Skip to main content
Log in

Artichoke (Cynara scolymus L.) Fruits and Leaves at Different Maturity Stages can Inhibit Digestive Enzymes and Formation of Advanced Glycation End-Products (AGEs)

  • Original Paper
  • Published:
Waste and Biomass Valorization Aims and scope Submit manuscript

Abstract

Artichoke has long been served as medicinal plant in Mediterranean area and central Asia. But very few information about their function on inhibiting the digestive enzyme and AGEs formation can be found. In order to expand the health benefit of the artichoke planted in Taiwan, we investigate the inhibitory activities of its fruits and leaves at different maturity stages on lipase, α-amylase, α-glucosidase and AGEs formation. Results showed that, young leaf (YL) exhibited the best inhibition of all the digestive enzymes and AGEs formation. For example, the IC50 of lipase and AGEs formation was 28.53 µg/µL and 7.09 µg/µL, respectively. The HPLC and PCA analysis further revealed that samples were clearly separated based on fruits and leaves maturity stages (a total variance of 91%). The major contribution factor is AGEs inhibition (F = 1156.30) followed by α-amylase inhibition (F = 292.66) and DPPH scavenging (F = 203.53). Among the phenolics, the amount of chlorogenic acid and Ethyl-3,4-dihydroxybenzoate were the most abundant, and account for 87.90% and 5.78%, respectively. The high correlation between these compounds and the inhibition of digestive enzymes and AGEs formation, indicating that fruits and leaves of artichoke planted in Taiwan can be a potential material of anti-diabetic and anti-obesity health supplements.

Graphical Abstract

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Data Availability

Data available from the corresponding authors on reasonable request.

References

  1. López-Salas, L., Borrás-Linares, I., Quintin, D., García-Gomez, P., Giménez-Martínez, R., Segura-Carretero, A., Lozano-Sánchez, J.: Artichoke by-products as natural source of phenolic food ingredient. Appl. Sci. 11, 3788 (2021)

    Article  Google Scholar 

  2. Aune, D., Giovannucci, E., Boffetta, P., Fadnes, L.T., Keum, N., Norat, T., Greenwood, D.C., Riboli, E., Vatten, L.J., Tonstad, S.: Fruit and vegetable intake and the risk of cardiovascular disease, total cancer and all-cause mortality-A systematic review and dose-response meta-analysis of prospective studies. Int. J. Epidemiol. 46, 1029–1056 (2017). doi:https://doi.org/10.1093/ije/dyw319

    Article  Google Scholar 

  3. Noriega-Rodríguez, D., Soto-Maldonado, C., Torres-Alarcón, C., Pastrana-Castro, L., Weinstein-Oppenheimer, C., Zúñiga-Hansen, M.E.: Valorization of globe artichoke (Cynara scolymus) agro-industrial discards, obtaining an extract with a selective effect on viability of cancer cell lines. Processes. 8, 715 (2020)

    Article  Google Scholar 

  4. Órbenes, G., Rodríguez-Seoane, P., Torres, M.D., Chamy, R., Zúñiga, M.E., Domínguez, H.: Valorization of artichoke industrial by-products using green extraction technologies: formulation of hydrogels in combination with paulownia extracts. Molecules 26, 4386 (2021)

    Article  Google Scholar 

  5. Doria, E., Boncompagni, E., Marra, A., Dossena, M., Verri, M., Buonocore, D.: Polyphenols extraction from vegetable wastes using a green and sustainable method. Front. Nutr. 5, 1–7 (2021)

    Google Scholar 

  6. Ribeiro, T.B., Voss, G.B., Coelho, M.C., Pintado, M.E.: Food waste and by-product valorization as an integrated approach with zero waste: future challenges. In: Bhat, R. (ed.) Future foods, pp. 569–596. Academic Press, Cambridge (2022)

    Chapter  Google Scholar 

  7. El Sayed, A.M., Hussein, R., Motaal, A.A., Fouad, M.A., Aziz, M.A., El-Sayed, A.: Artichoke edible parts are hepatoprotective as commercial leaf preparation. Revista Brasileira de Farmacognosia. 28, 165–178 (2018)

    Article  Google Scholar 

  8. Rocchetti, G., Lucini, L., Corrado, G., Colla, G., Cardarelli, M., Pascale, S.D., Rouphael, Y.: Phytochemical profile, mineral content, and bioactive compounds in leaves of seed-propagated artichoke hybrid cultivars. Molecules. 25, 3795 (2020)

    Article  Google Scholar 

  9. Mahboubi, M.: Cynara scolymus (artichoke) and its efficacy in management of obesity. Bull. Fac. Pharm. Cairo Univ. 56, 115–120 (2018)

    Google Scholar 

  10. Spínola, V., Castilho, P.C.: Evaluation of Asteraceae herbal extracts in the management of diabetes and obesity. Contribution of caffeoylquinic acids on the inhibition of digestive enzymes activity and formation of advanced glycation end-products (in vitro). Phytochemistry. 143, 29–35 (2017)

    Article  Google Scholar 

  11. Wu, D.-T., Nie, X.-R., Shen, D.-D., Li, H.-Y., Zhao, L., Zhang, Q., Lin, D.-R., Qin, W.: Phenolic compounds, antioxidant activities, and inhibitory effects on digestive enzymes of different cultivars of okra (Abelmoschus esculentus). Molecules. 25, 1276 (2020)

    Article  Google Scholar 

  12. Zhang, X., Jia, Y., Ma, Y., Cheng, G., Cai, S.: Phenolic composition, antioxidant properties, and inhibition toward digestive enzymes with molecular docking analysis of different fractions from Prinsepia utilis royle fruits. Molecules. 23, 3373 (2018)

    Article  Google Scholar 

  13. Lu, Y., Tian, C., Gao, C., Wang, B., Yang, W., Kong, X., Chai, L., Chen, G., Yin, X., He, Y.: -h.: Phenolic composition, antioxidant capacity and inhibitory effects on α-glucosidase and lipase of immature faba bean seeds. Int. J. Food Prope. 21, 2366–2377 (2018)

    Article  Google Scholar 

  14. Chen, J.-Y., Sridhar, K., Tsai, P.-J.: Anti-glycation and inhibition of starch hydrolyzing enzymes by enzymatically hydrolysed djulis (Chenopodium formosanum Koidz.) Hull, leaf and seedling. Int. J. Food Sci. Technol. 56, 6601–6610 (2021)

    Article  Google Scholar 

  15. Ruiz, H.H., Ramasamy, R., Schmidt, A.M.: Advanced glycation end products: building on the concept of the “common soil” in metabolic disease. Endocrinology 161, 1–10 (2019)

    Google Scholar 

  16. Nguyen, T.M.C., Gavahian, M., Tsai, P.-J.: Ultrasound-assisted extraction of Gac (Momordica cochinchinensis Spreng.) Leaves: effect of maturity stage on phytochemicals and carbohydrate-hydrolyzing enzymes inhibitory activity. Ital. J. Food Sci 33, 34–42 (2021)

    Article  Google Scholar 

  17. Cortez, J., Faicán, M., Pirovani, M., Piagentini, A.: Determination of polyphenols in fruits added with vitamin C: methodology to improve the specificity of the Folin-Ciocalteu test. Revista Iberoamericana de Tecnologia Postcosecha 19, 147–158 (2018)

    Google Scholar 

  18. Chang, C.-C., Yang, M.-H., Wen, H.-M., Chern, J.-C.: Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J. Food Drug Anal. 10, 178–182 (2002)

    Google Scholar 

  19. Wong, C.-C., Li, H.-B., Cheng, K.-W., Chen, F.: A systematic survey of antioxidant activity of 30 chinese medicinal plants using the ferric reducing antioxidant power assay. Food Chem. 97, 705–711 (2006)

    Article  Google Scholar 

  20. Jo, Y.H., Kim, S.B., Liu, Q., Do, S.-G., Hwang, B.Y., Lee, M.K.: Comparison of pancreatic lipase inhibitory isoflavonoids from unripe and ripe fruits of Cudrania tricuspidata. PloS One. 12, e0172069 (2017)

    Article  Google Scholar 

  21. Aleixandre, A., Gil, J.V., Sineiro, J., Rosell, C.M.: Understanding phenolic acids inhibition of α-amylase and α-glucosidase and influence of reaction conditions. Food Chem. 372, 131231 (2022)

    Article  Google Scholar 

  22. Wang, C., Li, W., Chen, Z., Gao, X., Yuan, G., Pan, Y., Chen, H.: Effects of simulated gastrointestinal digestion in vitro on the chemical properties, antioxidant activity, α-amylase and α-glucosidase inhibitory activity of polysaccharides from Inonotus obliquus. Food Res. Int. 103, 280–288 (2018)

    Article  Google Scholar 

  23. Jaradat, N., Zaid, A.N., Hussein, F., Zaqzouq, M., Aljammal, H., Ayesh, O.: Anti-lipase potential of the organic and aqueous extracts of ten traditional edible and medicinal plants in Palestine: a comparison study with Orlistat. Medicines 4, 89 (2017)

    Article  Google Scholar 

  24. Dechakhamphu, A., Wongchum, N.: Screening for anti-pancreatic lipase properties of 28 traditional thai medicinal herbs. Asian Pac. J. Trop. Biomed. 5, 1042–1045 (2015)

    Article  Google Scholar 

  25. Olaokun, O.O., McGaw, L.J., Eloff, J.N., Naidoo, V.: Evaluation of the inhibition of carbohydrate hydrolysing enzymes, antioxidant activity and polyphenolic content of extracts of ten african Ficus species (Moraceae) used traditionally to treat diabetes. BMC Complement. Altern. Med. 13, 94 (2013)

    Article  Google Scholar 

  26. Nadeem, M., Zeb, A.: Impact of maturity on phenolic composition and antioxidant activity of medicinally important leaves of Ficus carica L. Physiol. Mol. Biology Plants. 24, 881–887 (2018)

    Article  Google Scholar 

  27. Brahem, M., Eder, S., Renard, C.M.G.C., Loonis, M., Le Bourvellec, C.: Effect of maturity on the phenolic compositions of pear juice and cell wall effects on procyanidins transfer. LWT. 85, 380–384 (2017)

    Article  Google Scholar 

  28. Kim, J., Jeong, I.-H., Kim, C.-S., Lee, Y.M., Kim, J.M., Kim, J.S.: Chlorogenic acid inhibits the formation of advanced glycation end products and associated protein cross-linking. Arch. Pharm. Res. 34, 495–500 (2011)

    Article  Google Scholar 

  29. Bustos, A.-S., Håkansson, A., Linares-Pastén, J.A., Nilsson, L.: Interaction between myricetin aggregates and lipase under simplified intestinal conditions. Foods. 9, 777 (2020)

    Article  Google Scholar 

  30. Qiu, X.-L., Zhang, Q.-F.: Chemical profile and pancreatic lipase inhibitory activity of Sinobambusa tootsik (Sieb.) Makino leaves. PeerJ. 7, e7765–e7765 (2019)

    Article  Google Scholar 

  31. Martinez-Gonzalez, A.I., Díaz-Sánchez, Ã.G., Rosa, L.A., Vargas-Requena, C.L., Bustos-Jaimes, I., Alvarez-Parrilla, E.: Polyphenolic compounds and digestive enzymes: In vitro non-covalent interactions. Molecules 22, 669 (2017)

    Article  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the National Pingtung University of Science and Technology, Pingtung, Taiwan for providing research facilities. Also, we would like to thank Taiwan Tian Jian Biotechnology Co. Ltd., Nantou, Taiwan for providing partial financial support.

Funding

The authors have not disclosed any funding.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Kandi Sridhar or Pi-Jen Tsai.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

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

Ye, QM., Sridhar, K. & Tsai, PJ. Artichoke (Cynara scolymus L.) Fruits and Leaves at Different Maturity Stages can Inhibit Digestive Enzymes and Formation of Advanced Glycation End-Products (AGEs). Waste Biomass Valor 14, 3445–3454 (2023). https://doi.org/10.1007/s12649-023-02114-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12649-023-02114-7

Keywords

Navigation