Effect of Different Extracting Solvents on Antioxidant Activity and Inhibitory Effect on Diabetic Enzymes of Chlorella vulgaris and Spirulina platensis
Article Sidebar
Main Article Content
Abstract
This study aimed to determine the effect of the solvent used in microalgae extraction on the total phenolic content (TPC), total flavonoid content (TFC), antioxidant, and anti-carbohydrate-hydrolyzing enzyme activities of the crude extracts. Algal biomass of Chlorella vulgaris and Spirulina platensis was extracted by different types of solvent, namely n-hexane, ethanol, methanol, and distilled water. Additionally, the correlations of TPC and TFC with antioxidant activity as well as anti-diabetic activity (anti-α-amylase and anti-α-glucosidase) were investigated. Results demonstrated that C. vulgaris and S. platensis methanolic extracts had the highest TPC, with values of 40.62±4.13 and 64.38±7.39 mg GAE·g-1 (mg of gallic acid equivalent per gram extract), respectively. These extracts also showed the greatest antioxidant activity, with IC50 values for DPPH (2,2-diphenyl-1-picrylhydrazyl) of 117.62±4.46 and 97.89±4.64 µg·mL-1, respectively, and ABTS (2,2-azinobis [3-ethylbenzothiazoline-6-sulfonic acid]) of 102.52±2.50 and 46.21±0.88 µg·mL-1, respectively. Furthermore, they strongly inhibited α-amylase activity (IC50 of 262.97±9.61 and 275.46±12.44 µg·mL-1) and α-glucosidase activity (IC50 of 207.09±6.97 and 169.01±3.16 µg·mL-1). TPC was positively and significantly correlated with antioxidant and α-glucosidase inhibition activities. Meanwhile, only α-amylase inhibitory activity had a significant positive correlation with TFC. Therefore, crude methanolic extracts of C. vulgaris and S. platensis might be potential sources of natural antioxidants and anti-diabetic dietary supplements.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Abbasi, A., D. Juszczyk, C.H.M. van Jaarsveld and M.C. Gulliford. 2017. Body mass index and incident type 1 and type 2 diabetes in children and young adults: A retrospective cohort study. Journal of the Endocrine Society 1(5): 524-537. DOI: 10.1210/js.2017-00044.
Abdel-Moneim, A.M.E., M.T. El-Saadony, A.M. Shehata, A.M. Saad, S.A. Aldhumri, S.M. Ouda and N.M. Mesalam. 2022. Antioxidant and antimicrobial activities of Spirulina platensis extracts and biogenic selenium nanoparticles against selected pathogenic bacteria and fungi. Saudi Journal of Biological Sciences 29(2): 1197-1209. DOI: 10.1016/j.sjbs.2021.09.046.
Aizzat, O., S.W. Yap, H. Sopiah, M. Madiha, M. Hazreen, A. Shailah, W.Y. Wan Junizam, A. Nur Syaidah, D. Srijit, M. Musalmah and M.Y. Yasmin Anum. 2010. Modulation of oxidative stress by Chlorella vulgaris in streptozotocin (STZ) induced diabetic Sprague-Dawley rats. Advances in Medical Sciences 55(2): 281-288. DOI: 10.2478/v10039-010-0046-z.
Alqahtani, A.S., S. Hidayathulla, M.T. Rehman, A.A. Elgamal, S. Al-Massarani, V. Razmovski-Naumovski, M.S. Alqahtani, R.A. El Dib and M.F. Alajmi. 2020. Alpha-amylase and alpha-glucosidase enzyme inhibition and antioxidant potential of 3-oxolupenal and katononic acid isolated from Nuxia oppositifolia. Biomolecules 10(1): 61. DOI: 10.3390/biom10010061.
Altemimi, A., N. Lakhssassi, A. Baharlouei, D.G. Watson and D.A. Lightfoot. 2017. Phytochemicals: Extraction, isolation, and identification of bioactive compounds from plant extracts. Plants 6(4): 42. DOI: 10.3390/plants6040042.
Aryal, S., M.K. Baniya, K. Danekhu, P. Kunwar, R. Gurung and N. Koirala. 2019. Total phenolic content, flavonoid content and antioxidant potential of wild vegetables from western Nepal. Plants 8(4): 96. DOI: 10.3390/plants8040096.
Bai, Z., J. Meng, X. Huang, G. Wu, S. Zuo and S. Nie. 2020. Comparative study on antidiabetic function of six legume crude polysaccharides. International Journal of Biological Macromolecules 154: 25-30. DOI: 10.1016/j.ijbiomac.2020.03.072.
Buttermore, E., V. Campanella and R. Priefer. 2021. The increasing trend of type 2 diabetes in youth: An overview. Diabetes and Metabolic Syndrome: Clinical Research and Reviews 15(5): 102253. DOI: 10.1016/j.dsx.2021.102253.
Canelli, G., L. Neutsch, R. Carpine, S. Tevere, F. Giuffrida, Z. Rohfritsch, F. Dionisi, C.J. Bolten and A. Mathys. 2020. Chlorella vulgaris in a heterotrophic bioprocess: Study of the lipid bioaccessibility and oxidative stability. Algal Research 45: 101754. DOI: 10.1016/j.algal.2019.101754.
Chávez-González, M.L., L. Sepúlveda, D.K. Verma, H.A. Luna-García, L.V. Rodríguez-Durán, A. Ilina and C.N. Aguilar. 2020. Conventional and emerging extraction processes of flavonoids. Processes 8(4): 434. DOI: 10.3390/PR8040434.
de Jesus, S.S., G.F. Ferreira, L.S. Moreira, M.R. Wolf Maciel and R. Maciel Filho. 2019. Comparison of several methods for effective lipid extraction from wet microalgae using green solvents. Renewable Energy 143: 130-141. DOI: 10.1016/j.renene.2019.04.168.
Dirar, A.I., D.H.M. Alsaadi, M. Wada, M.A. Mohamed, T. Watanabe and H.P. Devkota. 2019. Effects of extraction solvents on total phenolic and flavonoid contents and biological activities of extracts from Sudanese medicinal plants. South African Journal of Botany 120: 261-267. DOI: 10.1016/j.sajb.2018.07.003.
Dirir, A.M., M. Daou, A.F. Yousef and L.F. Yousef. 2022. A review of alpha-glucosidase inhibitors from plants as potential candidates for the treatment of type-2 diabetes. Phytochemical Society of Europe 21(4): 1049-1079. DOI: 10.1007/s11101-021-09773-1.
Emami, S. and A. Olfati. 2017. Effects of dietary supplementing of Spirulina platensis and Chlorella vulgaris microalgae on hematologic parameters in streptozotocin-induced diabetic rats. Original Article Iran J Ped Hematol Oncol 7(3): 163-170.
Falleh, H., R. Ksouri, K. Chaieb, N. Karray-Bouraoui, N. Trabelsi, M. Boulaaba and C. Abdelly. 2008. Phenolic composition of Cynara cardunculus L. organs, and their biological activities. Comptes Rendus Biologies 331(5): 372-379. DOI: 10.1016/j.crvi.2008.02.008.
Ghwenm, S.S., F.S. Kata and A.M. Athbi. 2020. Hypoglycemicandantioxidant effect of the ethanol extract of Chlorella vulgaris inalloxan-induced diabetes mice. Biochemical and Cellular Archives 20: 3535-3542.
Goiris, K., K. Muylaert, S. Voorspoels, B. Noten, D. De Paepe, G.J.E Baart and L. De Cooman. 2014. Detection of flavonoids in microalgae from different evolutionary lineages. Journal of Phycology 50(3): 483-492. DOI: 10.1111/jpy.12180.
Hargrove, J.L., P. Greenspan, D.K. Hartle and C. Dowd. 2011. Inhibition of aromatase and α-amylase by flavonoids and proanthocyanidins from Sorghum bicolor bran extracts. Journal of Medicinal Food 14(7-8): 799-807. DOI: 10.1089/jmf.2010.0143.
Hemalatha, P., D.P. Bomzan, B.V.S. Rao and Y.N. Sreerama. 2016. Distribution of phenolic antioxidants in whole and milled fractions of quinoa and their inhibitory effects on α-amylase and α-glucosidase activities. Food Chemistry 199: 330-338. DOI: 10.1016/j.foodchem.2015.12.025.
Hua, F., P. Zhou, H.Y. Wu, G.X. Chu, Z.W. Xie and G.H. Bao. 2018. Inhibition of α-glucosidase and α-amylase by flavonoid glycosides from Lu’an GuaPian tea: molecular docking and interaction mechanism. Food and Function 9(8): 1-31. DOI: 10.1039/c8fo00562a.
Ibrahim, S., A. Al-Ahdal, A. Khedr and G. Mohamed. 2017. Antioxidant α-amylase inhibitors flavonoids from Iris germanica rhizomes. Revista Brasileira de Farmacognosia 27(2): 170-174. DOI: 10.1016/j.bjp.2016.10.001.
Jakopič, J., R. Veberič and F. Štampar. 2009. Extraction of phenolic compounds from green walnut fruits in different solvents. Acta Agriculturae Slovenica 93(1): 11-15. DOI: 10.2478/v10014-009-0002-4.
Kim, K.T., L.E. Rioux and S.L. Turgeon. 2014. Alpha-amylase and alpha-glucosidase inhibition is differentially modulated by fucoidan obtained from Fucus vesiculosus and Ascophyllum nodosum. Phytochemistry 98: 27-33. DOI: 10.1016/j.phytochem.2013.12.003.
Krentz, A.J. and C.J. Bailey. 2005. Oral antidiabetic agents: current role in type 2 diabetes mellitus. Drugs 65(3): 385-411. DOI: 10.2165/00003495-200565030-00005.
Kulshreshta, V. and S.M. Shahid. 2021. Epidemiology and prevalence of type 2 diabetes mellitus in children with obesity. European Journal of Medical and Health Sciences 3(1): 39-43. DOI: 10.24018/ejmed.2021.3.1.693.
Kumar, N. and N. Goel. 2019. Phenolic acids: Natural versatile molecules with promising therapeutic applications. Biotechnology Reports 24: e00370. DOI: 10.1016/j.btre.2019.e00370.
Lankatillake, C., S. Luo, M. Flavel, G.B. Lenon, H. Gill, T. Huynh and D.A. Dias. 2021. Screening natural product extracts for potential enzyme inhibitors: protocols, and the standardisation of the usage of blanks in α-amylase, α-glucosidase and lipase assays. Plant Methods 17(1): 1-19. DOI: 10.1186/s13007-020-00702-5.
Lee, B.H., R. Eskandari, K. Jones, K.R. Reddy, R. Quezada-Calvillo, B.L. Nichols, D.R. Rose, B.R. Hamaker and B.M. Pinto. 2012. Modulation of starch digestion for slow glucose release through “Toggling” of activities of mucosal α-glucosidases. Journal of Biological Chemistry 287(38): 31929-31938. DOI: 10.1074/jbc.M112.351858.
Liang, N. and D.D. Kitts. 2014. Antioxidant property of coffee components: Assessment of methods that define mechanism of action. Molecules 19(11): 19180-19208. DOI: 10.3390/molecules191119180.
Lin, Y.T., H.R. Lin, C.S. Yang, C.C. Liaw, P.J. Sung, Y.H. Kuo, M.J. Cheng and J.J. Chen. 2022. Antioxidant and anti-α-glucosidase activities of various solvent extracts and major bioactive components from the fruits of Crataegus pinnatifida. Antioxidants 11(2): 320. DOI: 10.3390/antiox11020320.
Lucakova, S., I. Branyikova and M. Hayes. 2022. Microalgal proteins and bioactives for food, feed, and other applications. Applied Sciences 12(9): 4402. DOI: 10.3390/app12094402.
Mallikarjun, G.K.G., S.K. Udaya, R. Sarada and G.A. Ravishankar. 2015. Supercritical CO2 extraction of functional compounds from Spirulina and their biological activity. Journal of Food Science and Technology 52(6): 3627-3633. DOI: 10.1007/s13197-014-1426-3.
Marín-Peñalver, J.J., I. Martín-Timón, C. Sevillano-Collantes and F.J. del Cañizo-Gómez. 2016. Update on the treatment of type 2 diabetes mellitus. World Journal of Diabetes 7(17): 354. DOI: 10.4239/wjd.v7.i17.354.
Martinez-Gonzalez, A.I., G. Díaz-Sánchez, L.A. de la Rosa, I. Bustos-Jaimes and E. Alvarez-Parrilla. 2019. Inhibition of α-amylase by flavonoids: Structure activity relationship (SAR). Spectrochimica Acta-Part A: Molecular and Biomolecular Spectroscopy 206(2019): 437-447. DOI: 10.1016/j.saa.2018.08.057.
Mechchate, H., I. Es-Safi, A. Louba, A.S. Alqahtani, F.A. Nasr, O.M. Noman, M. Farooq, M.S. Alharbi, A. Alqahtani, A. Bari, H. Bekkari and D. Bousta. 2021. In vitro alpha-amylase and alpha-glucosidase inhibitory activity and in vivo antidiabetic activity of Withania frutescens L. foliar extract. Molecules 26(2): 293. DOI: 10.3390/molecules26020293.
Miazek, K., L. Kratky, R. Sulc, T. Jirout, M. Aguedo, A. Richel and D. Goffin. 2017. Effect of organic solvents on microalgae growth, metabolism and industrial bioproduct extraction: A review. International Journal of Molecular Sciences 18(7): 1429. DOI: 10.3390/ijms18071429.
Mojzer, E.B., M. Knez Hrnčič, M. Škerget, Ž. Knez and U. Bren. 2016. Polyphenols: Extraction methods, antioxidative action, bioavailability and anticarcinogenic effects. Molecules 21(7): 901. DOI: 10.3390/molecules21070901.
Monteiro, M., R.A. Santos, P. Iglesias, A. Couto, C.R. Serra, I. Gouvinhas, A. Barros, A. Oliva-Teles, P. Enes and P. Díaz-Rosales. 2020. Effect of extraction method and solvent system on the phenolic content and antioxidant activity of selected macro- and microalgae extracts. Journal of Applied Phycology 32(1): 349-362. DOI: 10.1007/s10811-019-01927-1.
Mutha, R.E., A.U. Tatiya and S.J. Surana. 2021. Flavonoids as natural phenolic compounds and their role in therapeutics: an overview. Future Journal of Pharmaceutical Sciences 7(1): 25. DOI: 10.1186/s43094-020-00161-8.
Naik, S.R. and G.R. Kokil. 2013. Development and discovery avenues in bioactive natural products for glycemic novel therapeutics. Studies in Natural Products Chemistry 39: 431-466. DOI: 10.1016/B978-0-444-62615-8.00012-6.
Nair, S.S., V. Kavrekar and A. Mishra. 2013. In vitro studies on alpha amylase and alpha glucosidase inhibitory activities of selected plant extracts. European Journal of Experimental Biology 3(1): 128-132.
Nasirian, F., M. Dadkhah, N. Moradi-Kor and Z. Obeidavi. 2018. Effects of Spirulina platensis microalgae on antioxidant and anti-inflammatory factors in diabetic rats. Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy 11: 375-380. DOI: 10.2147/DMSO.S172104.
Nwosu, F., J. Morris, V.A. Lund, D. Stewart, H.A. Ross and G.J. McDougall. 2011. Anti-proliferative and potential anti-diabetic effects of phenolic-rich extracts from edible marine algae. Food Chemistry 126(3): 1006-1012. DOI: 10.1016/j.foodchem.2010.11.111.
O’Sullivan, A.M., Y.C. O’Callaghan, M.N. O’Grady, M. Hayes, J.P. Kerry and N.M. O’Brien. 2013. The effect of solvents on the antioxidant activity in Caco-2 cells of Irish brown seaweed extracts prepared using accelerated solvent extraction (ASE®). Journal of Functional Foods 5(2): 940-948. DOI: 10.1016/j.jff.2013.02.007.
Oboh, G., O.B. Ogunsuyi, M.D. Ogunbadejo and S.A. Adefegha. 2016. Influence of gallic acid on α-amylase and α-glucosidase inhibitory properties of acarbose. Journal of Food and Drug Analysis 24(3): 627-634. DOI: 10.1016/j.jfda.2016.03.003.
Ondo, J.P., L.C. Obame, T.A. Barhé, G.N. Akoue, E.N. Emvo and J. Lebibi. 2013. Phytochemical screening, total phenolic content and antiradical activity of Asplenium africanum (Aspleniaceae) and fruit of Megaphrinium macrostachyum (Marantaceae). Journal of Applied Pharmaceutical Science 3(8): 92-96. DOI: 10.7324/JAPS.2013.3816.
Panche, A.N., A.D. Diwan and S.R. Chandra. 2016. Flavonoids: An overview. Journal of Nutritional Science 5: 1-15. DOI: 10.1017/jns.2016.41.
Patil, L. and B.B. Kaliwal. 2019. Microalga Scenedesmus bajacalifornicus BBKLP-07, a new source of bioactive compounds with in vitro pharmacological applications. Bioprocess and Biosystems Engineering 42(6): 979-994. DOI: 10.1007/s00449-019-02099-5.
Pereira, D.M., P. Valentão, J.A. Pereira and P.B. Andrade. 2009. Phenolics: From chemistry to biology. Molecules 14(6): 2202-2211. DOI: 10.3390/molecules14062202.
Pinelo, M., M. Rubilar, M. Jerez, J. Sineiro and M.J. Núñez. 2005. Effect of solvent, temperature, and solvent-to-solid ratio on the total phenolic content and antiradical activity of extracts from different components of grape pomace. Journal of Agricultural and Food Chemistry 53(6): 2111-2117. DOI: 10.1021/jf0488110.
Pradeep, P.M. and Y.N. Sreerama. 2018. Phenolic antioxidants of foxtail and little millet cultivars and their inhibitory effects on α-amylase and α-glucosidase activities. Food Chemistry 247(2018): 46-55. DOI: 10.1016/j.foodchem.2017.11.103.
Pradhan, B., S. Patra, S.R. Dash, R. Nayak, C. Behera and M. Jena. 2021. Evaluation of the anti-bacterial activity of methanolic extract of Chlorella vulgaris Beyerinck [Beijerinck] with special reference to antioxidant modulation. Future Journal of Pharmaceutical Sciences 7(1): 17. DOI: 10.1186/s43094-020-00172-5.
Proença, C., M. Freitas, D. Ribeiro, S.M. Tomé, E.F.T. Oliveira, M.F. Viegas, A.N. Araújo, M.J. Ramos, A.M.S. Silva, P.A. Fernandes and E. Fernandes. 2019. Evaluation of a flavonoids library for inhibition of pancreatic α-amylase towards a structure-activity relationship. Journal of Enzyme Inhibition and Medicinal Chemistry 34(1): 577-588. DOI: 10.1080/14756366.2018.1558221.
Quan, N. Van, T.D. Xuan, H.D. Tran, N.T.D. Thuy, L.T. Trang, C.T. Huong, Y. Andriana and P.T. Tuyen. 2019. Antioxidant, α-amylase and α-glucosidase inhibitory activities and potential constituents of Canarium tramdenum bark. Molecules 24(3): 605. DOI: 10.3390/molecules24030605.
Rahim, A., C. Çakir, M. Ozturk, B. Şahin, A. Soulaimani, M. Sibaoueih, B. Nasser, R. Eddoha, A. Essamadi and B. El Amiri. 2021. Chemical characterization and nutritional value of Spirulina platensis cultivated in natural conditions of Chichaoua region (Morocco). South African Journal of Botany 141: 234-242. DOI: 10.1016/j.sajb.2021.05.006.
Ramos-Romero, S., J.R. Torrella, T. Pagès, G. Viscor and J.L. Torres. 2021. Edible microalgae and their bioactive compounds in the prevention and treatment of metabolic alterations. Nutrients 13(2): 1-16. DOI: 10.3390/nu13020563.
Sadeer, N.B., D. Montesano, S. Albrizio, G. Zengin and M.F. Mahomoodally. 2020. The versatility of antioxidant assays in food science and safety-chemistry, applications, strengths, and limitations. Antioxidants 9(8): 1-39. DOI: 10.3390/antiox9080709.
Saeedi, P., I. Petersohn, P. Salpea, B. Malanda, S. Karuranga, N. Unwin, S. Colagiuri, L. Guariguata, A.A. Motala, K. Ogurtsova, J.E. Shaw, D. Bright and R. Williams. 2019. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Research and Clinical Practice 157: 107843. DOI: 10.1016/j.diabres.2019.107843.
Sakran, N., Y. Graham, T. Pintar, W. Yang, R. Kassir, E.M. Willigendael, R. Singhal, Z.E. Kooreman, D. Ramnarain, K. Mahawar, C. Parmar, B. Madhok and S. Pouwels. 2022. The many faces of diabetes. Is there a need for re-classification? A narrative review. BMC Endocrine Disorders 22(1): 1-12. DOI: 10.1186/s12902-021-00927-y.
Shalaby, E.A. and S.M. Shanab. 2013. Comparison of DPPH and ABTS assays for determining antioxidant potential of water and methanol extracts of Spirulina platensis. Indian Journal of Geo-Marine Sciences 42(5): 556-564.
Shanab, S.M.M., S.S.M. Mostafa, E.A. Shalaby and G.I. Mahmoud. 2012. Aqueous extracts of microalgae exhibit antioxidant and anticancer activities. Asian Pacific Journal of Tropical Biomedicine 2(8): 608-615. DOI: 10.1016/S2221-1691(12)60106-3.
Shobana, S., Y.N. Sreerama and N.G. Malleshi. 2009. Composition and enzyme inhibitory properties of finger millet (Eleusine coracana L.) seed coat phenolics: Mode of inhibition of α-glucosidase and pancreatic amylase. Food Chemistry 115(4): 1268-1273. DOI: 10.1016/j.foodchem.2009.01.042.
Snyder, L.R. 1978. Classification off the solvent properties of common liquids. Journal of Chromatographic Science 16(6): 223-234. DOI: 10.1093/chromsci/16.6.223.
Spolaore, P., C. Joannis-Cassan, E. Duran and A. Isambert. 2006. Commercial applications of microalgae. Journal of Bioscience and Bioengineering 101(2): 87-96. DOI: 10.1263/jbb.101.87.
Sun, C., C. Zhao, E.C. Guven, P. Paoli, J. Simal‐Gandara, K.M. Ramkumar, S. Wang, F. Buleu, A. Pah, V. Turi, G. Damian, S. Dragan, M. Tomas, W. Khan, M. Wang, D. Delmas, M.P. Portillo, P. Dar, L. Chen and J. Xiao. 2020. Dietary polyphenols as antidiabetic agents: Advances and opportunities. Food Frontiers 1(1): 18-44. DOI: 10.1002/fft2.15.
Sun, L. and M. Miao. 2020. Dietary polyphenols modulate starch digestion and glycaemic level: A review. Critical Reviews in Food Science and Nutrition 60(4): 541-555. DOI: 10.1080/10408398.2018.1544883.
Swargiary, A., M.K. Roy and S. Mahmud. 2022. Phenolic compounds as α-glucosidase inhibitors: a docking and molecular dynamics simulation study. Journal of Biomolecular Structure and Dynamics. Online ahead of print. DOI: 10.1080/07391102.2022.2058092.
Takahama, U. and S. Hirota. 2018. Interactions of flavonoids with α-amylase and starch slowing down its digestion. Food and Function 9(2): 677-687. DOI: 10.1039/c7fo01539a.
Ul-Haq, I., N. Ullah, G. Bibi, S. Kanwal, M.S. Ahmad and B. Mirza. 2012. Antioxidant and cytotoxic activities and phytochemical analysis of Euphorbia wallichii root extract and its fractions. Iranian Journal of Pharmaceutical Research 11(1): 241-249. DOI: 10.22037/ijpr.2011.1030.
Xiao, J. 2022. Recent advances in dietary flavonoids for management of type 2 diabetes. Current Opinion in Food Science 44: 100806. DOI: 10.1016/j.cofs.2022.01.002.
Xiong, Y., K. Ng, P. Zhang, R.D. Warner, S. Shen, H.Y. Tang, Z. Liang and Z. Fang. 2020. In vitro α-glucosidase and α-amylase inhibitory activities of free and bound phenolic extracts from the bran and kernel fractions of five sorghum grain genotypes. Foods 9(9): 1301. DOI: 10.3390/foods9091301.
Yun, H.J., I. Kim, S.H. Kwon, J.S. Kang and A.S. Om. 2011. Protective effect of Chlorella vulgaris against lead-induced oxidative stress in rat brains. Journal of Health Science 57(3): 245-254. DOI: 10.1248/jhs.57.245.
Zhou, J., M. Wang, J.A. Saraiva, A.P. Martins, C.A. Pinto, M.A. Prieto, J. Simal-Gandara, H. Cao, J. Xiao and F.J. Barba. 2022. Extraction of lipids from microalgae using classical and innovative approaches. Food Chemistry 384: 132236. DOI: 10.1016/j.foodchem.2022.132236.
Zhou, W., G. Chen, D. Chen, H. Ye and X. Zeng. 2020. The antidiabetic effect and potential mechanisms of natural polysaccharides based on the regulation of gut microbiota. Journal of Functional Foods 75(9): 104222. DOI: 10.1016/j.jff.2020.104222.