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In vitro anthelmintic activity of Dennettia tripetala G. Baker (Annonaceae) Fruits against Haemonchus contortus

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Abstract

Helminthosis is one of the greatest causes of parasitic disease and loss in animal productivity. As such, the control of helminth parasites is of critical importance. This study was aimed to investigate the in vitro anthelmintic activity of Dennettia tripetala G. Baker (Annonaceae) fruits against Haemonchus contortus. Using in vitro techniques, the anthelmintic activity of extracts and fractions of D. tripetala G. Baker (Annonaceae) was evaluated for ovicidal (Egg hatch inhibition test) and larvicidal (larval mortality test) activity. Besides, the maximum tolerated dose was determined in adult albino rats administered, 300, 400, and 500 mg/kg body weight of the CME fraction, and observed over a period of 48 h for signs of toxicity and mortality. Phytochemical screening uncovered the occurrence of flavonoids, steroids/triterpenes, cardiac glycosides, saponins, tannins, carbohydrates, and alkaloids in the crude methanol extract (CME), the ethyl acetate fraction (EAF), and butanol fraction. The maximum tolerated dose of the CME of D. tripetala did not produce observable signs of toxicity or death in all the rats given up to 500 mg/kg. The CME and EAF of D. tripetala fruits produced a significant (\(p < 0.05\)) reduction in the hatchability of H. contortus eggs in a concentration-dependent manner, while the CME at concentrations between 12.5 and 100 mg/ml completely inhibited the hatching of H. contortus eggs. Similarly, EAF at doses of 25, 50, and 100 mg/ml completely inhibited the hatching of H. contortus eggs. The CME and EAF of D. tripetala fruits produced significant (\(p < 0.05\)) larvicidal activity against L3 of H. contortus in a concentration-dependent manner while the CME at concentrations between 6.25 and 100 mg/ml caused larval mortality of H. contortus L3 larvae completely. This study suggests that methanol extract and fractions of D. tripetala fruits possess beneficial anthelmintic (ovicidal and larvicidal) activity against H. contortus, and may be a suitable alternative anthelmintic candidate for the control of nematodes.

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References

  • Abbas II, Arigbede YA (2012) Green mapping of Ahmadu Bello University Main Campus, Zaria, Nigeria using remote sensing (Rs) and geographical information system (GIS) techniques. J Geogr Reg Plan 5(10):287–292

    Google Scholar 

  • Abonyi U, Omoiri M, Akah P (2020) Evaluation of the anti-diabetic effect of the methanol leaf extract and fractions of Dennettia tripetala G. Bak (Annonaceae) in alloxan-induced diabetic mice. J Drug Deliv Therap 10(2):129–139. https://doi.org/10.22270/jddt.v10i2.3969

    Article  CAS  Google Scholar 

  • Adedayo BC, Oboh G, Akindahusi AA (2010) Changes in the total phenol content and antioxidant properties of pepperfruit (Dennettia tripetala) with ripening. Afr J Food Sci 4:403–409

    CAS  Google Scholar 

  • Akefe I, Yusuf I, Adamu A, Abraham S, Dung E, Yusuf IL, Adegoke VA (2017) Phytochemical investigation and evaluation of analgesic effect of ethanolic leaves extract of Loranthus micranthus Linn (Nigerian Mistletoe). Am J Phytomed Clin Ther 5(3):23. https://doi.org/10.21767/2321-2748.100336

    Article  CAS  Google Scholar 

  • Akefe IO, Ayo JO, Sinkal VO (2020) Kaempferol and zinc gluconate mitigate neurobehavioral deficits and oxidative stress induced by noise exposure in Wistar rats. PLoS ONE 15(7):e0236251

    Article  CAS  Google Scholar 

  • Akefe IO, Yusuf IL, Adegoke VA (2019) C-glycosyl flavonoid orientin alleviates learning and memory impairment by radiofrequency electromagnetic radiation in mice via improving antioxidant defence mechanism. Asian Pac J Trop Biomed 9:518523. https://doi.org/10.4103/2221-1691.271725

    Article  CAS  Google Scholar 

  • Ali R, Rooman M, Mussarat S, Norin S, Ali S, Adnan M, Khan SN (2021) A systematic review on comparative analysis, toxicology, and pharmacology of medicinal plants against Haemonchus contortus. Front Pharmacol 12:644027. https://doi.org/10.3389/fphar.2021.644027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ameh MP, Mohammed M, Ofemile YP, Mohammed MG, Gabriel A, Isaac AO (2020) Detoxifying action of aqueous extracts of Mucuna pruriens seed and Mimosa pudica root against venoms of Naja nigricollis and Bitis arietans. Recent Pat Biotechnol 14(2):134–144. https://doi.org/10.2174/1872208313666191025110019

    Article  CAS  PubMed  Google Scholar 

  • Anosike CA, Okagu IU, Uchenn OK (2016) Phytoconstituents, acute toxicity study and protective effect of ethanol extract of Dennettia tripetala seed against aspirin-induced ulcer in rats. Int J Adv Sci Res 1(4):1–6

    Google Scholar 

  • Arsenopoulos KV, Fthenakis GC, Katsarou EI, Papadopoulos E (2021) Haemonchosis: a challenging parasitic infection of sheep and goats. Animals (Basel) 11(2):363. https://doi.org/10.3390/ani11020363

    Article  Google Scholar 

  • Aumont G, Pouillot R, Simon R, Hostache G, Varo H, Barre (1997) Parasitisme difestif des petits ruminants dans les Antilles Francaises. INRA Prod Anim 10:79–89

    Article  Google Scholar 

  • Baihaqi ZA, Widiyono I, Nurcahyo W (2020) In vitro anthelmintic activity of aqueous and ethanol extracts of Paraserianthes falcataria bark waste against Haemonchus contortus obtained from a local slaughterhouse in Indonesia. Veterinary World 13(8):1549–1554. https://doi.org/10.14202/vetworld.2020.1549-1554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ballweber LR (2001) Veterinary parasitology: parasitic diseases, vol I, pp 112–113.

  • Becker SL, Liwanag HJ, Snyder JS, Akogun O, Belizario V Jr, Freema MC, Gyorkos TW, Imtiaz R, Keiser J, Krolewiecki A, Levecke B, Mwandawiro C, Pullan RL, Addiss DG, Utzinger J (2018) Toward the 2020 goal of soil-transmitted helminthiasis control and elimination. PLoS Negl Trop Dis 12(8):e0006606. https://doi.org/10.1371/journal.pntd.0006606

    Article  PubMed  PubMed Central  Google Scholar 

  • Besier B (2009) Sheep worms—barbers pole worm. Note 476. Department of Agriculture and Food, Government of Western Australia, pp 1–4

  • Bordoloi G, Jas R, Ghosh JD (2012) Changes in the haemato-biochemical pattern due to experimentally-induced haemonchosis in Sahabadi sheep. J Parasit Dis 36(1):101–105

    Article  CAS  Google Scholar 

  • Buza V, Cătană L, Andrei SM, Ştefănuţ LC, Răileanu Ş, Matei MC, Vlasiuc I, Cernea M (2020) In vitro anthelmintic activity assessment of six medicinal plant aqueous extracts against donkey strongyles. J Helminthol 94:e147. https://doi.org/10.1017/S0022149X20000310

    Article  CAS  PubMed  Google Scholar 

  • Cavier R (1973) Chemotherapy of internal nematode. In: Hawkins F (ed) Chemotherapy of helminthiasis. International encyclopaedia of pharmacology and therapeutics, vol 1, 1st edn. Pergamon Press Ltd, Headington Hill Hall, Oxford, pp 437–500

    Google Scholar 

  • Coles GC, Bauer C, Borgsteede FH, 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  CAS  Google Scholar 

  • Crook EK, O’Brien DJ, Howell SB, Storey BE, Whitley NC, Burke JM, Kaplan RM (2016) Prevalence of anthelmintic resistance on sheep and goat farms in the mid-Atlantic region and comparison of in vivo and in vitro detection methods. Small Rumin Res 143:89–96

    Article  Google Scholar 

  • Cruz-Tamayo AA, López-Arellano ME, González-Garduño R, Torres-Hernández G, de la Mora-Valle A, Becerril-Pérez C, Hernández-Mendo O, Ramírez-Bribiesca E, Huchin-Cab M (2021) Haemonchus contortus infection induces a variable immune response in resistant and susceptible Pelibuey sheep. Vet Immunol Immunopathol 234:110218. https://doi.org/10.1016/j.vetimm.2021.110218

    Article  CAS  PubMed  Google Scholar 

  • Dai J, Mumper RJ (2010) Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 15:7313–7352

    Article  CAS  Google Scholar 

  • Davuluri T, Chennuru S, Pathipati M, Krovvidi S, Rao GS (2020) In vitro anthelmintic activity of three tropical plant extracts on Haemonchus contortus. Acta Parasitol 65(1):11–18. https://doi.org/10.2478/s11686-019-00116-x

    Article  CAS  PubMed  Google Scholar 

  • Evans (2007) Trease and evans pharmacognosy. Springer, New York, pp 153–157

    Google Scholar 

  • Fawzi EM, Gonzalez-Sanchez ME, Corral MJ, Cuquerella M, Alunda JM (2014) Vaccination of lambs against Haemonchus contortus infection with a somatic protein (Hc23) from adult helminthes. Int J Parasitol 44:429–436

    Article  CAS  Google Scholar 

  • Gabriel A, Mohammed M, Magaji MG, Ofemile YP, Matthew AP, Akefe IO (2020) In vitro and in vivo neutralizing activity of Uvaria chamae leaves fractions on the venom of Naja nigricollis in albino rat and bovine blood. Recent Pat Biotechnol 14(4):295–311

    Article  CAS  Google Scholar 

  • Gainza YA, Santos IBD, Figueiredo A, Santos LALD, Esteves SN, Barioni-Junior W, Minho AP, Chagas ACS (2021) Anthelmintic resistance of Haemonchus contortus from sheep flocks in Brazil: concordance of in vivo and in vitro (RESISTA-Test©) methods. Rev Bras Parasitol Vet 30(2):e025120. https://doi.org/10.1590/S1984-296120201093

    Article  CAS  PubMed  Google Scholar 

  • Handa SS, Khanuja SPS, Longo G, Rakesh DD (2008) Extraction technologies for medical and aromatic plants. In: International centre for science and high technology, Trieste, Italy, pp 21–25

  • Hansen J, Perry B, (1994) The epidemiology, diagnosis and control of helminth parasites of ruminants. A handbook. ILRAD Nairobi, Kenya, pp 17–132

  • Hoste H, Jackson F, Anthanasiadou S, Thamsborg SM, Hoskin SO (2006) The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends Parasitol 22:253–261. https://doi.org/10.1371/journal.pone.0236251

    Article  CAS  PubMed  Google Scholar 

  • Ikpi DE, Nku CO (2008) Effect of ethanolic extract of Dennettia tripetala fruit on haematological parameters in albino wistar rats. Niger J Physiol Sci 23(1–2):13–17

    PubMed  Google Scholar 

  • Isaac A, Ibrahim Y, Andrew A, Ibrahim Y, Edward D, Solomon A (2017a) The cortisol steroid levels as a determinant of health status in animals. J Proteom Bioinform 10:277–283. https://doi.org/10.4172/jpb.1000452

    Article  Google Scholar 

  • Isaac AO, Joseph AO, Victor SO, Lamidi YI, Andrew AM (2017b) Ameliorative effects of kaempferol and zinc gluconate on erythrocyte osmotic fragility and haematological parameters in Wistar rats exposed to noise stress. Insights Biomedicine 2(3):15. https://doi.org/10.21767/2572-5610.100031

    Article  Google Scholar 

  • Isaac OA, Joseph OA, Victor OS (2017c) Mitigative effects of anitoxidants in noise stress. J Clin Nutr Diet 3:21. https://doi.org/10.4172/2472-1921.100056

    Article  Google Scholar 

  • Krizova-Fortstova V, Lamka J, Cvilink V, Hanusova V, Skalova L (2010) Factors affecting pharmacokinetics of benzimidazole anthelmintics in food-producing animals: the consequencies and potential risks. Res Vet Sci 91:333–341

    Article  Google Scholar 

  • Lamidi IY, Hudu MG, Akefe IO, Adamu S, Salihu SI (2020) Sub-chronic administration of lavonoid fraction Dalon improve lead-induced alterations in delta-aminolevulinic acid dehydratase activity, erythrocytic parameters, and erythrocyte osmotic fragility in Wistar rats. Comp Clin Pathol. https://doi.org/10.1007/s00580-020-03144-6

    Article  Google Scholar 

  • Lamidi IY, Mikail HG, Adamu S, Akefe IO, Tijjani MB, Salihu SI, Hassan A, Daniel N, Adegoke VA (2021) Flavonoid fractions of diosmin and hesperidin mitigate lead acetate-induced biochemical, oxidative stress, and histopathological alterations in Wistar rats. Toxicol Res. https://doi.org/10.1007/s43188-020-00084-9

    Article  PubMed  Google Scholar 

  • Leathwick DM, Besier RB (2014) The management of anthelmintic resistance in grazing ruminants in Australiasia—strategies and experiences. Vet Parasitol 204:44–54

    Article  CAS  Google Scholar 

  • Pereira Machado, da Silva MA, Zehetmeyr FK, Pereira KM, Pacheco BS, Freitag RA, Pinto NB, Machado RH, Villarreal JP, de Oliveira HS, Aires Berne ME, da Silva NP (2020) Ovicidal in vitro activity of the fixed oil of Helianthus annus L. and the essential oil of Cuminum cyminum L. against Fasciola hepatica (Linnaeus, 1758). Experimental parasitology 218:107984. https://doi.org/10.1016/j.exppara.2020.107984

    Article  CAS  PubMed  Google Scholar 

  • Maestrini M, Tava MS, Tedesco D, Perrucci S (2020) In vitro anthelmintic activity of saponins from Medicago spp. against sheep gastrointestinal nematodes. Molecules (Basel, Switzerland) 25(2):242. https://doi.org/10.3390/molecules25020242

    Article  CAS  Google Scholar 

  • Miller JE, Burke JM, Terril TH, Kearney MT (2011) A Comparison of two integrated approaches of controlling nematode parasites in small ruminants. Vet Parasitol 178:300–310

    Article  CAS  Google Scholar 

  • Miró V, Lifschitz A, Viviani P, Rocha C, Lanusse C, Costa L Jr, Virkel G (2020) In vitro inhibition of the hepatic S-oxygenation of the anthelmintic albendazole by the natural monoterpene thymol in sheep. Xenobiot Fate Foreign Compd Biol Syst 50(4):408–414. https://doi.org/10.1080/00498254.2019.1644390

    Article  CAS  Google Scholar 

  • Okafor JC (1980) Edible indigenous woody plants in the rural economy of the Nigeria Forest Zone. For Ecol Manag 3:45–55

    Article  Google Scholar 

  • Okwu DE, Morah FNI (2004) Mineral and nutritive value of Dennettia tripetala fruits. Fruit Paris 59(6):439–442

    Google Scholar 

  • Onyechi JO, Chime SA, Onyishi IV, Eneiga A (2013) Formulation of Dennettia tripetala tablets by direct compression: standardization and quality control. Int J Pharm Sci Rev Res 22(2):1–4

    Google Scholar 

  • Osuagwu GGE, Eme CF (2013) The phytochemical composition and antimicrobial activity of Dialium guineense, Vitex doniana and Dennettia tripetala leaves. Asian J Nat Appl Sci 2(3):69–81

    Google Scholar 

  • Oyemitan IA, Elusiyan CA, Akanmu A, Olugbade TA (2013) Hypnotic, anticonvulsant and anxiolytic effects of 1-nitro-2-phenylethane isolated from the essential oil of Dennettia tripetala in mice. Phytomedicine 20:1315–1322

    Article  CAS  Google Scholar 

  • Peña-Espinoza M, Valente AH, Bornancin L, Simonsen HT, Thamsborg SM, Williams AR, López-Muñoz R (2020) Anthelmintic and metabolomic analyses of chicory (Cichorium intybus) identify an industrial by-product with potent in vitro antinematodal activity. Vet Parasitol 280:109088. https://doi.org/10.1016/j.vetpar.2020.109088

    Article  CAS  PubMed  Google Scholar 

  • Redfern J, Kinninmonth M, Burdass D, Verran J (2014) Using soxhlet ethanol extraction to produce and test plant materials (essential oils) for their antimicrobial properties. J Microbiol Biol Educ 15:45–46

    Article  Google Scholar 

  • Robinson S, Delongeas JL, Donald E, Dreher D, Festag M, Kervyn S (2008) A European pharmaceutical company initiative challenging the regulatory requirement for acute toxicity studies in pharmaceutical drug development. Regul Toxicol Pharmacol 50:345–352

    Article  Google Scholar 

  • Shetshak MA, Jatau ID, Suleiman MM, Ameh MP, Ada G, Akefe IO (2021) In vitro anticoccidial activities of the extract and fractions of Garcinia kola (Heckel h.) against Eimeria tenella Oocyst. Recent Patents Biotechnol. https://doi.org/10.2174/1872208315666210129095213

    Article  Google Scholar 

  • Shuaibu K (2015) Anthelmintic efficacy of crude methanol extract of dennetia tripetala G. Baker fruits with its various chemical fractions in mice experimentally infected with Heligmosomoides bakeri. MSc dissertation, Ahmadu Bello University, Zaria, p 76

  • Silva LP, Debiage RR, Bronzel-JÚnior JL, Silva R, Peixoto E (2020) In vitro anthelmintic activity of Psidium guajava hydroalcoholic extract against gastro-intestinal sheep nematodes. Anais Da Academia Brasileira De Ciencias 92(suppl 2):e20190074. https://doi.org/10.1590/0001-3765202020190074

    Article  CAS  PubMed  Google Scholar 

  • Soulsby EJL (1982) Arthropods and protozoa of domesticated animals, 7th edn. Bailer Tindal, London, p 809

    Google Scholar 

  • Taki AC, Brkljača R, Wang T, Koehler AV, Ma G, Danne J, Ellis S, Hofmann A, Chang B, Jabbar A, Urban S, Gasser RB (2020) Natural compounds from the Marine Brown Alga Caulocystis cephalornithos with potent in vitro-activity against the parasitic nematode Haemonchus contortus. Pathogens (Basel, Switzerland) 9(7):550. https://doi.org/10.3390/pathogens9070550

    Article  CAS  Google Scholar 

  • Taylor L (2000) Plant based drugs and medicines. The healing power of rainforest plants. Milam County, Texas 77857

  • Timothy CO, Okere CO (2008) Effect of Dennettia tripetala (Mmimi) seed intake on the intra-ocular pressure of Normotensive Emmetropic Nigerian Igbos. J Nigerian Optom Assoc 14:14–17

    Google Scholar 

  • Troell K, Waller P, Hoglund J (2005) The development and overwintering survival of free-living larvae of Haemonchus contortus in Sweden. J Helminthol 79:373–379

    Article  CAS  Google Scholar 

  • United States Department of Agriculture—APHIS-VS (1996). Reference of 1996 U.S. Sheep Health and Management Practices, pp 22.

  • Wabo PJ, Bilong BCF, Mpoame M (2010) In vitro nematocidal activity of extracts of Canthium manni (Rubiaceae) on different life cycle stages of Heligmosomoides polygyrus (Nematoda, Heligmosomoidae). J Helminthol 84:156–165

    Article  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 

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Acknowledgements

The authors are grateful for the technical assistance and facilities provided by the Department of Veterinary Pharmacology, Ahmadu Bello University, Zaria, in support of this research.

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  1. Department of Veterinary Pharmacology and Toxicology, Ahmadu Bello University, Zaria, Nigeria

    Rachel A. Nwosu, Mohammed M. Suleiman, Matthew P. Ameh & Manji A. Shetshak

  2. Small Ruminant Research Programme, National Animal Production Research Institute, Ahmadu Bello University, Zaria, Nigeria

    Hussaina J. Makun

  3. Department of Physiology, Biochemistry and Pharmacology, Faculty of Veterinary Medicine, University of Jos, Jos, Nigeria

    Isaac O. Akefe

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  1. Rachel A. Nwosu
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  2. Mohammed M. Suleiman
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Nwosu, R.A., Suleiman, M.M., Makun, H.J. et al. In vitro anthelmintic activity of Dennettia tripetala G. Baker (Annonaceae) Fruits against Haemonchus contortus. J Parasit Dis 46, 220–229 (2022). https://doi.org/10.1007/s12639-021-01438-2

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