Skip to main content
SpringerLink
Log in

Chemical composition, antioxidant, anticholinesterase, and alpha-glucosidase activity of Stevia rebaudiana Bertoni extracts cultivated in Algeria

  • Original Paper
  • Published:
Journal of Food Measurement and Characterization Aims and scope Submit manuscript

Abstract

Stevia rebaudiana Bertoni is an endemic species to Paraguay famous for its sweetening power and therapeutic potential for various diseases such as diabetes. The present work evaluates the chemical composition and antioxidant, anticholinesterase, and α-glucosidase activities of S. rebaudiana. The essential oil (EO) of dry Stevia leaves was analyzed by GC/MS and detected the presence of 33 components. Caryophyllene oxide (24.28%), spathulenol (12.31%) and nerolidol (11.8%), and manool oxide (7.36%) were identified as the major ones. The antioxidant activity was evaluated by four complementary methods: DPPH (2,2 diphenylpicrylhydrazyl, ABTS (2, 2’-azino-bis 3-ethylbenzthiazoline-6-sulfonic acid) free radicals scavenging, Cupric reducing antioxidant capacity (CUPRAC), and reducing power. The crude methanolic extract and its fractions showed a variable antioxidant activity and strongly correlated with the content of quantified bioactive compounds. The ethyl acetate fraction showed a very high antioxidant activity close to the tested standards, while EO was active only in the CUPRAC assy. The petrol ether and chloroform fractions showed the best butyrylcholinesterase (BChE) inhibitory activity with IC50 values: 123.7 ± 1.78 and 170.1 ± 0.78 μg/mL, respectively. On the other hand, EO and chloroform revealed a moderate inhibitory activity against acetylcholinesterase (AChE). The in vitro inhibitory effect of the extracts on α-glucosidase indicated that EO effectively inhibited the enzyme with an IC50: 74.9 ± 6.4 µg/mL, better than the standard acarbose. The EO of Stevia has a significant anti-diabetic potential.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. W. Mamache, S. Amira, C. Ben Souici, H. Laouer, F. Benchikh, In vitro antioxidant, anticholinesterases, anti α-amylase, and anti α-glucosidase effects of Algerian Salvia aegyptiaca and Salvia verbenaca. J. Food Biochem. (2020). https://doi.org/10.1111/jfbc.13472

    Article  PubMed  Google Scholar 

  2. L. Gali, F. Bedjou, Antioxidant and anticholinesterase effects of the ethanol extract, ethanol extract fractions and total alkaloids from the cultivated Ruta chalepensis. South Afr. J. Bot. 120, 163–169 (2019). https://doi.org/10.1016/j.sajb.2018.04.011

    Article  CAS  Google Scholar 

  3. S. Darvesh, D.A. Hopkins, C. Geula, Neurobiology of butyrylcholinesterase. Nat. Rev. Neurosci. 4(2), 131–138 (2003). https://doi.org/10.1038/nrn1035

    Article  CAS  PubMed  Google Scholar 

  4. A. Ibrahim et al., In vitro antioxidant and anti-diabetic potential of gymnema sylvestre methanol leaf extract. Eur. Sci. J. ESJ 13(36), 218 (2017). https://doi.org/10.19044/esj.2017.v13n36p218

    Article  Google Scholar 

  5. M. Mehta, A. Adem, M. Sabbagh, New acetylcholinesterase inhibitors for alzheimer’s disease. Int. J. Alzheimers Dis. 2012, 1–8 (2012). https://doi.org/10.1155/2012/728983

    Article  CAS  Google Scholar 

  6. R.C. Fierascu, I. Fierascu, A. Ortan, M.I. Georgiev, E. Sieniawska, Innovative approaches for recovery of phytoconstituents from medicinal/aromatic plants and biotechnological production. Molecules 25(2), 309 (2020). https://doi.org/10.3390/molecules25020309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. L.G. Sarmiento-López, M. López-Meyer, G. Sepúlveda-Jiménez, L. Cárdenas, M. Rodríguez-Monroy, Arbuscular mycorrhizal symbiosis in Stevia rebaudiana increases trichome development, flavonoid and phenolic compound accumulation. Biocatal. Agric. Biotechnol. 31, 101889 (2021). https://doi.org/10.1016/j.bcab.2020.101889

    Article  CAS  Google Scholar 

  8. R.P. Pereira et al., Antioxidant effects of different extracts from Melissa officinalis, Matricaria recutita and Cymbopogon citratus. Neurochem. Res. 34(5), 973–983 (2009). https://doi.org/10.1007/s11064-008-9861-z

    Article  CAS  PubMed  Google Scholar 

  9. R. Lemus-Mondaca et al., Antioxidant, antimicrobial and anti-inflammatory potential of Stevia rebaudiana leaves: effect of different drying methods. J. Appl. Res. Med. Aromat. Plants 11, 37–46 (2018). https://doi.org/10.1016/j.jarmap.2018.10.003

    Article  Google Scholar 

  10. M.F. Hossain, M.T. Islam, M.A. Islam, S. Akhtar, Cultivation and uses of stevia (Stevia rebaudiana bertoni): A review. Afr. J. FOOD Agric. Nutr. Dev. 17(4), 12745–12757 (2017). https://doi.org/10.18697/ajfand.80.16595

    Article  CAS  Google Scholar 

  11. R. Lemus-Mondaca, A. Vega-Gálvez, L. Zura-Bravo, K. Ah-Hen, Stevia rebaudiana Bertoni, source of a high-potency natural sweetener: A comprehensive review on the biochemical, nutritional and functional aspects. Food Chem. 132(3), 1121–1132 (2012). https://doi.org/10.1016/j.foodchem.2011.11.140

    Article  CAS  PubMed  Google Scholar 

  12. N. Ilias, H. Hamzah, I.S. Ismail, T.B. Mohd, M. Mohidin, F. Idris, M. Ajat, An insight on the future therapeutic application potential of Stevia rebaudiana Bertoni for atherosclerosis and cardiovascular diseases. Biomed. Pharmacother. 143, 112207 (2021). https://doi.org/10.1016/j.biopha.2021.112207

    Article  CAS  PubMed  Google Scholar 

  13. D. Bursać Kovačević et al., Innovative technologies for the recovery of phytochemicals from Stevia rebaudiana Bertoni leaves: a review. Food Chem. 268, 513–521 (2018). https://doi.org/10.1016/j.foodchem.2018.06.091

    Article  CAS  PubMed  Google Scholar 

  14. K. Gaweł-Bęben et al., Stevia Rebaudiana Bert. leaf extracts as a multifunctional source of natural antioxidants. Molecules 20(4), 5468–5486 (2015). https://doi.org/10.3390/molecules20045468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. J. Ahmad, I. Khan, R. Blundell, J. Azzopardi, M.F. Mahomoodally, Stevia rebaudiana Bertoni.: an updated review of its health benefits, industrial applications and safety. Trends Food Sci. Technol. 100, 177–189 (2020). https://doi.org/10.1016/j.tifs.2020.04.030

    Article  CAS  Google Scholar 

  16. G. Benelli, R. Pavela, E. Drenaggi, N. Desneux, F. Maggi, Phytol (E)-nerolidol and spathulenol from Stevia rebaudiana leaf essential oil as effective and eco-friendly botanical insecticides against Metopolophium dirhodum. Ind. Crops Prod. 155, 112844 (2020). https://doi.org/10.1016/j.indcrop.2020.112844

    Article  CAS  Google Scholar 

  17. A.B. Siddique, S.M. Mizanur Rahman, M.A. Hossain, Chemical composition of essential oil by different extraction methods and fatty acid analysis of the leaves of Stevia Rebaudiana Bertoni. Arab. J. Chem. 9, S1185–S1189 (2016). https://doi.org/10.1016/j.arabjc.2012.01.004

    Article  CAS  Google Scholar 

  18. T.S. Mann et al., In vitro cytotoxic activity guided essential oil composition of flowering twigs of Stevia rebaudiana. Nat. Prod. Commun. 9(5), 1934X1400900 (2014). https://doi.org/10.1177/1934578X1400900535

    Article  Google Scholar 

  19. Y.A. Turko et al., GC—MS research. I. essential oil from Stevia rebaudiana. Chem. Nat. Compd. 43(6), 744–745 (2007). https://doi.org/10.1007/s10600-007-0254-3

    Article  CAS  Google Scholar 

  20. F.N. Muanda, R. Soulimani, B. Diop, A. Dicko, Study on chemical composition and biological activities of essential oil and extracts from Stevia rebaudiana Bertoni leaves. LWT Food Sci. Technol. 44(9), 1865–1872 (2011). https://doi.org/10.1016/j.lwt.2010.12.002

    Article  CAS  Google Scholar 

  21. V.I. Babushok, P.J. Linstrom, I.G. Zenkevich, Retention indices for frequently reported compounds of plant essential oils. J. Phys. Chem. Ref. Data. 40(4), 043101 (2011). https://doi.org/10.1063/1.3653552

    Article  CAS  Google Scholar 

  22. V.L. Singleton, J.A. Rossi, Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 16(3), 144–158 (1965)

    Article  CAS  Google Scholar 

  23. G. Topçu, M. Ay, A. Bilici, C. Sarıkürkcü, M. Öztürk, A. Ulubelen, A new flavone from antioxidant extracts of Pistacia terebinthus. Food Chem. 103(3), 816–822 (2007). https://doi.org/10.1016/j.foodchem.2006.09.028

    Article  CAS  Google Scholar 

  24. A. Kumaran, R. Joel Karunakaran, In vitro antioxidant activities of methanol extracts of five Phyllanthus species from India. LWT Food Sci. Technol. 40(2), 344–352 (2007). https://doi.org/10.1016/j.lwt.2005.09.011

    Article  CAS  Google Scholar 

  25. M.S. Blois, Antioxidant determinations by the use of a stable free radical. Nature 181(4617), 1199–1200 (1958)

    Article  CAS  Google Scholar 

  26. R. Re, N. Pellegrini, A. Proteggente, A. Pannala, M. Yang, C. Rice-Evans, Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 26(9–10), 1231–1237 (1999). https://doi.org/10.1016/S0891-5849(98)00315-3

    Article  CAS  PubMed  Google Scholar 

  27. M. Oyaizu, Studies on products of browning reaction. Jpn. J. Nutr. Diet. 44(6), 307–315 (1986). https://doi.org/10.5264/eiyogakuzashi.44.307

    Article  CAS  Google Scholar 

  28. R. Apak, K. Güçlü, M. Özyürek, S.E. Karademir, Novel total antioxidant capacity index for dietary polyphenols and vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. J. Agric. Food Chem. 52(26), 7970–7981 (2004). https://doi.org/10.1021/jf048741x

    Article  CAS  PubMed  Google Scholar 

  29. G.L. Ellman, K.D. Courtney, V. Andres, R.M. Featherstone, A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7(2), 88–95 (1961). https://doi.org/10.1016/0006-2952(61)90145-9

    Article  CAS  PubMed  Google Scholar 

  30. S. Lordan, T.J. Smyth, A. Soler-Vila, C. Stanton, R.P. Ross, The α-amylase and α-glucosidase inhibitory effects of Irish seaweed extracts. Food Chem. 141(3), 2170–2176 (2013). https://doi.org/10.1016/j.foodchem.2013.04.123

    Article  CAS  PubMed  Google Scholar 

  31. A. Martelli, C. Frattini, F. Chialva, Unusual essential oils with aromatic properties—I. Volatile components of Stevia rebaudiana bertoni. Flavour Fragr. J. 1(1), 3–7 (1985). https://doi.org/10.1002/ffj.2730010103

    Article  CAS  Google Scholar 

  32. K. Fidyt, A. Fiedorowicz, L. Strządała, A. Szumny, β -caryophyllene and β -caryophyllene oxide-natural compounds of anticancer and analgesic properties. Cancer Med. 5(10), 3007–3017 (2016). https://doi.org/10.1002/cam4.816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. D. Fiorini, A. Molle, M. Nabissi, G. Santini, G. Benelli, F. Maggi, Valorizing industrial hemp (Cannabis sativa L.) by-products: Cannabidiol enrichment in the inflorescence essential oil optimizing sample pre-treatment prior to distillation. Ind. Crops Prod. 128, 581–589 (2019). https://doi.org/10.1016/j.indcrop.2018.10.045

    Article  CAS  Google Scholar 

  34. K.F. do Nascimento et al., Antioxidant, anti-inflammatory, antiproliferative and antimycobacterial activities of the essential oil of Psidium guineense Sw. and spathulenol. J. Ethnopharmacol. 210, 351–358 (2018). https://doi.org/10.1016/j.jep.2017.08.030

    Article  CAS  PubMed  Google Scholar 

  35. S. Dall’Acqua et al., Phytochemical investigations and antiproliferative secondary metabolites from Thymus alternans growing in Slovakia. Pharm. Biol. 55(1), 1162–1170 (2017). https://doi.org/10.1080/13880209.2017.1291689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. J.R. Medina-Medrano, J.E. Torres-Contreras, J.I. Valiente-Banuet, M.D. Mares-Quiñones, M. Vázquez-Sánchez, D. Álvarez-Bernal, Effect of the solid–liquid extraction solvent on the phenolic content and antioxidant activity of three species of Stevia leaves. Sep. Sci. Technol. 54(14), 2283–2293 (2019). https://doi.org/10.1080/01496395.2018.1546741

    Article  CAS  Google Scholar 

  37. Addai ZR, Abdullah A, Mutalib SA, Effect of extraction solvents on the phenolic content and antioxidant properties of two papaya cultivars. J. Med. Plants Res. 7, 3354–3359 (2013)

  38. U.H. Zaidan, N.I. Mohamad Zen, N.A. Amran, S. Shamsi, S.S.A. Gani, Biochemical evaluation of phenolic compounds and steviol glycoside from Stevia rebaudiana extracts associated with in vitro antidiabetic potential. Biocatal. Agric. Biotechnol. 18, 101049 (2019). https://doi.org/10.1016/j.bcab.2019.101049

    Article  Google Scholar 

  39. R. Lemus-Mondaca, K. Ah-Hen, A. Vega-Gálvez, C. Honores, N.O. Moraga, Stevia rebaudiana leaves: effect of drying process temperature on bioactive components, antioxidant capacity and natural sweeteners. Plant Foods Hum. Nutr. 71(1), 49–56 (2016). https://doi.org/10.1007/s11130-015-0524-3

    Article  CAS  PubMed  Google Scholar 

  40. F. Al-rimawi, S. Abu-lafi, J. Abbadi, A.A.A. Alamarneh, R.A. Sawahreh, I. Odeh, Analysis of phenolic and flavonoids of wild ephedra alata plant extracts by LC/PDA and LC/MS and their antioxidant activity. Afr. J. Tradit. Complement. Altern. Med. 14(2), 130–141 (2017). https://doi.org/10.21010/ajtcam.v14i2.14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. J. Bose, A. Rodrigo-Moreno, S. Shabala, ROS homeostasis in halophytes in the context of salinity stress tolerance. J. Exp. Bot. 65(5), 1241–1257 (2014). https://doi.org/10.1093/jxb/ert430

    Article  CAS  PubMed  Google Scholar 

  42. F.S. Ait Chaouche, F. Mouhouche, M. Hazzit, Antioxidant capacity and total phenol and flavonoid contents of Teucrium polium L. grown in Algeria. Mediterr. J. Nutr. Metab. 11(2), 135–144 (2018). https://doi.org/10.3233/MNM-17189

    Article  Google Scholar 

  43. A. Moongngarm, N. Sriharboot, P. Loypimai, T. Moontree, Ohmic heating-assisted water extraction of steviol glycosides and phytochemicals from Stevia rebaudiana leaves. LWT 154, 112798 (2022). https://doi.org/10.1016/j.lwt.2021.112798

    Article  CAS  Google Scholar 

  44. H. Chouit, O. Touafek, M. Brada, C. Benssouici, M.L. Fauconnier, M. El Hattab, GC-MS analysis and biological activities of Algerian Salvia microphylla essential oils. J. Chem. Soc. Mex. (2021). https://doi.org/10.29356/jmcs.v65i4.1581

    Article  Google Scholar 

  45. C. Bensouici et al., Chemical characterization, antioxidant, anticholinesterase and alpha-glucosidase potentials of essential oil of Rosmarinus tournefortii de noé. J. Food Meas. Charact. 14(2), 632–639 (2020). https://doi.org/10.1007/s11694-019-00309-y

    Article  Google Scholar 

  46. M. Hazzit, A. Baaliouamer, M.L. Faleiro, M.G. Miguel, Composition of the essential oils of Thymus and Origanum species from Algeria and their antioxidant and antimicrobial activities. J. Agric. Food Chem. 54(17), 6314–6321 (2006). https://doi.org/10.1021/jf0606104

    Article  CAS  PubMed  Google Scholar 

  47. I. Achili et al., Chemical constituents, antioxidant, anticholinesterase and antiproliferative effects of Algerian Pistacia atlantica Desf. extracts. Recent Pat. Food Nutr. Agric. 11(3), 249–256 (2020). https://doi.org/10.2174/2212798411666200207101502

    Article  CAS  PubMed  Google Scholar 

  48. B. Asghari, G. Zengin, M.B. Bahadori, M. Abbas-Mohammadi, L. Dinparast, Amylase, glucosidase, tyrosinase, and cholinesterases inhibitory, antioxidant effects, and GC-MS analysis of wild mint (Mentha longifolia var. calliantha) essential oil: A natural remedy. Eur. J. Integr. Med. 22, 44–49 (2018). https://doi.org/10.1016/j.eujim.2018.08.004

    Article  Google Scholar 

  49. American Diabetes Association, Diagnosis and classification of diabetes mellitus. Diabetes Care 37(Supplement_1), 8S81-S90 (2014). https://doi.org/10.2337/dc14-S081

    Article  Google Scholar 

  50. K. zar Myint et al., Polyphenols from Stevia rebaudiana (Bertoni) leaves and their functional properties. J. Food Sci. 85(2), 240–248 (2020). https://doi.org/10.1111/1750-3841.15017

    Article  CAS  Google Scholar 

  51. C. Lankatillake, T. Huynh, D.A. Dias, Understanding glycaemic control and current approaches for screening antidiabetic natural products from evidence-based medicinal plants. Plant Methods 15(1), 105 (2019). https://doi.org/10.1186/s13007-019-0487-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. H. Bischoff, The mechanism of alpha-glucosidase inhibition in the management of diabetes. Clin. Investig. Med. Med. Clin. Exp. 18(4), 303–311 (1995)

    CAS  Google Scholar 

  53. J.C. Ruiz-Ruiz, Y.B. Moguel-Ordoñez, A.J. Matus-Basto, M.R. Segura-Campos, Antidiabetic and antioxidant activity of Stevia rebaudiana extracts (Var. Morita) and their incorporation into a potential functional bread. J. Food Sci. Technol. 52(12), 7894–7903 (2015). https://doi.org/10.1007/s13197-015-1883-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. G.R.M. Perez, S.M.A. Zavala, G.S. Perez, G.C. Perez, Antidiabetic effect of compounds isolated from plants. Phytomedicine 5(1), 55–75 (1998). https://doi.org/10.1016/S0944-7113(98)80060-3

    Article  CAS  Google Scholar 

Download references

Funding

This research was funded by the Algerian Ministry of Higher Education through the scholarship (35/PNE/PHD/BELGIUM/2019-2020) granted to Lremizi Imane to finalize her Ph.D. thesis.

Author information

Authors and Affiliations

  1. Laboratory of Food Quality and Food Safety, Department of Agronomic Sciences, Mouloud-Mammeri University, BP 17, 15000, Tizi-Ouzou, Algeria

    Imane Lremizi

  2. Natural Resources Valorization and Bioengeering Laboratory – University Benyoucef Benkhedda Algiers 1, Algiers, Algeria

    Abdenour Ait Ouazzou

  3. Biotechnology Research Center (CRBT), Ali Mendjli New Town UV 03, BP E73, Constantine, Algeria

    Chawki Bensouici

  4. Laboratory of Chemistry of Natural Molecules, Gembloux Agro-Bio Tech, University of Liège, Passage of Deportees 2, 5030, Gembloux, Belgium

    Marie-Laure Fauconnier

Authors
  1. Imane Lremizi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Abdenour Ait Ouazzou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chawki Bensouici
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marie-Laure Fauconnier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abdenour Ait Ouazzou.

Ethics declarations

Conflict of interest

No potential conflict of interest was reported by the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lremizi, I., Ait Ouazzou, A., Bensouici, C. et al. Chemical composition, antioxidant, anticholinesterase, and alpha-glucosidase activity of Stevia rebaudiana Bertoni extracts cultivated in Algeria. Food Measure 17, 2639–2650 (2023). https://doi.org/10.1007/s11694-022-01704-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11694-022-01704-8

Keywords

Search

Navigation