Abstract
Jujube fruit is a considerable source of antioxidants that could be used as ingredients against several diseases. The optimization of microwave-assisted extraction (MAE) of bioactive compounds from Z. lotus pulp and peel (Zlp) was achieved using response surface methodology. The effect of the extraction parameters (microwave power “MW”, extraction time, ethanol/water solvent and liquid–solid ratio) on the total phenolic compounds (TPC) was well described by second-degree regression model. The liquid chromatography-high resolution tandem mass spectrometry (LC–MS–MS) was done. Best results were obtained at 600 W MW power, 180 s irradiation time, 51% ethanol concentration and 47:1 mL/g solvent-to solid ratio obtaining 7473.38 ± 740.55 mg GAE/100 g of TPC, 1019.96 ± 75.03 mg CE/100 g of TFC, 14,253.11 ± 2453.86 mg CE/100 g of TTC. LC–MS–MS determined that from all phytochemicals, 44.51% of the extract was flavonoids which represent 80.75% of all secondary metabolites from which 5-hydroxy-7-O-nerylflavanone is found to be the most abundant one. The extracts revealed the presence of 34 bioactive compounds, from which 10 phenolic compounds have never been previously identified from Zizyphus plant. The Zlp extract exhibited a greatest antioxidant effects by PAOT, DPPH, and FRAP activity; as well as, a lowest cytotoxic effects against both HepG2 and MCF-7 cells. In a concentration of 1 mg/mL, Zlp produced a strong AChE inhibition. This research revealed that MAE is more rapid and an effective method to extract TPC recovery which can be used in food matrixes and/or in nutraceutical formulations for its good biological effect.
Similar content being viewed by others
References
R. Ksouri, W.M. Ksouri, I. Jallali, A. Debez, C. Magné, I. Hiroko, C. Abdelly, Medicinal halophytes: potent source of health promoting biomolecules with medical, nutraceutical and food applications. Crit. Rev. Biotechnol. 32(4), 289–326 (2012)
K. Das, A. Roychoudhury, Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front. Environ. Sci. 2, 53 (2014)
F. Berkani, M.L. Serralheiro, F. Dahmoune, A. Ressaissi, N. Kadri, H. Remini, Ultrasound assisted extraction of phenolic compounds from a Jujube by-product with valuable bioactivities. Processes 8(11), 1441 (2020)
F. Berkani, F. Dahmoune, M.L. Serralheiro, A. Ressaissi, S. Dairi, N. Kadri, H. Remini, A. Abbou, K. Madani, New bioactive constituents characterized by LC–MS/MS in optimized microwave extract of jujube seeds (Zizyphus lotus L.). J. Food Meas. Charact. (2021). https://doi.org/10.1007/s11694-021-00903-z
Y. Li, B. Guo, W. Wang, L. Li, L. Cao, C. Yang, J. Liu, Q. Liang, J. Chen, S. Wu, Characterization of phenolic compounds from Phyllanthus emblica fruits using HPLC-ESI-TOF-MS as affected by an optimized microwave-assisted extraction. Int. J. Food Prop. 22(1), 330–342 (2019)
F. Biglari, A.F. AlKarkhi, A.M. Easa, Antioxidant activity and phenolic content of various date palm (Phoenix dactylifera) fruits from Iran. Food Chem. 107(4), 1636–1641 (2008)
C. Caleja, L. Barros, A.L. Antonio, M.B.P. Oliveira, I.C. Ferreira, A comparative study between natural and synthetic antioxidants: Evaluation of their performance after incorporation into biscuits. Food Chem. 216, 342–346 (2017)
F. Dahmoune, B. Nayak, K. Moussi, H. Remini, K. Madani, Optimization of microwave-assisted extraction of polyphenols from Myrtus communis L. leaves. Food Chem. 166, 585–595 (2015)
T. Garrido, M. Gizdavic-Nikolaidis, I. Leceta, M. Urdanpilleta, P. Guerrero, K. de la Caba, P.A. Kilmartin, Optimizing the extraction process of natural antioxidants from chardonnay grape marc using microwave-assisted extraction. Waste Manag. 88, 110–117 (2019)
W. Borgi, N. Chouchane, Anti-spasmodic effects of Zizyphus lotus (L.) Desf. extracts on isolated rat duodenum. J. Ethnopharmacol. 126(3), 571–573 (2009)
F. Berkani, M.L. Serralheiro, F. Dahmoune, M. Mahdjoub, N. Kadri, S. Dairi, S. Achat, H. Remini, A. Abbou, K. Adel, Ziziphus lotus (L.) Lam. plant treatment by ultrasounds and microwaves to improve antioxidants yield and quality: an overview. N. Afr. J. Food Nutr. Res. 5(12), 53–68 (2021)
A.H. Al-Saeedi, M.T.H. Al-Ghafri, M.A. Hossain, Comparative evaluation of total phenols, flavonoids content and antioxidant potential of leaf and fruit extracts of Omani Ziziphus jujuba L. Pac. Sci. Rev. A: Nat. Sci. Eng. 18(1), 78–83 (2016)
M. Škerget, P. Kotnik, M. Hadolin, A.R. Hraš, M. Simonič, Ž Knez, Phenols, proanthocyanidins, flavones and flavonols in some plant materials and their antioxidant activities. Food Chem. 89(2), 191–198 (2005)
K. Aya, T. M’hamed, Chemical compounds, antioxidant activity, and in vitro and in silico litholytic effects of Zizyphus lotus extracts. J. Basic Clin. Physiol. Pharmacol. (2020). https://doi.org/10.1515/jbcpp-2019-0091
W. Rached, L. Barros, B.E. Ziani, M. Bennaceur, R.C. Calhelha, S.A. Heleno, M.J. Alves, A. Marouf, I.C. Ferreira, HPLC-DAD-ESI-MS/MS screening of phytochemical compounds and the bioactive properties of different plant parts of Zizyphus lotus (L.) Desf. Food Funct. 10(9), 5898–5909 (2019)
R. Nuerxiati, A. Abuduwaili, P. Mutailifu, A. Wubulikasimu, N. Rustamova, C. Jingxue, H.A. Aisa, A. Yili, Optimization of ultrasonic-assisted extraction, characterization and biological activities of polysaccharides from Orchis chusua D. Don (Salep). Int. J. Biol. macromol. 141, 431–443 (2019)
I. Sarakatsianos, K. Adamopoulos, V. Samanidou, A. Goula, E. Ninou, Optimization of Microwave-Assisted Extraction of Phenolic Compounds from Medicinal and Aromatic Plants: Sideritis raeseri, Sideritis scardica and Origanum vulgare. Curr. Anal. Chem. 16(2), 106–111 (2020)
F. Berkani, F. Dahmoune, S. Achat, S. Dairi, N. Kadri, S. Zeghichi-Hamri, A. Abbou, I. Benzitoune, K. Adel, H. Remini, Response surface methodology optimization of microwave-assisted polysaccharide extraction from Algerian Jujube (Zizyphus lotus L.) pulp and peel. J. Pharm. Innov. (2020). https://doi.org/10.1016/j.ultsonch.2016.04.017
I. Alzorqi, S. Sudheer, T.-J. Lu, S. Manickam, Ultrasonically extracted β-d-glucan from artificially cultivated mushroom, characteristic properties and antioxidant activity. Ultrason. Sonochem. 35, 531–540 (2017)
E. Wei, R. Yang, H. Zhao, P. Wang, S. Zhao, W. Zhai, Y. Zhang, H. Zhou, Microwave-assisted extraction releases the antioxidant polysaccharides from seabuckthorn (Hippophae rhamnoides L.) berries. Int. J. Biol. Macromol. 123, 280–290 (2019)
M. Marić, A.N. Grassino, Z. Zhu, F.J. Barba, M. Brnčić, S.R. Brnčić, An overview of the traditional and innovative approaches for pectin extraction from plant food wastes and by-products: ultrasound-, microwaves-, and enzyme-assisted extraction. Trends Food Sci. Technol. 76, 28–37 (2018)
F. Chemat, M. Abert-Vian, A.S. Fabiano-Tixier, J. Strube, L. Uhlenbrock, V. Gunjevic, G. Cravotto, Green extraction of natural products. Origins, current status, and future challenges. TrAC Trends Anal. Chem. 118, 248–263 (2019)
K.M. Hammi, A. Jdey, C. Abdelly, H. Majdoub, R. Ksouri, Optimization of ultrasound-assisted extraction of antioxidant compounds from Tunisian Zizyphus lotus fruits using response surface methodology. Food Chem. 184, 80–89 (2015)
M.F. Ghafar, K.N. Prasad, K.K. Weng, A. Ismail, Flavonoid, hesperidine, total phenolic contents and antioxidant activities from Citrus species. A. J. Biotechnol. 9(3), 326–330 (2010)
L. Guedes, P.B. Reis, M. Machuqueiro, A. Ressaissi, R. Pacheco, M.L. Serralheiro, Bioactivities of Centaurium erythraea (Gentianaceae) decoctions: antioxidant activity. Enzyme Inhib. Docking Stud. Mol. 24(20), 3795 (2019)
M. Kaci, A. Belhaffef, S. Meziane, G. Dostert, P. Menu, E. Velot, S. Desobry, E. Arab-Tehrany, Nanoemulsions and topical creams for the safe and effective delivery of lipophilic antioxidant coenzyme Q10. Colloids Surf. B 167, 165–175 (2018)
P. Joël, K. Mouna-Messaouda, C.-B. Jean-Paul, D. Jean-Olivier, M. Smail, Electrochemical methodology for evaluating skin oxidative stress status (SOSS). Diseases 7(2), 40 (2019)
S. Achat, V. Tomao, K. Madani, M. Chibane, M. Elmaataoui, O. Dangles, F. Chemat, Direct enrichment of olive oil in oleuropein by ultrasound-assisted maceration at laboratory and pilot plant scale. Ultrason. Sonochem. 19(4), 777–786 (2012)
K.M. Hammi, M. Hammami, C. Rihouey, D. Le Cerf, R. Ksouri, H. Majdoub, Optimization extraction of polysaccharide from Tunisian Zizyphus lotus fruit by response surface methodology: composition and antioxidant activity. Food Chem. 212, 476–484 (2016)
G. Zhang, M. Hu, L. He, P. Fu, L. Wang, J. Zhou, Optimization of microwave-assisted enzymatic extraction of polyphenols from waste peanut shells and evaluation of its antioxidant and antibacterial activities in vitro. Food Bioprod. Process. 91(2), 158–168 (2013)
J.P. Maran, S. Manikandan, Response surface modeling and optimization of process parameters for aqueous extraction of pigments from prickly pear (Opuntia ficus-indica) fruit. Dyes Pigm. 95(3), 465–472 (2012)
K. Rewatkar, D.Z. Shende, K.L. Wasewar, Modeling and optimization of reactive extraction of gallic acid using RSM. Chem. Eng. Commun. 204(4), 522–528 (2017)
K. Hayat, S. Hussain, S. Abbas, U. Farooq, B. Ding, S. Xia, C. Jia, X. Zhang, W. Xia, Optimized microwave-assisted extraction of phenolic acids from citrus mandarin peels and evaluation of antioxidant activity in vitro. Sep. Purif. Technol. 70(1), 63–70 (2009)
J. Song, D. Li, C. Liu, Y. Zhang, Optimized microwave-assisted extraction of total phenolics (TP) from Ipomoea batatas leaves and its antioxidant activity. Innov. Food Sci. Emerg. Technol. 12(3), 282–287 (2011)
I.T. Stanisavljević, D.T. Veličković, Z.B. Todorović, M.L. Lazić, V.B. Veljković, Comparison of techniques for the extraction of tobacco seed oil. Eur. J. Lipid Sci. Technol. 111(5), 513–518 (2009)
A. Wojdyło, Á.A. Carbonell-Barrachina, P. Legua, F. Hernández, Phenolic composition, ascorbic acid content, and antioxidant capacity of Spanish jujube (Ziziphus jujube Mill.) fruits. Food Chem. 201, 307–314 (2016)
S. Cosmulescu, I. Trandafir, N. Violeta, G. Achim, B. Mihai, O. Iordanescu, Variation of bioactive compounds and antioxidant activity of jujube (Ziziphus jujuba) fruits at different stages of ripening. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 46(1), 134–137 (2018)
T.K. Koley, C. Kaur, S. Nagal, S. Walia, S. Jaggi, Antioxidant activity and phenolic content in genotypes of Indian jujube (Zizyphus mauritiana Lamk.). Arab. J. Chem. 9, S1044–S1052 (2016)
Q.H. Gao, C.S. Wu, J.G. Yu, M. Wang, Y.J. Ma, C.L. Li, Textural characteristic, antioxidant activity, sugar, organic acid, and phenolic profiles of 10 promising jujube (Ziziphus jujuba Mill.) selections. J. Food Sci. 77(11), C1218–C1225 (2012)
O.R. Alara, N.H. Abdurahman, Microwave-assisted extraction of phenolics from Hibiscus sabdariffa calyces: kinetic modelling and process intensification. Ind. Crops Prod. 137, 528–535 (2019)
H.-x Zhao, H.-s Zhang, S.-f Yang, Phenolic compounds and its antioxidant activities in ethanolic extracts from seven cultivars of Chinese jujube. Food Sci. Hum. Wellness 3(3–4), 183–190 (2014)
M.A. Benabderrahim, W. Elfalleh, C. Sarikurkcu, R.B. Sarikurkcu, Biological activities and phytochemical composition of organs from Loranthus europaeus. Ind. Crops Prod. 141, 111772 (2019)
W. Ma, P. Waffo-Téguo, M. Jourdes, H. Li, P.-L. Teissedre, First evidence of epicatechin vanillate in grape seed and red wine. Food Chem. 259, 304–310 (2018)
D. Šuković, B. Knežević, U. Gašić, M. Sredojević, I. Ćirić, S. Todić, J. Mutić, Ž Tešić, Phenolic profiles of leaves, grapes and wine of grapevine variety Vranac (Vitis vinifera L.) from Montenegro. Foods 9(2), 138 (2020)
G. Aldini, L. Regazzoni, A. Pedretti, M. Carini, S.-M. Cho, K.-M. Park, K.-J. Yeum, An integrated high resolution mass spectrometric and informatics approach for the rapid identification of phenolics in plant extract. J. Chromatogr. A 1218(20), 2856–2864 (2011)
W.T. Yang, K.M. Cho, J.H. Lee, Comparative analysis of isoflavone aglycones using microwave-assisted acid hydrolysis from soybean organs at different growth times and screening for their digestive enzyme inhibition and antioxidant properties. Food Chem. 305, 125462 (2020)
W. Xu, M. Huang, H. Li, X. Chen, Y. Zhang, J. Liu, W. Xu, K. Chu, L. Chen, Chemical profiling and quantification of Gua-Lou-Gui-Zhi decoction by high performance liquid chromatography/quadrupole-time-of-flight mass spectrometry and ultra-performance liquid chromatography/triple quadrupole mass spectrometry. J. Chromatogr. B 986, 69–84 (2015)
A. Guzel, H. Aksit, M. Elmastas, R. Erenler, Bioassay-guided isolation and identification of antioxidant flavonoids from Cyclotrichium origanifolium (Labill.) manden and scheng. Pharmacog. Mag. 13(50), 316 (2017)
M.N. Khan, F.U. Haq, S. Rahman, A. Ali, S.G. Musharraf, Metabolite distribution and correlation studies of Ziziphus jujuba and Ziziphus nummularia using LC-ESI-MS/MS. J. Pharm. Biomed. Anal. 178, 112918 (2020)
Y. Lamotte, P. Martres, N. Faucher, A. Laroze, D. Grillot, N. Ancellin, Y. Saintillan, V. Beneton, R.T. Gampe Jr., Synthesis and biological activities of novel indole derivatives as potent and selective PPARγ modulators. Bioorg. Med. Chem. Lett. 20(4), 1399–1404 (2010)
H. Amat-ur-Rasool, F. Symes, D. Tooth, L.-N. Schaffert, E. Elmorsy, M. Ahmed, S. Hasnain, W.G. Carter, Potential nutraceutical properties of leaves from several commonly cultivated plants. Biomolecules 10(11), 1556 (2020)
N.P. Thao, B.H. Tai, B.T.T. Luyen, S. Kim, J.E. Koo, Y.S. Koh, N.T. Cuong, N. Van Thanh, N.X. Cuong, N.H. Nam, Chemical constituents from Kandelia candel with their inhibitory effects on pro-inflammatory cytokines production in LPS-stimulated bone marrow-derived dendritic cells (BMDCs). Bioorg. Med. Chem. Lett. 25(7), 1412–1416 (2015)
M. Muchuweti, G. Zenda, A.R. Ndhlala, A. Kasiyamhuru, Sugars, organic acid and phenolic compounds of Ziziphus mauritiana fruit. Eur. Food Res. Technol. 221(3–4), 570–574 (2005)
M. Memarpoor-Yazdi, H. Mahaki, H. Zare-Zardini, Antioxidant activity of protein hydrolysates and purified peptides from Zizyphus jujuba fruits. J. Funct. Foods 5(1), 62–70 (2013)
C. Benammar, C. Baghdad, M. Belarbi, S. Subramaniam, A. Hichami, N. Khan, Antidiabetic and antioxidant activities of Zizyphus lotus L. aqueous extracts in Wistar rats. J. Nutr. Food Sci. 2014, 2–6 (2014)
A. Freitas, J. Andrade, F. Silva, T. Rocha-Santos, A. Duarte, A. Gomes, Antioxidative peptides: trends and perspectives for future research. Curr. Med. Chem. 20(36), 4575–4594 (2013)
S. Choonpicharn, S. Tateing, S. Jaturasitha, N. Rakariyatham, N. Suree, H. Niamsup, Identification of bioactive peptide from Oreochromis niloticus skin gelatin. J. Food Sci. Technol. 53(2), 1222–1229 (2016)
H. Zare-Zardini, B. Tolueinia, A. Hashemi, L. Ebrahimi, F. Fesahat, Antioxidant and cholinesterase inhibitory activity of a new peptide from Ziziphus jujuba fruits. Am. J. Alzheimer’s Dis. Demen. 28(7), 702–709 (2013)
C. Dang, T. Bannan, P. Shelley, M. Priestley, S.D. Worrall, J. Waters, H. Coe, C.J. Percival, D. Topping, The effect of structure and isomerism on the vapor pressures of organic molecules and its potential atmospheric relevance. Aerosol Sci. Technol. 53(9), 1040–1055 (2019)
R. Kaur, P. Yadav, A.K. Thukral, A. Sharma, R. Bhardwaj, M.N. Alyemeni, L. Wijaya, P. Ahmad, Castasterone and citric acid supplementation alleviates cadmium toxicity by modifying antioxidants and organic acids in Brassica juncea. J. Plant Growth Regul. 37(1), 286–299 (2018)
H. Ghazghazi, C. Aouadhi, L. Riahi, A. Maaroufi, B. Hasnaoui, Fatty acids composition of Tunisian Ziziphus lotus L. (Desf.) fruits and variation in biological activities between leaf and fruit extracts. Nat. Prod. Res 28(14), 1106–1110 (2014)
C. Wang, D. Cheng, J. Cao, W. Jiang, Antioxidant capacity and chemical constituents of Chinese jujube (Ziziphus jujuba Mill.) at different ripening stages. Food Sci. Biotechnol. 22(3), 639–644 (2013)
P. Joël, K. Mouna-Messaouda, K. Claire, T. Jessica, E.E. Raymond, M. Smail, PAOT-Liquid® technology: An easy electrochemical method for evaluating antioxidant capacity of wines. Diseases 7(1), 10 (2019)
J.M. Smail Meziane, Michel Mathé, Stephania Raimond, Jean-Luc. Yvon, Messaouda-Mouna. Kaci, Bioavailability of natural and synthetic vitamins: a significant difference on oxidative stress status (OSS). Oat J. (2021). https://doi.org/10.15761/IFNM.1000301
J. Wang, J. Zhang, B. Zhao, X. Wang, Y. Wu, J. Yao, A comparison study on microwave-assisted extraction of Potentilla anserina L. polysaccharides with conventional method: molecule weight and antioxidant activities evaluation. Carbohydr. Polym. 80(1), 84–93 (2010)
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)
G. Zengin, B. Atasagun, M.Z. Aumeeruddy, H. Saleem, A. Mollica, M.B. Bahadori, M.F. Mahomoodally, Phenolic profiling and in vitro biological properties of two Lamiaceae species (Salvia modesta and Thymus argaeus): a comprehensive evaluation. Ind. Crops Prod. 128, 308–314 (2019)
P.K. Yılmaz, A. Ertaş, M. Akdeniz, M.K. Avcı, U. Kolak, Chemical compositions by LC-MS/MS and GC-MS and biological activities of Chenopodium album subsp album var. microphyllum. Ind. Crops Prod. 141, 111755 (2019)
Y. Jiang, H. Gao, G. Turdu, Traditional Chinese medicinal herbs as potential AChE inhibitors for anti-Alzheimer’s disease: a review. Bioorg. Chem. 75, 50–61 (2017)
A. Ressaissi, N. Attia, P.L. Falé, R. Pacheco, B.L. Victor, M. Machuqueiro, M.L.M. Serralheiro, Isorhamnetin derivatives and piscidic acid for hypercholesterolemia: cholesterol permeability, HMG-CoA reductase inhibition, and docking studies. Arch. Pharmacal. Res. 40(11), 1278–1286 (2017)
Acknowledgements
This research was supported by the ministry of the higher education and scientific research and the faculty of Natural Sciences, Life and Earth Sciences, University of Bouira, Algeria; the Portuguese Foundation for Science and Technology, FCT, through the Research Unit grant UID/MULTI/04046/2019 to BioISI; FCT project PTDC/BIA-BQM/28355/2017; BioISI MassSPEC Facility.
Author information
Authors and Affiliations
Corresponding author
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
About this article
Cite this article
Berkani, F., Dahmoune, F., Kadri, N. et al. LC–ESI–MS/MS analysis, biological effects of phenolic compounds extracted by microwave method from Algerian Zizyphus lotus fruits. Food Measure 16, 3354–3371 (2022). https://doi.org/10.1007/s11694-022-01437-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11694-022-01437-8