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BMC Complementary Medicine and Therapies
Published in: BMC Complementary Medicine and Therapies 1/2023

Open Access 01-12-2023 | Albendazole | Research

Comprehensive chemical profiling of Bassia indica Wight. aerial parts extract using UPLC-ESI–MS/MS, and its antiparasitic activity in Trichinella spiralis infected mice: in silico supported in vivo study

Authors: Magdy M. D. Mohammed, Elham A. Heikal, Fatma M. Ellessy, Tarek Aboushousha, Mosad A. Ghareeb

Published in: BMC Complementary Medicine and Therapies | Issue 1/2023

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Abstract

Background

Trichinellosis is a public health threat infected both animals and humans as a result of eating undercooked meat. It caused by Trichinella spiralis that has widespread drug resistance and even developed many sophisticated strategies for their survival, this increases the demand in searching for new anthelmintic drugs from natural source.

Methods

Our objectives were to test the in vitro and in vivo anthelmintic activity of Bassia indica BuOH frac., and to characterize its chemical composition using UPLC-ESI–MS/MS. Besides an in silico molecular docking study with the prediction of the PreADMET properties.

Results

In vitro investigation of B. indica BuOH frac., showed severe destruction of the adult worm and larvae, marked cuticle swelling, areas with vesicles, blebs and loss of annulations. This was assured via in vivo study, which revealed a significant reduction (P < 0.05) in the mean adult worm count with efficacy of 47.8% along with a significant decrease (P < 0.001) in the mean larval count per gram muscle with efficacy 80.7%. Histopathological examinations of the small intestine and muscular sections showed marked improvement. In addition, immunohistochemical findings demonstrated that B. indica BuOH frac. depressed the proinflammatory cytokines expressions of TNF-α, which was obviously upregulated by T. spiralis. Precise chemical investigation of the BuOH frac. using UPLC-ESI–MS/MS resulted in the identification of 13 oleanolic type triterpenoid saponins; oleanolic acid 3-O-6´-O-methyl-β-D-glucurono-pyranoside (1), chikusetsusaponin-IVa (2) and its methyl ester (3), chikusetsusaponin IV (4) and its methyl ester (5), momordin-Ic (6) and its methyl ester (7), betavulgaroside-I (8), -II (9) -IV (10), -X (11), licorice-saponin-C2 (12) and -J2 (13). In addition, 6 more phenolics were identified as syringaresinol (14), 3,4-di-O-caffeoylquinic acid (15), 3-O-caffeoyl-4-O-dihydrocaffeoylquinic acid (16), 3,4-di-O-caffeoylquinic acid butyl ester (17), 3,5-di-O-galloyl-4-O-digalloylquinic acid (18) and quercetin 3-O-(6´´-feruloyl)-sophoroside (19). The auspicious anthelmintic activity was further ascertained using in silico molecular docking approach that targeted certain protein receptors (β-tubulin monomer, tumor necrosis factor alpha (TNF-α), cysteine protease (Ts-CF1), calreticulin protein (Ts-CRT)), all the docked compounds (1–19) fit into the binding site of the active pocket with binding affinities noteworthy than albendazole. In addition, ADMET properties, drug score and drug likeness were predicted for all compounds.
Appendix
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Literature
1.
Rainova I, Kaftandjiev I, Harizanov R, Tsvetkova N, Jordanova D, Marinova I, Kurdova R, Kantardjiev T, Lalkovski N. Outbreaks of human trichinellosis, still a challenge for the public health authorities in Bulgaria. J Public Health. 2016;24:291–7.CrossRef
2.
Sofronic-Milosavljevic L, Ilic N, Gruden-Movsesijan A. “50. Trichinella,” in Laboratory Models for Foodborne Infections, edn. Liu D. Boca Raton FL: CRC Press; 2017. 793–08.
3.
4.
FAW/WHO. Multicriteria-based ranking for risk management of food-borne parasites, Expert Meeting, 3–7 September 2012, Rome, Italy: FAO Headquarters.
5.
McKerrow JH, Caffrey C, Kelly B, Loke P, Sajid M. Proteases in parasitic diseases. Ann Rev Pathol. 2006;1:497–536.CrossRef
6.
Qu Z-G, Ma X-T, Li W-H, Zhang N-Z, Yue L, Cui J-M, Cai J-P, Jia W-Z, Fu B-Q. Molecular characterization of a cathepsin F-like protease in Trichinella spiralis. Parasit Vectors. 2015;8:652.PubMedPubMedCentralCrossRef
7.
Shao S, Sun X, Chen Y, Zhan B, Zhu X. Complement evasion: an effective strategy that parasites utilize to survive in the host. Front Microbiol. 2019;10:532.PubMedPubMedCentralCrossRef
8.
Sharma S, Anand N. Approaches to Design and Synthesis of Antiparasitic Drugs, Vol.2, Chapter 8, Amsterdam: Elsevier; 1997.
9.
Lubega GW, Prichard RK. Specific interaction of benzimidazoles anthelmintics with tubulin: high-affinity binding and benzimidazoles resistance in Hemonchus contortus. Mol Biomol Parasitol. 1990;38:221–32.CrossRef
10.
Jiménez-González A, De Armas-Serra C, Criado-Fprnelio A, Casado-Escribano N, Rodriquez-Caabeiro F, Díez JC. Preliminary characterization and interaction of tubulin from Trichinella spiralis larvae with benzimidazole derivatives. Vet Parasitol. 1991;39:89–99.PubMedCrossRef
11.
Fennell CW, Lindsey KL, McGaw LJ, Sparg SG, Stafford GI, Elgorashi EE, Grace OM, van Staden J. Assessing African medicinal plants for efficacy and safety: pharmacological screening and toxicology. J Ethnopharmacol. 2004;94:205–17.PubMedCrossRef
12.
González-Coloma A, Reina M, Sáenz C, Lacret R, Ruiz-Mesia L, Arán VJ, Sanz J, Martínez-Díaz RA. Antileishmanial, antitrypanosomal, and cytotoxic screening of ethnopharmacologically selected Peruvian plants. Parasitol Res. 2011;110(4):1381–92.PubMedCrossRef
13.
Tackholm V. Students’ Flora of Egypt, Cairo University. 2nd Edn. 1974; 128.
14.
Othman A, Amen Y, Shimizu K. A novel acylated flavonol tetraglycoside and rare oleanane saponins with a unique acetal-linked dicarboxylic acid substituent from the xero-halophyte Bassia indica. Fitoterapia. 2021;152: 104907.PubMedCrossRef
15.
Othman A, Amen Y, Matsumoto M, Nagata M, Shimizu K, Bassiamide A. a new alkaloid from xero-halophyte Bassia indica Wight. Nat Prod Res. 2022;36(14):3610–8.PubMedCrossRef
16.
Othman A, Sayed AM, Amen Y, Shimizu K. Possible neuroprotective effects of amide alkaloids from Bassia indica and Agathophora alopecuroides: in vitro and in silico investigations. RSC Adv. 2022;12:18746.PubMedPubMedCentralCrossRef
17.
Choi YY, Kim MH, Lee JY, Hong J, Kim S-H, Yang WM. Topical application of Kochia scoparia inhibits the development of contact dermatitis in mice. J Ethnopharmacol. 2014;154(2):380–5.PubMedCrossRef
18.
Al-Snafi AE. A review on pharmacological activities of Kochia scoparia. Indo American J Pharmaceut Sci. 2018;5(4):2213–21.
19.
Yusufoglu HS. Analgesic, antipyretic, nephritic and antioxidant effects of the aerial parts of Bassia eriophora (Family: Chenopodiaceae) plant on rats. Asian Pacific J Trop Dis. 2015;5(7):559–63.CrossRef
20.
Aboul-Enein AM, Abu El-Ela F, Shalaby EA, El-Shemy HA. Traditional medicinal plants research in Egypt: studies of antioxidant and anticancer activities. J Med Plants Res. 2012;6(5):689–703.
21.
Bibi H, Hussain M, Jan G, Shah GM, Khan S, Ihsan Ullah. Phytochemical analysis and antimicrobial activities of Kochia indica (Wight), plant growing in District Karak Khyber Puhktunkhuwa. Pakistan Pure Appl Biol. 2021;10(3):789–96.
22.
Javed S, Javaid A, Qureshi MZ. Antifungal phytocomponents in n-butanol fraction of leaf extract of kochia indica WIGHT. Int J Biol Biotech. 2018;15(4):661–6.
23.
Wagner H, Bladt S. Plant Drug Analysis: A Thin Layer Chromatography Atlas. 2nd ed. New York: Springer; 1996. p. 320.CrossRef
24.
Abou Rayia DM, Saad AE, Ashour DS, Oreiby RM. Implication of artemisinin nematocidal activity on experimental trichinellosis: In vitro and in vivo studies. Parasitol Int. 2017;66(2):56–63.PubMedCrossRef
25.
Ozkoc S, Tuncay S, Delibas SB, Akisu C. In vitro effects of resveratrol on Trichinella spiralis. Parasitol Res. 2009;105(4):1139–43.PubMedCrossRef
26.
Dennis D, Despommier D, Davis N. Infectivity of the newborn larva of Trichinella spiralis in the rat. The J Parasitol. 1970;56(5):974–7.PubMedCrossRef
27.
Kapel CMO, Webster P, Gamble HR. Muscle distribution of sylvatic and domestic Trichinella larvae in production animals and wildlife. Vet Parasitol. 2005;132(1–2):101–5.PubMedCrossRef
28.
Wakelin D, Wilson MM. Immunity to Trichinella spiralis in irradiated mice. Int J Parasitol. 1980;10(1):37–41.PubMedCrossRef
29.
Vila-Nova SM, de Morais SM, Falcão MJC, Alcantara TTN, Ferreira PAT, Cavalcanti ESB, Vieira IGP, Campello CC, Wilson M. Different susceptibilities of Leishmania spp. promastigotes to the Annona muricata acetogenins annonacinone and corossolone, and the Platymiscium floribundum coumarin scoparone. Exp Parasitol. 2013;133(3):334–8.PubMedCrossRef
30.
Bughdadi FA. Ultrastructural studies on the parasitic worm Trichinella Spiralis. J Taibah Univ Sci. 2010;3(1):33–8.CrossRef
31.
Saxena SCRC, Chaurasia ID, Shrivastav R. Antidiabetic activity of Luffa aegyptiaca (Mill) in alloxan induced diabetic rats. J Chem Pharm Res. 2011;3:522–5.
32.
Attia RA, Mahmoud AE, Farrag HM, Makboul R, Mohamed ME, Ibraheim Z. Effect of myrrh and thyme on Trichinella spiralis enteral and parenteral phases with inducible nitric oxide expression in mice. Memorias do Institue Oswaldo Cruz. 2015;110(8):1035–41.CrossRef
33.
Nunez GG, Gentile T, Costantino SN, Sarchi MI, Venturiello SM. In vitro & in vivo effects of progesterone on Trichinella spiralis newborn larvae. Parasitol. 2005;131(2):255–9.CrossRef
34.
Drury RA, Wallington EA. Carleton’s Histological Technique. 5th ed. New York: Oxford University Press; 1980.
35.
36.
Lovell S, Davis I, Arendall WB, De Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC. Structure validation by Cα geometry: ϕ, ψ and Cβ deviation. Proteins. 2003;50(3):437–50.PubMedCrossRef
37.
Oduselu GO, Olayinka OA, Yvonne UA, Brors B, Adebiyi E. Homology modelling and molecular docking studies of selected substituted benzo [d] Imidazol-1-Yl) Methyl) benzimidamide scaffolds on plasmodium falciparum adenylosuccinate lyase receptor. Bioinform Biol Insights. 2019;13:1–10.CrossRef
38.
Muir AD, Ballantyne KD, Hall TW. LC-MS and LC-MS/MS Analysis of Saponins and Sapogenins Comparison of Ionization Techniques and Their Usefulness in Compound Identification. Chapter 4. In: Saponins in Food, Feedstuffs and Medicinal Plants. Oleszek W, Marston A. (eds.). Netherlands: Kluwer Academic Publishers; 2000. 35–41.
39.
Mohamed KM, Hasanean HH, Ohtani K, Yamasaki K. Triterpenoidal saponins from Kochia indica Wight. Bull Pharmaceut Sci Assuit Univ. 1998;21(1):27–36.
40.
Choi J, Lee KT, Jung HJ, Park HS, Park HJ. Anti-rheumatoid arthritis effect of the Kochia scoparia fruits and activity comparison of momordin Ic, its prosapogenin and sapogenin. Arch Pharmacal Res. 2002;25(3):336–42.CrossRef
41.
Kamel MS, Ohtani K, Mohamed KM, Hassanean HA, Kasai R, Yamasaki K. Acylated flavonoid glycosides from Bassia muricate. Phytochem. 2001;57:1259–62.CrossRef
42.
Zhou J, Xie G, Yan X. Encyclopedia of Traditional Chinese Medicines; Molecular Structures, Pharmacological Activities, Natural Sources and Applications Vol. 1–6. Berlin Heidelberg: Springer-Verlag; 2011.
43.
Yannai S. Dictionary of Food Compounds. Taylor & Francis Group, Boca Raton: CRC Press; 2013.
44.
Yadav AK. Anthelmintic activity of Gynura angulosa against Trichinella spiralis infections in mice. Pharmacol Online. 2006;2:299–306.
45.
Djurković-Djaković O, Bobić B, Nikolić A, Klun I, Dupouy-Camet J. Pork as a source of human parasitic infection. Clin Microbiol Infect. 2013;19(7):586–94.PubMedCrossRef
46.
Thompson DP, Geary TG. The Structure and Function of Helminth Surfaces. In: Marr JJ, editor. Edn, Biochemistry and Molecular Biology of Parasites. New York: Academic Press; 1995. p. 203–32.CrossRef
47.
Xiao SH, Guo J, Chollet J, Wu JT, Tanner M, Utzinger J. Effect of artemether on Schistosoma mansoni: dose-efficacy relationship, and changes in worm morphology and histopathology. Chinese J Parasitol Parasit Dis. 2004;22(3):148–53.
48.
Abdel-Hamid NM, Tabl GA, El-Bolkiny YE, Zeina WO. In vitro antitumor efficacy of Kochia indica extract on human hepatocellular carcinoma cell line with or without 5-fluorouracil. Hepatoma Res. 2017;3:149–55.CrossRef
49.
Nikesh M, Binitha G, Rekha S, Ravindra N, Anto-Sharing M. Comparative in vitro anthelmintic activity of chloroform and acetone extracts of Menthe piperita. Int J Pharmaceut Biologic Arch. 2011;2:945–50.
50.
Hostettmann K, Marston A. Saponins: Chemistry and Pharmacology of Natural Products; Phillipson JD, Baxter H. Eds.; Cambridge, UK: Cambridge University Press; 1995.
51.
Cavalcanti Gomes DC, de Lima HG, Vaz AV, Santos NS, Santos FO, Dias ÊR, Botura MB, Branco A, Batatinha MJ. In vitro anthelmintic activity of the Zizyphus joazeiro bark against gastrointestinal nematodes of goats and its cytotoxicity on Vero cells. Vet Parasitol. 2016;226:10–6.CrossRef
52.
Hernandez-Villegas MM. Ovicidal and larvicidal activity of the crude extracts from Phytolacca icosandra against Haemonchus contortus. Vet Parasitol. 2011;179:100–6.PubMedCrossRef
53.
Ekeanyanwu RC, Etienjirhevwe OF. In vitro anthelmintic potentials of Xylopia aethiopica and Mondora myristica from Nigeria. Afr J Biochem Res. 2012;6:115–20.CrossRef
54.
55.
Lu C, Zhang HY, Ji J, Wang GX. In vivo anthelmintic activity of Dryopteris crassirhizoma, Kochia scoparia, and Polygala tenuifolia against Dactylogyrus intermedius (Monogenea) in goldfish (Carassius auratus). Parasitol Res. 2012;110(3):1085–90.PubMedCrossRef
56.
El-Wakil ES, Abdelmaksoud HF, AbouShousha TS, Ghallab MMI. Evaluation of Annona muricata (Graviola) leaves activity against experimental trichinellosis: In vitro and in vivo studies. J Helminthol. 2021;95: e53.PubMedCrossRef
57.
Dyab AK, Ahmed MA, Abdelazeem AG. Prevalence and histopathology of Trichinella spiralis larvae of slaughtered pigs in Cairo governorate. Egypt J Egyptian Soc Parasitol. 2019;49(2):439–42.CrossRef
58.
Bruschi F, D’Amato C, Piaggi S, Bianchi C, Castagna B, Paolicchi A, Pinto B. Matrix metalloproteinase (MMP)-9: A reliable marker for inflammation in early human trichinellosis. Vet Parasitol. 2016;231:132–6.PubMedCrossRef
59.
Li Z, Li J, Zhu L, Zhang Y, Zhang J, Yao L, Liang D, Wang L. Celastrol nanomicelles attenuate cytokine secretion in macrophages and inhibit macrophage-induced corneal neovascularization in rats. Int J Nanomed. 2016;11:6135–48.CrossRef
60.
Xu F, Hou B, Zhu X, Liu Y, Shi X, Li S, Li Z, Cai W, Zhou Y, Qiu L. Vaccaria n-butanol extract lower the production of proinflammatory cytokines and the infection risk of T. spiralis in vivo. Acta Parasitologic. 2019;64(3):520–7.CrossRef
61.
62.
63.
Satyendra RV, Vishnumurthy KA, Vagdevi HM, Dhananjaya BL, Shruthi A. Synthesis, in vitro anthelmintic, and molecular docking studies of novel 5-nitro benzoxazole derivatives. Med Chem Res. 2015;24:1342–50.CrossRef
64.
Aguayo-Ortiz R, Méndez-Lucio O, Medina-Franco JL, Castillo R, Yépez-Mulia L, Hernández-Luis F, Hernández-Campos A. Towards the identification of the binding site of benzimidazoles to β-tubulin of Trichinella spiralis: insights from computational and experimental data. J Mol Graph Mod. 2013;41:12–9.CrossRef
65.
Robinson MW, McFerran N, Trudgett A, Hoey L, Fairweather I. A possible model of benzimidazole binding to β-tubulin disclosed by invoking an inter-domain movement. J Mol Graph Mod. 2004;23:275–84.CrossRef
66.
Zia K, Ashraf S, Jabeen A, Saeed M, Nur-e-Alam M, Ahmed S, Al-Rehaily AJ, Ul-Haq Z. Identification of potential TNF-alpha inhibitors; from in silico to in vitro studies. Sci Rep. 2020;10:20974.PubMedPubMedCentralCrossRef
67.
Zhao L, Shao S, Chen Y, Sun X, Sun R, Huang J, Zhan B, Zhu XT. spiralis calreticulin binds human complement C1q as an immune evasion strategy. Front Immunol. 2017;8:636.PubMedPubMedCentralCrossRef
68.
Patil R, Das S, Stanley A, Yadav L, Sudhakar A, Varma AK. Optimized hydrophobic interactions and hydrogen bonding at the target-ligand interface leads the pathways of drug-designing. PLoS One. 2010;5(8): e12029.PubMedPubMedCentralCrossRef
69.
Barry M, Feely J. Enzyme induction and inhibition. Pharmacol Therapeut. 1990;48:71–91.CrossRef
70.
Lipinski CA, Franco L, Dominy BW, Feeney PJ. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev. 1997;23(1–3):3–26.CrossRef
71.
Daina A, Michielin O, Zoete V. SwissADME: a free web tool to evaluate pharmaco-kinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Sci Rep. 2017;7:42717.PubMedPubMedCentralCrossRef
72.
Yee S. In vitro permeability across Caco-2 cells (colonic) can predict in vivo (small intestinal) absorption in man-fact or myth. Pharmaceut Res. 1997;14:763–6.CrossRef
73.
Yamashita S, Furubayashi T, Kataoka M, Sakane T, Sezaki H, Tokuda H. Optimized conditions for prediction of intestinal drug permeability using Caco-2 cells. European J Pharmaceut Sci. 2000;10:195–204.CrossRef
74.
Ma X, Chen C, Yang J. Predictive model of blood-brain barrier penetration of organic compounds. Acta Pharmacol Sin. 2005;26:500–12.PubMedCrossRef
75.
Finch A, Pillans P. P-glycoprotein and its role in drug-drug interactions. Aust Prescr. 2014;37:137–9.CrossRef
76.
Lynch T, Price A. The effect of cytochrome P450 metabolism on drug response, interactions, and adverse effects. Am Fam Phys. 2007;76(3):391–6.
Metadata
Title
Comprehensive chemical profiling of Bassia indica Wight. aerial parts extract using UPLC-ESI–MS/MS, and its antiparasitic activity in Trichinella spiralis infected mice: in silico supported in vivo study
Authors
Magdy M. D. Mohammed
Elham A. Heikal
Fatma M. Ellessy
Tarek Aboushousha
Mosad A. Ghareeb
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2023
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-023-03988-9

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