Abstract
Alstonia scholaris, Cardiospermum halicacabum, Hydrocotyle sibthorpioides, and Hypericum japonicum are important folk medicinal plants used by tribal communities of Bodoland region of Assam to treat helminth infections. Because of their ethnomedicinal values, the present study was designed to investigate the antioxidant, antiproliferative, and anthelmintic activities of the plants. The antioxidant activity was measured by total antioxidant capacity, total phenolics (TPC), total flavonoid (TFC), FRAP, DPPH, ABTS, and TBARS assay. Antiproliferative and apoptosis-inducing activities of plants were conducted in Dalton’s lymphoma (DL) cells. Cells were treated for 24 h with different doses (25–200 mg/mL) of plant extracts. Anthelmintic study was conducted by treating the Paramphistomum sp. at different doses of plant extracts. Phytochemical and antioxidant studies showed rich TPC, TFC, and free radical scavenging activity in H. japonicum and H. sibthorpioides. Both the antiproliferative and anthelmintic bioassays showed a dose-dependent efficacy in all plants. H. japonicum showed the strongest anthelmintic activity (LC50 0.21 mg/mL) followed by H. sibthorpioides (5.36 mg/mL), C. halicacabum (13.40 mg/mL), and A. scholaris (18.40 mg/mL). Evidently, H. sibthorpioides showed the strongest antiproliferative and apoptosis-inducing activities among all the plants. The study observed a positive correlation between the antioxidant properties and antiproliferative and anthelmintic activities of the plants. We, therefore, conclude that the phytocompounds present in the crude extracts along with antioxidant molecules may have combined effects contributing to the antiproliferative and anthelmintic activities of the plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
The authors confirm that the data supporting the findings of the study are available within the manuscript.
References
Akhtar MS, Iqbal Z, Khan MN et al (2000) Anthelmintic activity of medicinal plants with particular reference to their use in animals in the Indo-Pakistan subcontinent. Small Ruminant Res 38(2):99–107
Akkari H, B’chir F, Hajaji H et al (2016) Potential anthelmintic effect of Capparis spinosa (Capparidaceae) as related to its polyphenolic content and antioxidant activity. Vet Med 61:308–316. https://doi.org/10.17221/169/2015-VETMED
Alasmary FAS, Awaad AS, Kamal M et al (2018) Antitumor activity of extract and isolated compounds from Drechslera rostrata and Eurotium tonophilum. Saudi Pharm J 26(2):279–285. https://doi.org/10.1016/j.jsps.2017.11.011
Aryal A, Upreti S, Das K (2017) Evaluation of anthelmintic activity of Citrus reticulata: In vitro and its phytochemical investigation. Asian J Pharm Clin Res 10(5):278–280. https://doi.org/10.22159/ajpcr.2017.v10i5.17406
Athnasiadou S, Kyriazakis I, Jackson F et al (2001) Direct anthelmintic effects of condensed tannins towards different gastrointestinal nematodes of sheep: In vitro and in vivo studies. Vet Parasitol 99:205–219. https://doi.org/10.1016/s0304-4017(01)00467-8
Barukial J, Sarmah JN (2011) Ethnomedicinal plants used by the people of Golaghat district, Assam, India. Int J Med Aromat Plants 1(3):203–211
Basu P, Meza E, Bergel M et al (2020) Estrogenic, antiestrogenic and antiproliferative activities of Euphorbia bicolor (Euphorbiaceae) latex extracts and its phytochemicals. Nutrients 12(1):59. https://doi.org/10.3390/nu12010059
Belemlilga MB, Traore A, Ouedraogo S et al (2016) Anthelmintic activity of Saba senegalensis (A.DC.) Pichon (Apocynaceae) extract against adult worms and eggs of Haemonchus contortus. Asian Pac J Trop Biomed 6(11):945–949. https://doi.org/10.1016/j.apjtb.2016.07.015
Carlson CJ, Phillips AJ, Dallas TA et al (2020) What would it take to describe the global diversity of parasites? Proc R Soc B 287:20201841. https://doi.org/10.1098/rspb.2020.1841
Daimari M, Roy MK, Swargiary A et al (2019) An ethnobotanical survey of antidiabetic medicinal plants used by the Bodo tribe of Kokrajhar district. Assam Indian J Tradit Know 18(3):421–429
Dillard CJ, German JB (2000) Phytochemicals: Nutraceuticals and human health. J Sci Food Agric 80:1744–1756. https://doi.org/10.1002/1097-0010(20000915)80:12%3c1744::AID-JSFA725%3e3.0.CO;2-W
Divya PJ, Jamuna P, Jyothi LA (2016) Antioxidant properties of fresh and processed Citrus aurantium fruit. Cogent Food Agric 2:1184119. https://doi.org/10.1080/23311932.2016.1184119
Dixon MA, Braae UC, Winskill P et al (2019) Strategies for tackling Taenia solium taeniosis/cysticercosis: a systematic review and comparison of transmission models, including an assessment of the wider Taeniidae family transmission models. PLOS Negl Trop Dis 13(4):1–24. https://doi.org/10.1371/journal.pntd.0007301
Eguale T, Giday M (2009) In vitro anthelmintic activity of three medicinal plants against Haemonchus contortus. Int J Green Pharm 3(1):29–34. https://doi.org/10.4103/0973-8258.49371
Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516. https://doi.org/10.1080/01926230701320337
Erdogan MK, Geçibesler IH, Behcet L (2020) Chemical constituents, antioxidant, anti-proliferative and apoptotic effects of a new endemic Boraginaceae species: Paracaryum bingoelianum. Results Chem. https://doi.org/10.1016/j.rechem.2020.100032
Fahad FI, Barua N, Islam MS et al (2021) Investigation of the pharmacological properties of Lepidagathis hyaline Nees through experimental approaches. Life 11(3):180. https://doi.org/10.3390/life11030180
Gainza YA, Domingues LF, Perez OP et al (2015) Anthelmintic activity in vitro of Citrus sinensis and Melaleuca quinquenervia essential oil from Cuba on Haemonchus contortus. Ind Crop Prod 76:647–652. https://doi.org/10.1016/j.rechem.2020.100032
Grigalius I, Petrikaite V (2017) Relationship between antioxidant and anticancer activity of trihydroxyflavones. Molecules 22(12):2169. https://doi.org/10.3390/molecules22122169
Horwitt MK (1991) Data supporting supplementation of humans with vitamin E. J Nutr 121:424–429. https://doi.org/10.1093/jn/121.3.424
Hotez PJ, Pecoul B, Rijal S et al (2018) Eliminating the neglected tropical diseases: translational science and new technologies. PLoS Negl Trop Dis 10(3):e0003895. https://doi.org/10.1371/journal.pntd.0003895
Huang S, Huang G, Ho Y et al (2008) Antioxidant and antiproliferative activities of the four Hydrocotyle species from Taiwan. Bot Stud 49:311–322
Huda-Faujan N, Noriham A, Norrakiah AS et al (2009) Antioxidant activity of plants methanolic extracts containing phenolic compounds. Afr J Biotechnol 8(3):484–489
Iloki-Assanga SB, Lewis L, Rivera EG et al (2013) Effect of maturity and harvest season on antioxidant activity, phenolic compounds and ascorbic acid of Morinda citrifolia L (Noni) grown in Mexico. Afr J Biotechnol 12(29):4630–4639
Iloki-Assanga SB, Lewis-Lujan LM, Lara-Espinoza CL et al (2015) Solvent effects on phytochemical constituent profiles and antioxidant activities, using four different extraction formulations for analysis of Bucida buceras L. and Phoradendron californicum. BMC Res Notes 8:396. https://doi.org/10.1186/s13104-015-1388-1
Irshad M, Singh M, Rizvi M (2010) Assessment of anthelmintic activity of Cassia fistula L. Middle East J Sci Res 5(5):346–349. https://doi.org/10.5455/javar.2019.f338
Irshad M, Zafaryab M, Singh M et al (2012) Comparative analysis of the antioxidant activity of Cassia fistula extracts. Int J Med Chem. https://doi.org/10.1155/2012/157125
James SL, Abate D, Abate KH et al (2018) Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 392:1789–1858. https://doi.org/10.1016/S0140-6736(18)32279-7
Kamaruddin MF, Hossain MZ, Mohamed Alabsi A et al (2019) The antiproliferative and apoptotic effects of capsaicin on an oral squamous cancer cell line of Asian Origin, ORL-48. Medicina 55(7):322. https://doi.org/10.3390/medicina55070322
Khurshid Y, Syed B, Simjee SU et al (2020) Antiproliferative and apoptotic effects of proteins from black seeds (Nigella sativa) on human breast MCF-7 cancer cell line. BMC Complem Med Ther 20(5):1–11. https://doi.org/10.1186/s12906-019-2804-1
Khyade MS, Kasote DM, Vaikos NP (2014) Alstonia scholaris (L.) R. Br. and Alstonia macrophylla Wall. ex G. Don: a comparative review on traditional uses, phytochemistry and pharmacology. J Ethnopharmacol 153(1):1–18. https://doi.org/10.1016/j.jep.2014.01.025
Krishna Murti K, Panchal MA, Lambole V et al (2010) Pharmacological properties of Cardiospermum halicacabum—a review. Pharmacologyonline 2:1005–1009
Kumar HN, Kulkarni BD, Hoskeri JH et al (2013) Bactericidal, fungicidal and anthelmintic activities of Alstonia scholaris bark extracts. Int J Phytomed 5:18–25
Kumari S, Elancheran R, Kotoky J et al (2016) Rapid screening and identification of phenolic antioxidants in Hydrocotyle sibthorpioides Lam. by UPLC–ESI-MS/MS. Food Chem 203:521–529. https://doi.org/10.1016/j.foodchem.2016.02.101
Liu L, Liu M, He J (2014) Hypericum japonicum Thunb. ex Murray: phytochemistry, pharmacology, quality control and pharmacokinetics of an important herbal medicine. Molecules 19(8):10733–10754. https://doi.org/10.3390/molecules190810733
Lowe HI, Toyang NJ, Watson C et al (2013) In vitro anticancer activity of the crude extract and two dicinnamate isolates from the Jamaican Ball Moss (Tillandsia recurvata L). Am Int J Contemp Res 3(1):93–96
Mamta, Mehrotra S, Amitabh et al (2015) Phytochemical and antimicrobial activities of Himalayan Cordyceps sinensis (Berk.) Sacc. Indian J Exp Biol 53(1):36–43
Mathan Kumar S, Juju V, Chamundeeswari D (2019) Investigation of phytoconstituents of Cardiospermum halicacabum and its efficacy as a potential anti-cancer drug candidate. J Drug Deliv Ther 9(4-s):252–257. https://doi.org/10.22270/jddt.v9i4-s.2592
Mohaddesi B, Dudhrejiya A, Sheth NR (2015) Anticancer screening of various seed extract of Cardiospermum halicacabum on human colorectal, skin and breast cancer cell lines. Arch Breast Cancer 2(3):91–95. https://doi.org/10.19187/abc.20152391-95
Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55. https://doi.org/10.1016/0022-1759(83)90303-4
Mosthafa MH, Sheweita S, O’Connor PJ (1999) Relationship between schistosomiasis and bladder cancer. Clin Microbiol Rev 12(1):97–111
Mphahlele M, Molefe N, Tsotetsi-Khambule A et al (2019) Anthelmintic resistance in livestock, helminthiasis, omolade olayinka Okwa. IntechOpen. https://doi.org/10.5772/intechopen.87124
Ohkawa H, Ohishi N, Yagi K (1979) Assay of lipid peroxidation in animal tissue by thiobarbituric acid reaction. Anal Biochem 95(2):351–358. https://doi.org/10.1016/0003-2697(79)90738-3
Ordonez AAL, Gomez JD, Vattuone MA et al (2006) Antioxidant activities of Sechium edule (Jacq.) Swartz extracts. Food Chem 97(3):452–458. https://doi.org/10.1016/j.foodchem.2005.05.024
Panda SK, Das R, Leyssen P et al (2018) Assessing medicinal plants traditionally used in the Chirang Reserve Forest, Northeast India for antimicrobial activity. J Ethnopharmacol 225:220–233. https://doi.org/10.1016/j.jep.2018.07.011
Pereira DM, Valentão P, Pereira JA et al (2009) Phenolics: from chemistry to biology. Molecules 14(6):2202–2211. https://doi.org/10.3390/molecules14062202
Qamar MF, Maqbool A, Ahmad N (2011) Economic losses due to haemonchosis in sheep and goats. Sci Intern 23(4):321–324
Rais J, Jafri A, Bano S et al (2019) Antiproliferative and apoptotic effects of Rheum emodi on human breast adeno carcinoma, MCF-7 Cells, and antimicrobial effectiveness against selected bacterial strains. Phcog Mag 15(64):237–242. https://doi.org/10.4103/pm.pm_674_18
Re R, Pellegrini N, Proteggente A et al (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26(9–10):1231–1237. https://doi.org/10.1016/s0891-5849(98)00315-3
Roy B, Swargiary A (2009) Anthelmintic efficacy of ethanolic shoot extract of Alpinia nigra on tegumental enzymes of Fasciolopsis buski, a giant intestinal parasite. J Parasit Dis 33(1–2):48–53. https://doi.org/10.1007/s12639-009-0008-1
Salhan M, Kumar B, Tiwari P et al (2011) Comparative anthelmintic activity of aqueous and ethanolic leaf extracts of Clitoria ternatea. Int J Drug Dev Res 3(1):62–69
Sammar M, Abu-Farich B, Rayan I et al (2019) Correlation between cytotoxicity in cancer cells and free radical-scavenging activity: in vitro evaluation of 57 medicinal and edible plant extracts. Oncol Lett 18:6563–6571. https://doi.org/10.3892/ol.2019.11054
Seidel V (2005) Initial and bulk extract. In: Satyajit D, Sarker SD, Latif Z, Gray AI (eds) Natural product research, 2nd edn. Humana Press, Totowa, New Jersey, pp 29–33
Serafini M, Ghiselli A, Ferro-Luzzi A (1996) In-vivo antioxidant effect of green and black tea in man. Eur J Clin Nutr 50:28–32 (PMID: 8617188)
Singh M, Kaur M, Silakari O (2014) Flavones: An important scaffold for medicinal chemistry. Eur J Med Chem 84:206–239. https://doi.org/10.1016/j.ejmech.2014.07.013
Squier MKT, Cohen JJ (2001) Standard quantitative assays for apoptosis. Mol Biotechnol 19:305. https://doi.org/10.1385/MB:19:3:305
Stein JH, Keevil JG, Wiebe DA et al (1999) Purple grape juice improves endothelial function and reduces the susceptibility of LDL cholesterol to oxidation in patients with coronary artery disease. Circulation 100(10):1050–1055. https://doi.org/10.1161/01.cir.100.10.1050
Surya Surendren P, Jayanthi G, Smitha KR (2011) In vitro evaluation of the anticancer effect of methanolic extract of Alstonia scholaris leaves on mammary carcinoma. J Appl Pharm Sci 2(5):142–149. https://doi.org/10.7324/JAPS.2012.2526
Swargiary A, Daimari A, Daimari M et al (2016) Phytochemicals, antioxidant and anthelmintic activity of selected traditional wild edible plants of Lower Assam. Indian J Pharmacol 48(4):418–423. https://doi.org/10.4103/0253-7613.186212
Swargiary A, Daimari M (2021) GC–MS analysis of phytocompounds and antihyperglycemic property of Hydrocotyle sibthorpioides Lam. SN Appl Sci. https://doi.org/10.1007/s42452-020-04101-2
Swargiary A, Daimari M, Roy MK (2020) Survey and documentation of anthelmintic plants used in traditional medicine system of tribal communities of Udalguri district of Assam. India. J Appl Pharm Sci 10(1):46–54. https://doi.org/10.7324/JAPS.2020.101006
Swargiary A, Nath P, Basumatary B et al (2017) Phytochemical, antioxidant, and trace element analysis of anthelmintic plants of north-east India. Int J Pharm Pharm Sci 9(9):228–232. https://doi.org/10.22159/ijpps.2017v9i9.20668
Swargiary A, Roy MK, Daimari M (2019a) Survey and documentation of ethnobotanicals used in the traditional medicines system of tribal communities of Chirang district of Assam against helminthiasis. Biomed Pharmacol J 12(4):1923–1935. https://doi.org/10.13005/bpj/1824
Swargiary A, Roy MK, Daimari M (2019b) Survey and documentation of putative anthelmintic plants used in ethnomedicinal systems of tribal communities of Baksa district of Assam. Med Plants 11(4):368–379. https://doi.org/10.5958/0975-6892.2019.00048.0
Swargiary A, Verma AK, Singh S et al (2021) Antioxidant and antiproliferative activity of selected medicinal plants of lower Assam, India: an in vitro and in-silico study. Anticancer Agent Med Chem 21(2):267–277. https://doi.org/10.2174/1871520620666200719000449
Tandon V, Yadav AK, Roy B et al (2011) Phytochemicals as cure of worm infections in traditional medicine systems. In: Kumar S (ed) Srivastava UC. Emerging trends in zoology, Narendra Publishing House, pp 351–378
Uniting to Combat Neglected Tropical Diseases (2014) Delivering on promises and driving progress. https://unitingtocombatntds.org/wp-content/uploads/2017/11/2nd_report_summary_english.pdf
Valko M, Leibfritz D, Moncol J et al (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39(1):44–84. https://doi.org/10.1016/j.biocel.2006.07.001
Verma AK, Prasad SB (2013) Changes in glutathione, oxidative stress and mitochondrial membrane potential in apoptosis involving the anticancer activity of cantharidin isolated from redheaded blister beetles, Epicauta hirticornis. Anticancer Agent Med Chem 13:1096. https://doi.org/10.2174/18715206113139990131
Wahyuni S, Sunarso S, Prasetiyono BWHE et al (2019) Exploration of anthelmintic activity of Cassia spp. extracts on gastrointestinal nematodes of sheep. J Adv Vet Anim Res 6:236–240. https://doi.org/10.5455/javar.2019.f338
Wang CM, Tsai SJ, Jhan YL et al (2017) Anti-proliferative activity of triterpenoids and sterols isolated from Alstonia scholaris against non-small-cell lung carcinoma cells. Molecules 22(12):2119. https://doi.org/10.3390/molecules22122119
WHO (2010) Working to overcome the global impact of neglected tropical diseases: First WHO report on Neglected Tropical Diseases. WHO Press, World Health Organization, Switzerland. https://apps.who.int/iris/handle/10665/70503
Wong RS (2011) Apoptosis in cancer: from pathogenesis to treatment. J Exp Clin Cancer Res 30(87):1–14. https://doi.org/10.1186/1756-9966-30-87
Yang X, Li Y, Su J et al (2016) Hyperjapones A-E, terpenoid polymethylated acylphloroglucinols from Hypericum japonicum. Org Lett 18(8):1876–1879. https://doi.org/10.1021/acs.orglett.6b00650
Yu F, Yu F, McGuire PM et al (2007) Effects of Hydrocotyle sibthorpioides extract on transplanted tumors and immune function in mice. Phytomedicine 14(2–3):166–171. https://doi.org/10.1016/j.phymed.2006.03.010
Zhu W, Qiu J, Zeng Y et al (2019) Cytotoxic phenolic constituents from Hypericum japonicum. Phytochemistry 164:33–40. https://doi.org/10.1016/j.phytochem.2019.04.012
Acknowledgements
AS would like to thank SERB, Govt. of India for providing financial assistance in the form of research project to carry out the present work. The authors would also like to thank the traditional healer and elderly people for providing ethnomedicinal information. The authors also acknowledge Dr. Sanjib Baruah, Department of Botany for helping in the scientific validation of the sample plants. The authors also acknowledge the infrastructural facilities provided by the Department of Zoology, Bodoland University.
Funding
The present study was funded by Science and Engineering Research Board, Government of India (File no. EEQ/2017/000071).
Author information
Authors and Affiliations
Contributions
AS involved in designing the study, statistical calculations, and writing of the manuscript, MKR carried out the antioxidant and anthelmintic study, and AKV conducted the antiproliferative and apoptosis study. All authors read and reviewed the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Authors do not have any conflict of interest.
Consent for publication
All the authors gave their consent for publication.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Swargiary, A., Roy, M.K. & Verma, A.K. In vitro study of the antioxidant, antiproliferative, and anthelmintic properties of some medicinal plants of Kokrajhar district, India. J Parasit Dis 45, 1123–1134 (2021). https://doi.org/10.1007/s12639-021-01410-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12639-021-01410-0