Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-24T16:46:54.409Z Has data issue: false hasContentIssue false

Evaluation of Annona muricata (Graviola) leaves activity against experimental trichinellosis: in vitro and in vivo studies

Published online by Cambridge University Press:  13 September 2021

E.S. El-Wakil*
Affiliation:
Department of Parasitology, Theodor Bilharz Research Institute, Kornaish El-Nile, Warrak El-Hadar, Imbaba (P.O. 30), Giza, 12411, Egypt
H.F. Abdelmaksoud
Affiliation:
Department of Parasitology, Theodor Bilharz Research Institute, Kornaish El-Nile, Warrak El-Hadar, Imbaba (P.O. 30), Giza, 12411, Egypt
T.S. AbouShousha
Affiliation:
Department of Pathology, Theodor Bilharz Research Institute, Kornaish El-Nile, Warrak El-Hadar, Imbaba (P.O. 30), Giza, 12411, Egypt
M.M.I. Ghallab
Affiliation:
Department of Medical Parasitology, kafrelsheikh Faculty of Medicine, Kafrelsheikh University, ElGiesh street, kafrelsheikh governorate, 33516, Egypt
*
Author for correspondence: E.S. El-Wakil, E-mail: [email protected]

Abstract

Our work aimed to evaluate the possible effect of Annona muricata (Graviola) leaf extract on Trichinella spiralis in in vitro and in vivo studies. Trichinella spiralis worms were isolated from infected mice and transferred to three culture media – group I (with no drugs), group II (contained Graviola) and group III (contained albendazole) – then they were examined using the electron microscope. In the in vivo study, mice were divided into five groups: GI (infected untreated), GII (prophylactically treated with Graviola for seven days before infection), GIII (infected and treated with Graviola), GIV (infected and treated with albendazole) and GV (infected and treated with a combination of Graviola plus albendazole in half doses). Drug effects were assessed by adults and larvae load beside the histopathological small intestinal and muscular changes. A significant reduction of adult and larval counts occurred in treated groups in comparison to the control group. Histopathologically, marked improvement in the small intestinal and muscular changes was observed in treated groups. Also, massive destruction of the cultured adults’ cuticle was detected in both drugs. This study revealed that Graviola leaves have potential activity against trichinellosis, especially in combination with albendazole, and could serve as an adjuvant to anti-trichinellosis drug therapy.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdul Wahab, SM, Jantan, I, Haque, MA and Arshad, L (2018) Exploring the leaves of Annona muricata as a source of potential anti-inflammatory and anticancer agents. Frontiers in Pharmacology 9, 659661.CrossRefGoogle ScholarPubMed
Abou Rayia, DM, Saad, AE, Ashour, DS and Oreiby, RM (2017) Implication of artemisinin nematocidal activity on experimental trichinellosis: in-vitro and in-vivo studies. Parasitology International 66(2), 5663.CrossRefGoogle ScholarPubMed
Abu El Ezz, NM (2005) Effect of Nigella sativa and Allium cepa oils on Trichinella spiralis in experimentally infected rats. Journal of Egyptian Society of Parasitology 35, 511523.Google ScholarPubMed
Aguayo-Ortiz, R, Méndez-Lucio, O, Medina-Franco, JL, Castillo, R, Yépez-Mulia, L, Hernández-Luis, F and Hernández-Campos, A (2013) Towards the identification of the binding site of benzimidazoles to β-tubulin of trichinella spiralis: insights from computational and experimental data. Journal of Molecular Graphics and Modelling 41, 1219.CrossRefGoogle ScholarPubMed
Attia, RA, Mahmoud, AE, Farrag, HM, Makboul, R, Mohamed, ME and Ibraheim, Z (2015) Effect of myrrh and thyme on Trichinella spiralis enteral and parenteral phases with inducible nitric oxide expression in mice. Memorias do Institue Oswaldo Cruz 110(8), 10351041.CrossRefGoogle ScholarPubMed
Boyom, FF, Fokou, PV, Yamthe, LR, et al. (2010) Potent antiplasmodial extract from Cameroonian Annonaceae. Journal of Ethnopharmacology 134, 717724.CrossRefGoogle Scholar
Bughdadi, FA (2010) Ultrastractural studies on the parasitic worm Trichinella Spiralis. Journal of Tibah Univerity for Science 3, 3338.CrossRefGoogle Scholar
Chung, MS, Joo, KH, Quan, FS, Kwon, HS and Cho, SW (2001) Efficacy of flubendazole and albendazole against Trichinella spiralis in mice. Parasite 8(2), S195S198.CrossRefGoogle ScholarPubMed
Coria-Téllez, AV, Montalvo-Gónzalez, E, Yahia, EM and Obledo-Vázquez, EN (2018) Annona muricata: a comprehensive review on its traditional medicinal uses, phytochemicals, pharmacological activities, mechanisms of action and toxicity. Arabian Journal of Chemistry 11(5), 662691.CrossRefGoogle Scholar
Dennis, D, Despommier, D and Davis, N (1970) Infectivity of the newborn larva of Trichinella spiralis in the rat. The Journal of Parasitology 56(5), 974977.CrossRefGoogle ScholarPubMed
Djurkovc, O, Bobic, B, Nikolic, A, Klun, I and Dupouy-Camet, J (2013) Pork as a source of human parasitic infection. Clinical Microbiology and Infection 19, 586594.CrossRefGoogle Scholar
Drury, R and Wallington, E (1980) Carlton's histological technique. 5th edn. Oxford, New York, Oxford University Press.Google Scholar
Dunn, IJ and Wright, KA (1985) Cell injury caused by Trichinella spiralis in the mucosal epithelium of B10A mice. Journal of Parasitology 71(6), 757766.CrossRefGoogle ScholarPubMed
Dyab, AK, Ahmed, MA and Abdelazeem, AG (2019) Prevalence and histopathology of Trichinella spiralis larvae of slaughtered pigs in Cairo governorate, Egypt. Journal of the Egyptian Society of Parasitology 49(2), 439442.CrossRefGoogle Scholar
Ferreira, LE, Castro, P, Chagas, A, Franca, S and Beleboni, R (2013) In-vitro anthelmintic activity of aqueous leaf extract of Annona muricata (Annonaceae) against Haemonchus contortus from sheep. Experimental Parasitology 134, 327332.CrossRefGoogle ScholarPubMed
Gallardo, T, Aragón, R, Tormo, JR, Blázquez, MA, Zafra-Polo, MC and Cortes, D (1998) Acetogenins from Annona glabra seeds. Phytochemistry 47, 811816.CrossRefGoogle Scholar
Gottstein, B, Pozio, E and Nöckler, K (2009) Epidemiology, diagnosis, treatment, and control of trichinellosis. Clinical Microbiology Reviews 22, 127145.CrossRefGoogle ScholarPubMed
Hounzangbe-Adote, MS, Paolini, V, Fouraste, I, Moutairou, K and Hoste, H (2005) In-vitro effects of four tropical plants on three lifecycle stages of the parasitic nematode Haemonchus contortus. Research in Veterinary Science 78, 155160.CrossRefGoogle Scholar
Huang, H, Yao, J, Liu, K, Yang, W, Wang, G, Shi, C and Yang, G (2020) Sanguinarine has anthelmintic activity against the enteral and parenteral phases of trichinella infection in experimentally infected mice. Acta tropica 201, 105226.CrossRefGoogle ScholarPubMed
Kamaraj, C and Abdul Rahuman, A (2011) Efficacy of anthelmintic properties of medicinal plant extracts against Haemonchus contortus. Research in Veterinary Science 91, 400404.CrossRefGoogle ScholarPubMed
Kapel, CMO, Webster, P and Gamble, R (2005) Muscle distribution of sylvatic and domestic Trichinella larvae in production animals and wildlife. Veterinary Parasitology 132, 101105.CrossRefGoogle ScholarPubMed
Kim, CW and Myron, CL (1980) Surface morphology of Trichinella Spiralis by scanning electron microscopy. The Journal of Parasitology 66(1), 7581.CrossRefGoogle ScholarPubMed
Nada, S, Mohammad, SM, Moad, HS, El-Shafey, MA, Al-Ghandour, AM and Ibrahim, N (2018) Therapeutic effect of Nigella sativa and ivermectin versus albendazole on experimental trichinellosis in mice. Journal of the Egyptian Society of Parasitology 48(1), 8592.CrossRefGoogle Scholar
Nguyen-Pouplin, J, Tran, H, Tan, H, et al. (2007) Antimalarial and cytotoxic activities of ethnopharmacologically selected medicinal plants from South Vietnam. Journal of Ethnopharmacology 109, 417427.CrossRefGoogle ScholarPubMed
Nuñez, G, Gentile, T, Costantino, S, Sarchi, M and Venturiello, S (2005) In-vitro and in-vivo effects of progesterone on Trichinella spiralis newborn larvae. Parasitology 131(2), 255259.CrossRefGoogle ScholarPubMed
Osorio, E, Arango, GJ, Jiménez, N, Alzate, F, Ruiz, G, Gutiérrez, D and Robledo, S (2007) Antiprotozoal and cytotoxic activities in-vitro of Colombian Annonaceae. Journal of Ethnopharmacology 111, 630635.CrossRefGoogle ScholarPubMed
Othman, AA and Shoheib, ZS (2016) Detrimental effects of geldanamycin on adults and larvae of Trichinella spiralis. Helminthologia 53(2), 126132.CrossRefGoogle Scholar
Ozkoc, S, Tuncay, S, Delibas, SB and Akisu, C (2009) In-vitro effects of resveratrol on trichinella spiralis. Parasitology Research 105, 11391143.CrossRefGoogle ScholarPubMed
Pozio, E (2019) Trichinella and trichinellosis in Europe. Veterinarski Glasnik 73(2), 6584.CrossRefGoogle Scholar
Rady, I, Bloch, MB, Chamcheu, RN, et al. (2018) Anticancer properties of Graviola (Annona muricata): a comprehensive mechanistic review. Oxidative Medicine and Cellular Longevity 30, 139.CrossRefGoogle Scholar
Ren, Y, Qin, Y, Zhang, X, Zheng, L, Dai, X, Wu, H and Cui, Y (2018) Killing the muscular larvae of Trichinella spiralis and the anti-fibrotic effect of the combination of Wortmannilatone F and recombinant G31P in a murine model of trichinellosis. Biomedicine & Pharmacotherapy 108, 934940.CrossRefGoogle Scholar
Ross, IA (2010) Medicinal plants of the world. Chemical Constituents, Traditional and Modern Medicinal: vol. 1. 2nd edn. Totowa, New Jersey, Humana Press, 133–142.Google Scholar
Shalaby, MA, Moghazy, FM, Shalaby, HA and Nasr, SM (2010) Effect of methanolic extract of Balanites aegyptiaca fruits on enteral and parenteral stages of Trichinella spiralis in rats. Parasitology Research 107, 1725.CrossRefGoogle ScholarPubMed
Shoheib, ZS, Shamloula, MM, Abdin, AA and El-Segai, O (2006) Role of α-chymotrypsin and colchicine as adjuvant therapy in experimental muscular trichinellosis: parasitological, biochemical and immunohistochemical study. Egyptian Journal of Medical Microbiology 15, 773790.Google Scholar
Siriyasatien, P, Yingyourd, P and Nuchprayoon, S (2003) Efficacy of albendazole against early and late stage of Trichinella spiralis infection in mice. Journal of the Medical Association of Thailand 86, S257S262.Google ScholarPubMed
Somsak, V, Polwiang, N and Chachiyo, S (2016) In-vivo antimalarial activity of Annona muricata leaf extract in mice infected with Plasmodium berghei. Journal of Pathogens, 15.CrossRefGoogle ScholarPubMed
Souza, MM, Bevilaqua, CM, Morais, SM, Costa, CT, Silva, AR and Braz-Filho, R (2008) Anthelmintic acetogenin from Annona squamosa L. seeds. Anais da Academia Brasileira de Ciencias 80, 271277.CrossRefGoogle ScholarPubMed
Tritten, L, Nwosu, U, Vargas, M and Keiser, J (2012) In-vitro and in-vivo efficacy of tribendimidine and its metabolites alone and in combination against the hookworms Heligmosomoides bakeri and Ancylostoma ceylanicum. Acta Tropica 122(1), 101107.CrossRefGoogle ScholarPubMed
Vieira, LS, Cavalcante, ACR, Pereira, MF, Dantas, LB and Ximenes, LJF (1999) Evaluation of anthelmintic efficacy of plants available in Ceará state, northeast Brazil, for the control of goat gastrointestinal nematodes. Revue de Medecine Veterinaire 150, 447452.Google Scholar
Vila-Nova, NS, de Morais, SM, Falcão, MJ, Alcantara, TT, Ferreira, PA, Cavalcanti, ES, Vieira, IG, Campello, CC and Wilson, M (2013) Different susceptibilities of Leishmania spp. Promastigotes to the Annona muricata acetogenins annonacinone and corossolone, and the Platymiscium floribundum coumarin scoparone. Experimental Parasitology 133(3), 334338.CrossRefGoogle ScholarPubMed
Wakelin, D and Margaret, MW (1980) Immunity to Trichinella spiralis in irradiated mice. International Journal for Parasitology 10(1), 3741.CrossRefGoogle ScholarPubMed
Wang, X, Li, L, Wei, X, Wang, Y, Zhang, H, Shi, A, Liu, T, Yang, X and Fang, Q (2018) Proteomic analysis of the response of Trichinella spiralis muscle larvae to exogenous nitric oxide. PLoS One 13(6), 115.Google ScholarPubMed
Wassom, DL, Debra, A and Dick, TA (1988) Trichinella Spiralis infections of inbred mice: immunologically specific responses induced by different Trichinella isolates. The Journal of Parasitology 74(2), 283287.CrossRefGoogle ScholarPubMed
Yadav, AK (2012) Efficacy of Lasia spinosa leaf extract in treating mice infected with Trichinella spiralis. Parasitol Research 110(1), 493498.CrossRefGoogle ScholarPubMed
Yamthe, L, Fokou, P, Mbouna, C, Keumoe, R, Ndjakou, B, Djouonzo, P and Boyom, F (2015) Extracts from Annona muricata L and Annona Rreticulata L. (Annonaceae) potently and selectively inhibit plasmodium falciparum. Medicines 2(2), 5566.CrossRefGoogle ScholarPubMed