Combined enzymatic and ultrasound-assisted aqueous two-phase extraction of antidiabetic flavonoid compounds from Strobilanthes crispus leaves
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Keywords:
Ultrasound, enzymatic, aqueous two-phase, S. crispus, antidiabetic
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Abstract
A novel green extraction method combining enzymatic and ultrasound-assisted aqueous two-phase extractions was employed to enhance and purify the flavonoid extract from Strobilanthes crispus leaves. Cellulase was used in the pretreatment, and ethanol-(NH4)2SO4 was selected as the solvent. A concentration of 7% (w/w) cellulase and a duration of 2 h were the optimal conditions for pretreatment. The optimal conditions for ultrasound-assisted aqueous two-phase extraction were 33% (w/w) ethanol and 14% (w/w) (NH4)2SO4 as they produced a yield (77.81%), partition coefficient (31.17), extraction efficiency (98.04%), and a high total flavonoid content (0.3666 mg QE/g dry leaf powder). Six compounds from the leaf extract were identified through liquid chromatography-mass spectrometry/mass spectrometry-quadrupole-time of flight (LCMS/MS-Q-TOF) analysis. The crude extract and three compounds in it (kaempferol, graveobioside A, and genistein) showed an antidiabetic activity with IC50 values of 390.35, 201.87, 292.73, and 431.82 mg/mL, respectively. These values are comparable to the standard drug acarbose.
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Arbianti, R., Angelina, Suryapranata, B., Purwati Latifah, L., Fadilah Putri, N., Surya Utami, T., Muharam, Y., & Slamet. (2023). Combined enzymatic and ultrasound-assisted aqueous two-phase extraction of antidiabetic flavonoid compounds from Strobilanthes crispus leaves. Communications in Science and Technology, 8(2), 113-123. https://doi.org/10.21924/cst.8.2.2023.1214
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9. H. M. Yankuzo, Y. S. Baraya, Z. Mustapha, K. K. Wong, and N. S. Yaacob, Immunomodulatory effects of a bioactive fraction of Strobilanthes crispus in NMU-induced rat mammary tumor model, J. Ethnopharmacol. 213 (2018) 31–37.
10. Y-Y. Siew, H-C. Yew, S-Y. Neo, S-V. Seow, S-M. Lew,. S.W. Lim, CSE-S. Lim, Y-C. Ng, W-G. Seetoh, A. Ali, C.H. Tan, and H-L. Koh,. Evaluation of anti-proliferative S-W activity of medicinal plants used in Asian Traditional Medicine to treat cancer, J. Ethnopharmacol. 235 (2019) 75–87.
11. A. Ghasemzadeh, H. Z. E. Jaafar, and A. Rahmat, Phytochemical constituents and biological activities of different extracts of Strobilanthes crispus (L.) Bremek leaves grown in different locations of Malaysia, BMC Complement. Altern. Med. 15 (2015) 1-10.
12. W. Gu, W. Wang, X. Li, Y. Zhang, L. Wang, C. Yuan, L. Huang, and X. Hao, A novel isocoumarin with anti-influenza virus activity from Strobilanthes cusia, Fitoterapia 107 (2015) 60–62.
13. B. Singh, P.M. Sahu, and M.K. Sharma, Anti-inflammatory and antimicrobial activities of triterpenoids from Strobilanthes callosus Nees, Phytomedicine 9 (2002) 355-359.
14. J. Zhu, X. Kou, C. Wu, G. Fan, T. Li, J. Dou, and D. Shen, Enhanced extraction of bioactive natural products using ultrasound-assisted aqueous two-phase system: Application to flavonoids extraction from jujube peels, Food Chem. 395 (2022) 1-9.
15. B. K. Tiwari, Ultrasound: A clean, green extraction technology, Trends Anal. Chem. 71 (2015) 100–109.
16. M. Singla and N. Sit, Application of ultrasound in combination with other technologies in food processing: A review, Ultrason. Sonochem. 73 (2021) 1-13.
17. J. Q. Quiroz, A. M. N. Duran, M. S. Garcia, G. L. C. Gomez, and J. J. R. Camargo, Ultrasound-assisted extraction of bioactive compounds from annatto seeds, evaluation of their antimicrobial and antioxidant activity, and identification of main compounds by LC/ESI-MS analysis, Int. J. Food Sci. 2019 (2019) 1-9.
18. H.S. Kusuma, P.D. Amelia, C. Admiralia, and M. Mahfud, Kinetics study of oil extraction from Citrus auranticum L. by solvent-free microwave extraction, Commun. Sci. Technol. 1 (2016) 15-18.
19. J-B. Pu, B-H. Xia, Y-J. Hu, H-J. Zhang, J. Chen, J. Zhou, W-Q. Liang, and P. Xu, Multi-optimization of ultrasonic-assisted enzymatic extraction of atratylodes macrocephala polysaccharides and antioxidants using response surface methodology and desirability function approach, Molecules 20 (2015) 22220–22235.
20. S. J. Marathe, S. B. Jadhav, S. B. Bankar, K. K. Dubey, and R. S. Singhal, Improvements in the extraction of bioactive compounds by enzymes, Curr. Opin. Food Sci. 25 (2019) 62–72.
21. W. Tchabo, Y. Ma, F. N. Engmann, and H. Zhang, Ultrasound-assisted enzymatic extraction (UAEE) of phytochemical compounds from mulberry (Morus nigra) must and optimization study using response surface methodology, Ind. Crops Prod. 63 (2015) 214–225.
22. Y. Gao, Y. Shi, N. Miao, W. Xing, C. Yun, S. Wang, W. Wang, and H. Wang, H. A green ultrasound-assisted enzymatic extraction method for efficient extraction of total polyphenols from Empetrum nigrum and determination of its bioactivities, J. Ind. Eng. Chem. 109 (2022) 559–567.
23. O. Gligor, A. Mocan, C. Moldovan, M. Locatelli, G. Cri?an, and I. C. F. R. Ferreira, Enzyme-assisted extractions of polyphenols – A comprehensive review, Trends Food Sci. Technol. 88 (2019) 302–315.
24. M. Puri, D. Sharma, and C. J. Barrow, Enzyme-assisted extraction of bioactives from plants, Trends Biotechnol. 30 (2012) 37–44.
25. X. Zhang, G. Teng, and J. Zhang, Ethanol/salt aqueous two-phase system based ultrasonically assisted extraction of polysaccharides from Lilium davidiivar. unicolor Salisb: Physicochemical characterization and antiglycation properties, J. Mol. Liq. 256 (2018) 497–506.
26. J. Zhu, X. Kou, C. Wu, G. Fan, T. Li, J. Dou, and D. Shen, Enhanced extraction of bioactive natural products using ultrasound-assisted aqueous two-phase system: Application to flavonoids extraction from jujube peels, Food Chem. 395 (2022) 1-9.
27. B. Dong, X. Yuan, Q. Zhao, Q. Feng, B. Liu, Y. Guo, and B. Zhao, Ultrasound-assisted aqueous two-phase extraction of phenylethanoid glycosides from Cistanche deserticola Y. C. Ma stems, J. Sep. Sci. 38 (2015) 1194–1203.
28. Z. Cheng, H. Song, X. Cao, Q. Shen, D. Han, F. Zhong, H. Hu, and Y. Yang, Simultaneous extraction and purification of polysaccharides from Gentiana scabra Bunge by microwave-assisted ethanol-salt aqueous two-phase system, Ind. Crops Prod. 102 (2017) 75–87.
29. H. Wijayanti, P. Mardina, A. Tuhuloula, L. T. Ananda, Z. S. A. Rauf, A. Lutfi, S. F. Riyadi, Evaluation of stirring rate and pH on phenolic compounds recovery from palm kernel shell heavy phase bio-oil, Commun. Sci. Technol. 8 (2023) 25-30.
30. J. C. W. Ouédraogo, C. Dicko, F. B. Kini, Y. L. Bonzi-Coulibaly, and E.S. Dey, Enhanced extraction of flavonoids from Odontonema strictum leaves with antioxidant activity using supercritical carbon dioxide fluid combined with ethanol, J. Supercrit. Fluids. 131 (2018) 66–71.
31. A. Malik, H. Ardalani, S. Anam, L.M. McNair, K.J.K. Kromphardt, R.J.N. Frandsen, H. Franzyk, D. Staerk, and K.T. Kongstad, Antidiabetic xanthones with ?-glucosidase inhibitory activities from an endophytic Penicillium canescens, Fitoterapia 142 (2020) 1-8.
32. X. Peng, G. Zhang, Y. Liao, and D. Gong, Inhibitory kinetics and mechanism of kaempferol on ?-glucosidase, Food Chem. 190 (2016) 207–215.
33. S. S. Nadar, P. Rao, and V. K. Rathod, Enzyme assisted extraction of biomolecules as an approach to novel extraction technology: A review, Food Res. Int. 108 (2018) 309–330.
34. N. Liao, J. Zhong, X. Ye, S. Lu, W. Wang, R. Zhang, J. Xu, S. Chen, and D. Liu, Ultrasonic-assisted enzymatic extraction of polysaccharide from Corbicula fluminea: Characterization and antioxidant activity, LWT – Food Sci. and Tech. 60 (2015) 1113–1121.
35. N. Rokhati, Ratnawati, A. Prasetyaningrum, W. Anggraini, A. Nugroho, N. H. Novita, P. Andarani, and T. Riyanto, Effect of microwave and ultrasonic irradiation on the enzymatic hydrolysis of water hyacinth biomass in the presence of surfactants, Commun. Sci. Technol. 8 (2023) 57-65.
36. Y. Yang, Z. Wang, D. Hu, K. Xiao, and J. Y. Wu, Efficient extraction of pectin from sisal waste by combined enzymatic and ultrasonic process, Food Hydrocolloid. 79 (2018) 189–196.
37. R. Saeed, D. Ahmed, and M. Mushtaq, Ultrasound-aided enzyme-assisted efficient extraction of bioactive compounds from Gymnema sylvestre and optimization as per response surface methodology, Sustain. Chem. Pharm. 29 (2022) 1-15.
38. S. B. Zhang, Z. Wang, and S. Y. Xu, Optimization of the aqueous enzymatic extraction of rapeseed oil and protein hydrolysates, JAOCS 84 (2007) 97–105.
39. D. Huang, X. Zhou, J. Si, X. Gong, and S. Wang, Studies on cellulase ultrasonic-assisted extraction technology for flavonoids from Illicium verum residues, Chem. Cent. J. 10 (2016) 1-9.
40. X. Luo, R. Bai, D. Zhen, Z. Yang, D. Huang, H. Mao, X. Li, H. Zou, Y. Xiang, K. Liu, Z. Wen, and C. Fu, Response surface optimization of the enzyme-based ultrasound-assisted extraction of acorn tannins and their corrosion inhibition properties, Ind. Crops Prod. 129 (2019) 405–413.
41. L. Zhou, B. Jiang, T. Zhang, and S. Li, Ultrasound-assisted aqueous two-phase extraction of resveratrol from the enzymatic hydrolysates of Polygonum cuspidatum, Food Biosci. 31 (2019) 1-9.
42. H. Wijngaard, M. B. Hossain, D. K. Rai, and N. Brunton, Techniques to extract bioactive compounds from food by-products of plant origin, Food Res. Int. 46 (2012) 505–513.
43. Y. Sun and J. Cheng, Hidrolysis of lignocellulosic materials for ethanol production: a review, Bioresour. Technol. 83 (2002) 1-11.
44. T. Guo, D. Su, Y. Huang, Y. Wang, and Y. H. Li, Ultrasound-assisted aqueous two-phase system for extraction and enrichment of zanthoxylum armatum lignans, Molecules 20 (2015) 15273–15286.
45. F. Chávez-Silva, L. Ceron-Romero, L. Arias-Duran, G. Navarrete -Vázquez, J. Almanza-Pérez, R. Román-Ramos, G. Ramírez-Ávila, I. Perea-Arango, R. Villalobos-Molina, and S. Estrada-Soto, Antidiabetic effect of Achillea millefollium through multitarget interactions: ?-glucosidases inhibition, insulin sensitization and insulin secretagogue activities, J. Ethnopharmacology 212 (2018) 1–7.
46. S. Joseph, L. Kumar, and V. N. Bai, Evaluation of anti-diabetic activity of Strobilanthes cuspidata in alloxan induced diabetic rats and the effect of bioactive compounds on inhibition of ?-amylase enzyme, J. Pharmacogn. Phytochem. 5 (2016) 169–175.
47. C. Wang, W. Li, Z. Chen, X. Gao, G. Yuan, Y. Pan, and H. Chen, Effect of simulated gastrointestinal digestion in vitro on the chemical properties, antioxidant activity, alpha-amilase and alpha glucosidase inhibitory activiti of polysaccharides from Innotus obliquus, Food Res. Int. 103 (2018) 280-288.
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