Nutritional assessment, antioxidant, anti-inflammatory and antidiabetic potential of traditionally used wild plant, Berberis tinctoria Lesch.

Subject Areas : Phytomedicine

Arumugam Vignesh ¹ , Kumarasamy Pradeepa Veerakumari ² , Subramaniam Selvakumar ³ , Rajan Rakkiyappan ⁴ , Krishnan Vasanth ⁵

1 - Department of Botany, Bharathiar University, Coimbatore 641 046, Tamil Nadu, India
2 - Department of Statistics, Bharathiar University, Coimbatore - 641 046, Tamil Nadu, India
3 - Department of Biochemistry, Bharathiar University, Coimbatore 641 046, Tamil Nadu, India
4 - Department of Mathematics, Bharathiar University, Coimbatore - 641 046, Tamil Nadu, India
5 - Department of Botany, Bharathiar University, Coimbatore 641 046, Tamil Nadu, India

Received: 2020-11-11 Accepted : 2021-05-15 Published : 2021-06-01

Keywords: <i>Berberis tinctoria</i> Lesch, Anti-inflammatory, Proximate analysis, Antioxidant, micronutrients, Antidiabetic,

Abstract :

< p>This study divulges a comparative analysis of Berberis tinctoria Lesch. leaf, stem, and fruit towards proximate contents assessment, e.g., moisture, crude-ash, crude-fibre, crude-lipid, crude-protein, nitrogen-free extract, energy followed by ICP-MS analysis which revealed that fruits have a higher amount of essential minerals. The primary metabolites were higher in the fruit extract, whereas more secondary metabolites were observed in the methanolic extracts in the hierarchy of leaf and fruit then stem, respectively. Likewise, a higher amount of antioxidant activities were observed in ethyl acetate and methanolic extracts. The fruit ethyl acetate extract showed a maximum of 95.27% anti-inflammatory activity. The fruit methanolic extract exhibited an antidiabetic activity with IC50 values of 75.5 ± 6.8 μg/mL and 45.4 ± 11.1 μg/mL for α-amylase and α-glucosidase, respectively. A significantly positive correlation was identified between the secondary metabolites and antioxidant activities. The principal component analysis implies ethyl acetate and methanolic extracts as pivotal extracts of B. tinctoria.

References:

Afifi, T.O., Mather, A., Boman, J., Fleisher, W., Enns, M.W., MacMillan, H., Sareen, J., 2011. Childhood adversity and personality disorders: results from a nationally representative population-based study. J. Psychiatr. Res. 45(6), 814- 822.
Akpanyung, E., 2005. Proximate and mineral element composition of bouillon cubes produced in Nigeria. Pak. J. Nutr. 4(5), 327-329.
Alamgeer, Hasan, U.H., Uttra, A.M., Rasool, S., 2015. Evaluation of in vitro and in vivo anti-arthritic potential of Berberis calliobotrys. Bangladesh J. Pharmacol. 10(4), 807-819.
Alén-Ruiz, F., Pérez-Gregorio, M. R., Martínez-Carballo, E., García-Falcón, M. S., Simal-Gándara, J., 2008. Influence of polyphenols on color and antioxidant value in plant foods. Electron. J. Environ. Agric. Food Chem, 7, 3171-3176.
Ali, A., Deokule, S., 2009. Studies on nutritional values of some wild edible plants from Iran and India. Pak. J. Nutr. 8(1), 26-31.
Ali, H., Houghton, P., Soumyanath, A., 2006. α-Amylase inhibitory activity of some Malaysian plants used to treat diabetes; with particular reference to Phyllanthus amarus. J. Ethnopharmacol. 107(3), 449-455.
Amritpal, S., Sanjiv, D., Navpreet, K., Jaswinder, S., 2010. Berberine: alkaloid with wide spectrum of pharmacological activities. Indian J. Nat. Prod. Resour. 3, 64-75.
Andola, H.C., 2012. Genus Berberis and berberine HPLC: an overview. JBAPN. 2(5), 256-264.
AOAC., 2000. Official Methods of Analysis, 17th Ed. The Association of Official Analytical Chemists, Gaithersburg, MD, USA. Methods 925.10, 65.17, 974.24, 992.16.
Arango Duque, G., Descoteaux, A., 2014. Macrophage cytokines: involvement in immunity and infectious diseases. Front. Immunol. 5(491), 1-12.
Awan, M.S., Ali, S., Ali, A., Hussain, A., Ali, M., 2014. A comparative study of barberry fruits in terms of its nutritive and medicinal contents from CKNP region, Gilgit-Baltistan, Pakistan. J. Bio. Env. Sci. 5(2), 9-17.
Belwal, T., Dhyani, P., Bhatt, I.D., Rawal, R.S., Pande, V., 2016. Optimization extraction conditions for improving phenolic content and antioxidant activity in Berberis asiatica fruits using response surface methodology (RSM). Food Chem. 207, 115-124.
Benderitter, M., Maupoil, V., Vergely, C., Dalloz, F., Briot, F., Rochette, L., 1998. Studies by electron paramagnetic resonance of the importance of iron in the hydroxyl scavenging properties of ascorbic acid in plasma: effects of iron chelators. Fundam. Clin. Pharmacol. 12(5), 510-516.
Bhat, R., Paliyath, G., 2016. Fruits of tropical climates: Biodiversity and Dietary Importance, in: B, Caballero., P, Finglas., F, Tol-drá. (Eds.), Encyclopedia of Food and Health, Oxford: Academic Press (Elsevier), UK. pp. 138-144.
Bober, Z., Stępień, A., Aebisher, D., Ożóg, Ł., Bartusik-Aebisher, D., 2018. Fundamentals of the use of Berberis as a medicinal plant. Eur. J. Clin. Exp. Med. 1, 41-46.
Boudjelthia, K., Hammadi, K., Kouidri, M., Djebli, N., 2017. Evaluation of antidiabetic activity of two plants Berberis vulgaris and Zygophyllum geslini. J. Phys. Chem. Biophys. 7(1), 1-7.
Braca, A., De Tommasi, N., Di Bari, L., Pizza, C., Politi, M., Morelli, I., 2001. Antioxidant principles from Bauhinia tarapotensis. J. Nat. Prod. 64(7), 892-895.
Brand-Williams, W., Cuvelier, M.E., Berset, C.L.W.T., 1995. Use of a free radical method to evaluate antioxidant activity. LWT- Food Sci. Technol. 28(1), 25-30.
Cavarape, A., Feletto, F., Mercuri, F., Quagliaro, L., Damante, G., Ceriello, A., 2001. High-fructose diet decreases catalase mRNA levels in rat tissues. J. Endocrinol. Invest. 24(11), 838-845.
Cencic, A., Chingwaru, W., 2010. The role of functional foods, nutraceuticals, and food supplements in intestinal health. Nutrients 2(6), 611-625.
Chen, L., Deng, H., Cui, H., Fang, J., Zuo, Z., Deng, J., Li, Y., Wang, X., Zhao, L., 2018. Inflammatory responses and inflammation-associated diseases in organs. Oncotarget. 9(6), 7204-7218.
Dinis, T.C., Madeira, V.M., Almeida, L.M., 1994. Action of phenolic derivatives (acetaminophen, salicylate, and 5-aminosalicylate) as inhibitors of membrane lipid peroxidation and as peroxyl radical scavengers. Arch. Biochem. Biophys. 315(1), 161-169.
Doss, A., 2009. Preliminary phytochemical screening of some Indian medicinal plants. Anc. Sci. Life. 29(2), 12-16.
Duh, P.D., Tu, Y.Y., Yen, G.C., 1999. Antioxidant activity of water extract of Harng Jyur (Chrysanthemum morifolium Ramat). LWT - Food Sci. Technol. 32(5), 269-277.
Dulić, M., Ciganović, P., Vujić, L., Zovko Končić, M., 2019. Antidiabetic and cosmeceutical potential of common Barbery (Berberis vulgaris L.) root bark extracts obtained by optimization of ‘Green’ ultrasound-assisted extraction. Molecules 24(19),1-17.
Farmani, F., Moein, M., Khoshnood, M.J., Sabahi, Z., 2018. Anthocyanin isolation from Berberis integerrima Bunge. fruits and determination of their antioxidant activity. Free Radic. Antioxid. 8(1), 1-5.
Fernández-Poyatos, M.D.P., Ruiz-Medina, A., Zengin, G., Llorent-Martínez, E.J., 2019. Phenolic characterization, antioxidant activity, and enzyme inhibitory properties of Berberis thunbergii DC. leaves: A valuable source of phenolic acids. Molecules 24(22), 4171.
Francis, G., Kerem, Z., Makkar, H.P., Becker, K., 2002. The biological action of saponins in animal systems: a review. Br. J. Nutr. 88(6), 587-605.
Fyson, P.F., 1974. The Flora of the Nilgiris and Pulney Hill Tops, in: Bishen Singh and Mahendra Pal Singh, vol. 1, 1st Ed, Dehradun, India.
Gudise, V., Chowdhury, B., Manjappa, A.S., 2019. In vitro free radical scavenging and antidiabetic activity of aqueous and ethanolic leaf extracts: a comparative evaluation of Argyreia pierreana and Matelea denticulata. Futur J. Pharm. Sci. 5(13), 1-11.
Gurib-Fakim, A., 2006. Medicinal plants: traditions of yesterday and drugs of tomorrow. Mol. Asp. Med. 27(1), 1-93.
Hagerman, A. E., Riedl, K. M., Jones, G. A., Sovik, K. N., Ritchard, N. T., Hartzfeld, P. W., Riechel, T. L., 1998. High molecular weight plant polyphenolics (tannins) as biological antioxidants. J. Agric. Food Chem. 46(5), 1887-1892.
Hanachi, P., Golkho, S., 2009. Using HPLC to determination the composition and antioxidant activity of Berberis vulgaris. Eur. J. Res. 29(1), 47-54.
Hara, Y., Honda, M., 1990. The inhibition of α-amylase by tea polyphenols. Agr. Biol. Chem. 54(8), 1939-1945.
Hinz, H., Zenk, M., 1981. Production of protoberberine alkaloids by cell suspension cultures of Berberis species. Naturwissenschaften 68(12), 620-621.
Hodge, J., 1962. Determination of Reducing Sugars And Carbohydrates. Methods in Carbohydrate Chemistry. Vol. 1, 380-394.
Hyun, T.K., Kim, H.C., Kim, J.S., 2015. In vitro screening for antioxidant, antimicrobial, and antidiabetic properties of some Korean native plants on Mt. Halla, Jeju Island. Indian J. Pharm. Sci. 77(6), 668-674.
Jayasri, M., Lazar, M., Radha, A., 2009. A report on the antioxidant activity of leaves and rhizomes of Costus pictus D. Don. Int. J. Integr. Biol. 5(1), 20-26.
Kaur, S., Syed Ali, M., Anuradha, V., Suganya, V., Ashashalini, A., Bhuvana, P., 2018. In vitro anti-inflammatory activity of mangrove plant Rhizophora mucronata Lam. (Malpighiales: Rhizophoraceae). Brazilian J. Biol. Sci. 5(10), 417-426.
Kazeem, M.I., Adamson, J.O., Ogunwande, I.A., 2013. Modes of inhibition of α-amylase and α-glucosidase by aqueous extract of Morinda lucida Benth. leaf. BioMed Res. Int. 2013, 1-6.
Kim, G.N., Shin, J.G., Jang, H.D., 2009. Antioxidant and antidiabetic activity of Dangyuja (Citrus grandis Osbeck) extract treated with Aspergillus saitoi. Food Chem. 117(1), 35-41.
Kirtikar, K., Basu, B., 1995. Indian Medicinal Plants. International Book Distributors Vol. 1, Dehradun, India. pp. 371-372.
Lamichhane, B., Adhikari, S., Shrestha, P., Shrestha, B.G., 2014. Study of phytochemical, antioxidant, antimicrobial and anticancer activity of Berberis aristata. J. Trop. Life Sci. 4(1), 01-07.
Latha, R., Sagaya Jansi, R., Agastian, P., 2015. Physicochemical and phytochemical investigation on medicinal plants used by ethnic tribes of Nilgiri Mountains, South India. World J. Pharm. Sci. 3(3), 632-644.
Li, Z., Geng, Y.N., Jiang, J.D., Kong, W.J., 2014. Antioxidant and anti-inflammatory activities of berberine in the treatment of diabetes mellitus. J. Evid. Based Complementary Altern. Med. 2014, 1-12.
Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J., 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem.193, 265-275.
Makkar, H., Francis, G., Becker, K., 2007. Bioactivity of phytochemicals in some lesser-known plants and their effects and potential applications in livestock and aquaculture production systems. Animal 1(9), 1371-1391.
Makkar, H.P., 2003. Quantification of Tannins in Tree and Shrub Foliage: A Laboratory Manual. Springer, Dordrecht, Netherlands.
Marchetti, P., Del Prato, S., Lupi, R., Del Guerra, S., 2006. The pancreatic beta-cell in human Type 2 diabetes. Nutr. Metab. Cardiovasc. Dis. 16, S3- S6.
Markert, B., 1994. Plants as Biomonitors- Potential Advantages and Problems, in: D.C. Adriano, Z.S. Chen and S.S. Yang (Ed), Biogeochemistry of Trace Elements. Science and Technology Letters. Northwood, New York, pp. 601-613.
Matarredona, L., Camacho, M., Zafrilla, B., Bonete, M. J., Esclapez, J., 2020. The role of stress proteins in haloarchaea and their adaptive response to environmental shifts. Biomolecules 10(10), 1390.
Miller, G.L., 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31(3), 426-428.
Miller, N.J., Rice-Evans, C.A., 1997. Factors influencing the antioxidant activity determined by the ABTS•+ radical cation assay. Free Radic. Res. 26(3), 195-199.
Moore, S., Stein, W.H., 1948. Photometric nin-hydrin method for use in the ehromatography of amino acids. J. Biol. Chem. 176, 367-388.
Motalleb, G., Hanachi, P., Kua, S., Fauziah, O., Asmah, R., 2005. Evaluation of phenolic content and total antioxidant activity in Berberis vulgaris fruit extract. J. Biol. Sci. 5(5), 648-653.
Murugesh, K., Yeligar, V.C., Dash, D.K., Maiti, B., Maity, T.K., 2006. Effect of Berberis tinctoria leaf (Berberidaceae) extract on antidiabetic, antihyperlipidemic and antioxidant status in streptozotocin induced diabetes in rats. Orient. Pharm. Exp. Med. 6(4), 336-343.
Nithiyanantham, S., Selvakumar, S., Siddhuraju, P., 2012. Total phenolic content and antioxidant activity of two different solvent extracts from raw and processed legumes, Cicer arietinum L. and Pisum sativum L. J. Food Compos. Anal. 27(1), 52-60.
Ogurtsova, K., da Rocha Fernandes, J., Huang, Y., Linnenkamp, U., Guariguata, L., Cho, N.H., Cavan, D., Shaw, J., Makaroff, L., 2017. IDF diabetes atlas: Global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res. Clin. Pract. 128, 40-50.
Paredes-López, O., Cervantes-Ceja, M.L., Vigna-Pérez, M., Hernández-Pérez, T., 2010. Berries: improving human health and healthy aging, and promoting quality life- a review. Plant Foods Hum. Nutr. 65(3), 299-308.
Pham-Huy, L.A., He, H., Pham-Huy, C., 2008. Free radicals, antioxidants in disease and health. Int. J. Biomed. Sci. 4(2), 89-96.
Podsedek, A., Majewska, I., Redzynia, M., Sosnowska, D., Koziołkiewicz, M., 2014. In vitro inhibitory effect on digestive enzymes and antioxidant potential of commonly consumed fruits. J. Agric. Food Chem. 62(20), 4610-4617.
Prieto, P., Pineda, M., Aguilar, M., 1999. Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal. Biochem. 269(2), 337-341.
Prior, R.L., Wu, X., Schaich, K., 2005. Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J. Agric. Food Chem. 53(8), 3101-3113.
Pulido, R., Bravo, L., Saura-Calixto, F., 2000. Antioxidant activity of dietary polyphenols as determined by a modified ferric reducing/antioxidant power assay. J. Agric. Food Chem. 48(8), 3396-3402.
Raffauf, R.F., 1996. Plant Alkaloids: A Guide to Their Discovery and Distribution. Food Products Press, Northeastern University, Boston, Massachusetts, USA.
Rana, Z.H., Alam, M.K., Akhtaruzzaman, M., 2019. Nutritional composition, total phenolic content, antioxidant and α-amylase inhibitory activities of different fractions of selected wild edible plants. Antioxidants 8(7), 203.
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(9-10), 1231-1237.
Ricciotti, E., FitzGerald, G.A., 2011. Prostaglandins and inflammation. Arterioscler. Thromb. Vasc. Biol. 31(5), 986-1000.
Rivero-Cruz, J.F., Granados-Pineda, J., Pedraza-Chaverri, J., Pérez-Rojas, J.M., Kumar-Passari, A., Diaz-Ruiz, G., Rivero-Cruz, B.E., 2020. Phytochemical constituents, antioxidant, cytotoxic, and antimicrobial activities of the ethanolic extract of Mexican brown propolis. Antioxidants 9(1), 70.
Sadasivam, S., Manickam, A., 2008. Biochemical methods, 3rd Ed, New Age International Publishers, New Delhi, India.
Sampson, S., Bucris, E., Horovitz-Fried, M., Parnas, A., Kahana, S., Abitbol, G., Chetboun, M., Rosenzweig, T., Brodie, C., Frankel, S., 2010. Insulin increases H2O2-induced pancreatic beta cell death. Apoptosis 15(10), 1165-1176.
Sasikumar, J., Maheshu, V., Smilin, A., Gincy, M., Joji, C., 2012. Antioxidant and antihemolytic activities of common Nilgiri barberry (Berberis tinctoria Lesch.) from south India. Int. Food Res. 19(4), 1601-1607.
Shah, H., Shad, A.A., Perveen, S., Khattak, S., Khanzadi Fatima Khattak, 2003. Physiochemical Composition of Wild Medicinal Plant Berberis lycium. J. Appl. Sci. 3, 370-375.
Shahidi, F., Ambigaipalan, P., 2015. Phenolics and polyphenolics in foods, beverages and spices: Antioxidant activity and health effects-A review. J. Funct. Foods 18(B), 820-897.
Shenoy, R.S., Prashanth, K., Manonmani, H., 2018. In vitro antidiabetic effects of isolated triterpene glycoside fraction from Gymnema sylvestre. Evid.-Based Complementary Altern. Med. 2018, 1-12.
Shigwan, H., Saklani, A., Hamrapurkar, P.D., Mane, T., Bhatt, P., 2013. HPLC method development and validation for quantification of berberine from Berberis aristata and Berberis tinctoria. Int. J. Appl. Sci. Eng. 2, 203-211.
Siddhuraju, P., Vijayakumari, K., Janardhanan, K., 1996. Chemical composition and protein quality of the little-known legume, velvet bean (Mucuna pruriens (L.) DC.). J. Agric. Food Chem. 44(9), 2636-2641.
Singh, D.K., Srivastava, B., Sahu, A., 2004. Spectrophotometric Determination of Rauwolfia Alkaloids: Estimation of Reserpine in Pharmaceuticals. Anal Sci. 20(3), 571-573.
Soare, J.R., Dinis, T.C., Cunha, A.P., Almeida, L., 1997. Antioxidant activities of some extracts of Thymus zygis. Free Radic. Res. 26(5), 469-478.
Sodipo, O., Akinniyi, J.A., Ogunbameru, J., 2000. Studies on certain characteristics of the extracts of bark of Pausinystalia johimbe and Pausinystalia macroceras (K Schum) Pierre ex Beille. Global J. Pure Appl. Sci. 6(1), 83-88.
Sood, P., Modgil, R., Sood, M., 2010. Physico-chemical and nutritional evaluation of indigenous wild fruit Kasmal, Berberis lycium Royle. Indian J. Nat. Prod. Resour. 1(3), 362-366.
Srivastava, S. K., Rai, V., Srivastava, M., Rawat, A. K. S., Mehrotra, S., 2006. Estimation of heavy metals in different Berberis species and its market samples. Environ. Monit. Assess. 116(1), 315-320.
Srivastava, S., Srivastava, M., Misra, A., Pandey, G., Rawat, A., 2015. A review on biological and chemical diversity in Berberis (Berberidaceae). EXCLI. J. 14, 247-267.
Srivastava, S.K., Rawat, A.K.S., 2007. Pharmacognostic evaluation of the roots of Berberis tinctoria Lesch. Nat. Prod. Sci. 13(1), 27-32.
Tabeshpour, J., Imenshahidi, M., Hosseinzadeh, H., 2017. A review of the effects of Berberis vulgaris and its major component, berberine , in metabolic syndrome. Iran J. Basic Med. Sci. 20(5), 557-568.
Tacon, A., Ferns, P., 1979. Activated sewage sludge, a potential animal foodstuff I. Proximate and mineral content: seasonal variation. J. Agri. Envi. 4(4), 257-269.
Tan, B.L., Norhaizan, M.E., Liew, W.P.P., Sulaiman Rahman, H., 2018. Antioxidant and oxidative stress: a mutual interplay in age-related diseases. Front. pharmacol. 9(1162), 1-28.
Upwar, N., Patel, R., Waseem, N., Mahobia, N.K., 2011. Hypoglycemic effect of methanolic extract of Berberis aristata DC stem on normal and streptozotocin induced diabetic rats. Int. J. Pharm. Pharm. Sci. 3(1), 222-224.
Van den Berg, R.A., Hoefsloot, H.C., Westerhuis, J.A., Smilde, A.K., van der Werf, M.J., 2006. Centering, scaling, and transformations: improving the biological information content of metabolomics data. BMC Genom. 7(1), 142.
Vasarri, M., Leri, M., Barletta, E., Ramazzotti, M., Marzocchini, R., Degl''Innocenti, D., 2020. Anti-inflammatory properties of the marine plant Posidonia oceanica (L.) Delile. J. Ethnopharmacol. 247, 112252.
Wang, S.Y., Lin, H.S., 2000. Antioxidant activity in fruits and leaves of blackberry, raspberry, and strawberry varies with cultivar and developmental stage. J. Agric. Food Chem. 48(2), 140-146.
Weston, R., Gore Jr, P.A., 2006. A brief guide to structural equation modeling. Couns. Psychol. 34(5), 719-751.
Yamamoto, H., Fujimori, T., Sato, H., Ishikawa, G., Kami, K., Ohashi, Y., 2014. Statistical hypothesis testing of factor loading in principal component analysis and its application to metabolite set enrichment analysis. BMC bioinformatics 15(1), 51.
Zee-Cheng, R.Y., 1997. Anticancer research on Loranthaceae plants. Drugs Future 22(5), 519-530.
Zhuang, X., Lu, Y., Yang, G., 1992. Extraction and determination of flavonoid in ginkgo. Chin. Herb. Med. 23, 122-124.