in sheep and goats. Vet Parasitol 169:138–143

    Article  CAS  PubMed  Google Scholar 

  • McGaw LJ, Jäger AK, Van Staden J (2000) Antibacterial, anthelmintic and anti-amoebic activity in South African medicinal plants. J Ethnopharmacol 72:247–263

    Article  CAS  PubMed  Google Scholar 

  • McGaw LJ, Van der Merwe D, Eloff JN (2007) In vitro anthelmintic, antibacterial and cytotoxic effects of extracts from plants used in South African ethnoveterinary medicine. Vet J 173:366–372

    Article  CAS  PubMed  Google Scholar 

  • Meddeb E, Charni M, Ghazouani T, Cozzolino A, Fratianni F, Raboudi F, Nazzaro F, Fattouch S (2017) Biochemical and molecular study of Carpobrotus edulis bioactive properties and their effects on Dugesia sicula (Turbellaria, Tricladida) regeneration. Appl Bioch Biotech 182:1131–1143

    Article  CAS  Google Scholar 

  • Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Met 65:55–63

    Article  CAS  Google Scholar 

  • Ndjonka D, Abladam ED, Djafsia B, Ajonina-Ekoti I, Achukwi MD, Liebau E (2014) Anthelmintic activity of phenolic acids from the axlewood tree Anogeissus leiocarpus on the filarial nematode Onchocerca ochengi and drug-resistant strains of the free-living nematode Caenorhabditis elegans. J Helm 88:481–488

    Article  CAS  Google Scholar 

  • Olennikov DN, Kashchenko NI (2014) Componential profile and amylase inhibiting activity of phenolic compounds from Calendula officinalis L. leaves. Sc World J 2014:654193

  • Ondua M, Mfotie Njoya E, Abdalla MA, McGaw LJ (2019) Anti-inflammatory and antioxidant properties of leaf extracts of eleven South African medicinal plants used traditionally to treat inflammation. J Ethnopharm 234:27–35

    Article  Google Scholar 

  • Otieno JN, Hosea KMM, Lyaruu HV, Mahunnah RLA (2008) Multi–plant or single plant extract, which is the most effective for local healing in Tanzania? Afr J Tradit Compl Altern Med 5:165–172

    Google Scholar 

  • Rasoanaivo P, Ratsimamanga-Urverg S, Scott G (1993) Biological evaluation of plants with reference to the Malagasy flora. Napreca

  • Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237

    Article  CAS  PubMed  Google Scholar 

  • Roeber F, Jex AR, Gasser RB (2013) Next-generation molecular-diagnostic tools for gastrointestinal nematodes of livestock, with an emphasis on small ruminants: a turning point? Adv Parasitol 83:267–333

    Article  PubMed  PubMed Central  Google Scholar 

  • Samje M, Metuge J, Mbah J, Nguesson B, Cho-Ngwa F (2014) In vitro anti-Onchocerca ochengi activities of extracts and chromatographic fractions of Craterispermum laurinum and Morinda lucida. BMC Complement Altern Med 14:325

    Article  PubMed  PubMed Central  Google Scholar 

  • Scanlan LD, Lund SP, Coskun SH, Hanna SK, Johnson ME, Sims CM, Brignoni K, Lapasset P, Petersen EJ, Elliott JT, Nelson BC (2018) Counting Caenorhabditis elegans: protocol optimization and applications for population growth and toxicity studies in liquid medium. Sci Rep 8:904

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Seif el-Din SH, El-Lakkany NM, Mohamed MA, Hamed MM, Sterner O, Botros SS (2014) Potential effect of the medicinal plants Calotropis procera, Ficus elastica and Zingiber officinale against Schistosoma mansoni in mice. Pharm Biol 52:144-150

  • Shibano M, Kakutani K, Taniguchi M, Yasuda M, Baba K (2008) Antioxidant constituents in the dayflower (Commelina communis L.) and their α-glucosidase-inhibitory activity. J Nat Med 62:349

  • Shode FO, Mahomed AS, Rogers CB (2002) Typhaphthalide and typharin, two phenolic compounds from Typha capensis. Phytochem 61:955–957

    Article  CAS  Google Scholar 

  • Skantar AM, Agama K, Meyer SLF, Carta LK, Vinyard BT (2005) Effects of geldanamycin on hatching and juvenile motility in Caenorhabditis elegans and Heterodera glycines. J Chem Ecol 31:2481–2491

    Article  CAS  PubMed  Google Scholar 

  • Szewezuk VD, Mongelli ER, Pomilio AB (2003) Antiparasitic activity of Melia azadirach growing in Argentina. Mol Med Chem 1:54–7

    Google Scholar 

  • Van Wyk JA, Stenson MO, Van der Merwe JS, Vorster RJ, Viljoen PG (1999) Anthelmintic resistance in South Africa: surveys indicate an extremely serious situation in sheep and goat farming. Onderstepoort J Vet Res 66:273

    PubMed  Google Scholar 

  • Van Wyk BE, Van Oudtshoorn B, Gericke N (2009) Medicinal plants of South Africa. Briza Publications, Pretoria

    Google Scholar 

  • Waller PJ, Chandrawathani P (2005) Haemonchus contortus: parasite problem No. 1 from tropics polar circle. Problems and prospects for control based on epidemiology. Trop Biomed 22:131–137

    Google Scholar 

  • Wang DM, Pu WJ, Wang YH, Zhang YJ, Wang SS(2012). A new isorhamnetin glycoside and other phenolic compounds from Callianthemum taipaicum. Molecules, 17:4. pp. 4595–4603.

  • Watt JM, Breyer-Brandwijk MG (1962) The medicinal and poisonous plants of Southern and Eastern Africa, 2nd edn. Livingstone, Edinburgh

    Google Scholar 

  • Youness R, Assal R, Gad M, Motaal AA (2018) Halting triple-negative breast cancer progression through repressing NO machinery by a novel methoxylated flavonol glycoside isolated from Cleome droserifolia. Eur J Canc 92:S131

    Article  Google Scholar 

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Acknowledgements

The National Research Foundation, South Africa (grant number 105993) is thanked for providing research funding to LJM. The NRF and University of Pretoria, South Africa, are acknowledged for doctoral fellowships to OM. Ms Elsa van Wyk and Ms Magda Nel are thanked for assisting with preparation of herbarium voucher specimens. Johan Scholtz and Waldo Freese (MSD Animal Health) are gratefully acknowledged for providing Haemonchus contortus larvae. Dr Gerhard du Preez and Prof Driekie Fourie (North West University) are thanked for providing Caenorhabditis elegans.

Funding

The National Research Foundation, South Africa (grant number 105993) is thanked for providing research funding. The NRF and University of Pretoria, South Africa are acknowledged for doctoral fellowships to OM.

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Authors and Affiliations

  1. Phytomedicine Programme, Department of Paraclinical Sciences, Faculty of Veterinary Science, University of Pretoria, Private Bag X04, Onderstepoort, 0110, South Africa

    Moise Ondua, Emmanuel Mfotie Njoya, Muna Ali Abdalla & Lyndy J. McGaw

  2. School of Veterinary Medicine and Science, University of Ngaoundéré, P.O. BOX 454, Ngaoundéré, Cameroon

    Moise Ondua

  3. Department of Food Science and Technology, Faculty of Agriculture, University of Khartoum, 13314, Khartoum North, Sudan

    Muna Ali Abdalla

  4. Institut Für Pflanzenernährung Und Bodenkunde, Christian-Albrechts-Universität Zu Kiel, Hermann-Rodewald-Strasse 2, 24118, Kiel, Germany

    Muna Ali Abdalla

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  1. Moise Ondua
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  2. Emmanuel Mfotie Njoya
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  3. Muna Ali Abdalla
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  4. Lyndy J. McGaw
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Contributions

Experiments were carried out and results analysed by Moise Ondua with the assistance of Emmanuel Mfotie Njoya and Muna Ali Abdalla. Lyndy McGaw, Emmanuel Mfotie Njoya and Muna Ali Abdalla supervised the work and Lyndy McGaw made funding and facilities available. All authors were involved in writing and editing the manuscript.

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Correspondence to Lyndy J. McGaw.

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Ondua, M., Mfotie Njoya, E., Abdalla, M.A. et al. Investigation of anthelmintic activity of the acetone extract and constituents of Typha capensis against animal parasitic Haemonchus contortus and free-living Caenorhabditis elegans. Parasitol Res 120, 3437–3449 (2021). https://doi.org/10.1007/s00436-021-07269-7

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