Antioxidant Activity, Total Polyphenol Content, and Cytotoxicity of Various Types of Starch with the Addition of Different Polyphenols
Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
LM2023064
Infrastructure for Promoting Metrology in Food and Nutrition in the Czech Republic
AD43
funding for research of the University of Agriculture in Kraków
LM2023064
Infrastructure for Promoting Metrology in Food and Nutrition in the Czech Republic
PubMed
40509345
PubMed Central
PMC12156204
DOI
10.3390/molecules30112458
PII: molecules30112458
Knihovny.cz E-resources
- Keywords
- (+)-catechin, antioxidant activity, cytotoxicity, epigallocatechin gallate, polyphenol, quercetin, starch, total polyphenol content, trans-ferulic acid,
- MeSH
- Antioxidants * pharmacology chemistry MeSH
- HT29 Cells MeSH
- Caco-2 Cells MeSH
- Catechin analogs & derivatives MeSH
- Zea mays chemistry MeSH
- Humans MeSH
- Cell Line, Tumor MeSH
- Polyphenols * chemistry pharmacology MeSH
- Oryza chemistry MeSH
- Starch * chemistry pharmacology MeSH
- Cell Survival drug effects MeSH
- Check Tag
- Humans MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Antioxidants * MeSH
- Catechin MeSH
- Polyphenols * MeSH
- Starch * MeSH
Given the high incidence of diet-related diseases, including type 2 diabetes and cancer, there is a growing need to explore new strategies for their prevention. Although polyphenols are known to reduce starch digestibility and lower the in vitro glycemic index, their antioxidant capacity and cytotoxic properties, when complexed with starches, remain underexplored. Therefore, this study aimed to investigate the antioxidant activity, total polyphenol content, and cytotoxic potential of polyphenol-starch complexes formed using common dietary polyphenols-(+)-catechin, epigallocatechin gallate, hesperidin, naringenin, trans-ferulic acid, p-coumaric acid, quercetin, and kaempferol-and widely consumed starches from wheat, rice, potato, and maize. Antioxidant activity (FRAP and DPPH) together with the total polyphenols content (Folin-Ciocalteu) were tested: (1) before (undigested) enzymatic hydrolysis of the tested sample; (2) after (digested) enzymatic hydrolysis of the tested sample and (3) after hydrolysis of the sample and its centrifugation (supernatant). Cytotoxicity against colon cancer (Caco-2, HT29) and normal colon (CCD 841CoN) cell lines were determined in vitro by the MTT method. In undigested samples, the highest antioxidant activity was obtained with the addition of quercetin to wheat, rice, and maize starch (6735.8 µmol Fe2+/g d.m., 678.8, 539.4 µmol Trolox/g d.m., respectively), and epigallocatechin gallate to wheat, rice, potato, and maize starch (692.1, 538.0, 625.8, 573.6 µmol Trolox/g d.m., respectively). In digested samples, the highest antioxidant activity was obtained with the addition of quercetin to wheat and rice starch (2104.5 µmol Fe2+/g d.m., 742.1 µmol Trolox/g d.m., respectively). In the case of the natant of the digested samples, the highest value was recorded for the addition of (+)-catechin to potato starch and trans-ferulic acid to maize starch (823.7 µmol Fe2+/g d.m., 245.1 µmol Trolox/g d.m., respectively). The addition of quercetin to wheat and rice starch and (+)-catechin to potato starch (0.239, 0.151, 0.085 g gallic acid/g d.m., respectively) resulted in the highest total polyphenol content. Furthermore, quercetin demonstrated the most significant level of cytotoxic activity against the tumor cell line Caco-2 (IC50 = 275.6 µg/mL; potato starch). Overall, quercetin was identified as the most significant or one of the most significant for all parameters evaluated.
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Kwaśny D., Borczak B., Sikora M., Kapusta-Duch J. Preliminary Study on the Influence of the Polyphenols of Different Groups on the Digestibility of Wheat Starch, Measured by the Content of Resistant Starch. Appl. Sci. 2022;12:10859. doi: 10.3390/app122110859. DOI
Kwaśny D., Borczak B., Kapusta-Duch J., Kron I. The Influence of Different Polyphenols on the Digestibility of Various Kinds of Starch and the Value of the Estimated Glycemic Index. Appl. Sci. 2024;14:8065. doi: 10.3390/app14178065. DOI
Ngo T.V., Kusumawardani S., Kunyanee K., Luangsakul N. Polyphenol-Modified Starches and Their Applications in the Food Industry: Recent Updates and Future Directions. Foods. 2022;11:3384. doi: 10.3390/foods11213384. PubMed DOI PMC
Types of Carbohydrates|ADA. [(accessed on 14 May 2025)]. Available online: https://diabetes.org/food-nutrition/understanding-carbs/types-carbohydrates.
Carbs and Diabetes|ADA. [(accessed on 14 May 2025)]. Available online: https://diabetes.org/food-nutrition/understanding-carbs.
Diabetes. [(accessed on 14 May 2025)]. Available online: https://www.who.int/news-room/fact-sheets/detail/diabetes.
Carbohydrates in the Diet|Oklahoma State University. [(accessed on 14 May 2025)]. Available online: https://extension.okstate.edu/fact-sheets/carbohydrates-in-the-diet.html.
Bashir K., Aggarwal M. Physicochemical, Structural and Functional Properties of Native and Irradiated Starch: A Review. J. Food Sci. Technol. 2019;56:513–523. doi: 10.1007/s13197-018-3530-2. PubMed DOI PMC
Food, Nutrition and Agriculture 24 Carbohydrates in Human Nutrition. [(accessed on 14 May 2025)]. Available online: https://www.fao.org/4/x2650t/x2650t02.htm.
Brand-Miller J., Buyken A.E. The Relationship between Glycemic Index and Health. Nutrients. 2020;12:536. doi: 10.3390/nu12020536. PubMed DOI PMC
International Tables of Glycemic Index and Glycemic Load Values: 2008|Diabetes Care|American Diabetes Association. [(accessed on 14 May 2025)]. Available online: https://diabetesjournals.org/care/article/31/12/2281/24911/International-Tables-of-Glycemic-Index-and. PubMed PMC
Giri S., Banerji A., Lele S.S., Ananthanarayan L. Starch Digestibility and Glycaemic Index of Selected Indian Traditional Foods: Effects of Added Ingredients. Int. J. Food Prop. 2017;20:S290–S305. doi: 10.1080/10942912.2017.1295387. DOI
Corgneau M., Gaiani C., Petit J., Nikolova Y., Banon S., Ritié-Pertusa L., Le D.T.L., Scher J. Digestibility of Common Native Starches with Reference to Starch Granule Size, Shape and Surface Features towards Guidelines for Starch-containing Food Products. Int. J. Food Sci. Technol. 2019;54:2132–2140. doi: 10.1111/ijfs.14120. DOI
Sies H., Berndt C., Jones D.P. Oxidative Stress. Annu. Rev. Biochem. 2017;86:715–748. doi: 10.1146/annurev-biochem-061516-045037. PubMed DOI
Influence of Technological Processing of Wheat Grain on Starch Digestibility and Resistant Starch Content—Štěrbová—2016—Starch—Stärke—Wiley Online Library. [(accessed on 14 May 2025)]. Available online: https://onlinelibrary.wiley.com/doi/full/10.1002/star.201500162. DOI
Ells L.J., Seal C.J., Kettlitz B., Bal W., Mathers J.C. Postprandial glycaemic, lipaemic and haemostatic responses to ingestion of rapidly and slowly digested starches in healthy young women. Br. J. Nutr. 2005;94:948–955. doi: 10.1079/BJN20051554. PubMed DOI
Seal C.J., Daly M.E., Thomas L.C., Bal W., Birkett A.M., Jeffcoat R., Mathers J.C. Postprandial carbohydrate metabolism in healthy subjects and those with type 2 diabetes fed starches with slow and rapid hydrolysis rates determined in vitro. Br. J. Nutr. 2003;90:853–864. doi: 10.1079/BJN2003972. PubMed DOI
Englyst H.N., Kingman S.M., Hudson G.J., Cummings J.H. Measurement of resistant starch in vitro and in vivo. Br. J. Nutr. 1996;75:749–755. doi: 10.1079/BJN19960178. PubMed DOI
Afandi F.A., Wijaya C.H., Faridah D.N., Suyatma N.E., Jayanegara A. Evaluation of Various Starchy Foods: A Systematic Review and Meta-Analysis on Chemical Properties Affecting the Glycemic Index Values Based on In Vitro and In Vivo Experiments. Foods. 2021;10:364. doi: 10.3390/foods10020364. PubMed DOI PMC
Gourineni V., Stewart M.L., Wilcox M.L., Maki K.C. Nutritional Bar with Potato-Based Resistant Starch Attenuated Post-Prandial Glucose and Insulin Response in Healthy Adults. Foods. 2020;9:1679. doi: 10.3390/foods9111679. PubMed DOI PMC
Biskup I., Golonka I., Gamian A., Sroka Z. Antioxidant activity of selected phenols estimated by ABTS and FRAP methods. Adv. Hyg. Exp. Med. Hig. Med. Dosw. 2013;67 doi: 10.5604/17322693.1066062. PubMed DOI
Korus J., Gumul D., Czechowska K. Effect of Extrusion on the Phenolic Composition and Antioxidant Activity of Dry Beans of Phaseolus vulgaris L. Food Technol. Biotechnol. 2007;45:139–146.
Harasym J., Oledzki R. Effect of fruit and vegetable antioxidants on total antioxidant capacity of blood plasma. Nutrition. 2014;30:511–517. doi: 10.1016/j.nut.2013.08.019. PubMed DOI
Han X., Shen T., Lou H. Dietary Polyphenols and Their Biological Significance. Int. J. Mol. Sci. 2007;8:950–988. doi: 10.3390/i8090950. DOI
Rudrapal M., Khairnar S.J., Khan J., Dukhyil A.B., Ansari M.A., Alomary M.N., Alshabrmi F.M., Palai S., Deb P.K., Devi R. Dietary Polyphenols and Their Role in Oxidative Stress-Induced Human Diseases: Insights Into Protective Effects, Antioxidant Potentials and Mechanism(s) of Action. Front. Pharmacol. 2022;13:806470. doi: 10.3389/fphar.2022.806470. PubMed DOI PMC
Elsayed Azab A., Adwas A., Ibrahim Elsayed A.S., Adwas A., Ibrahim Elsayed A.S., Quwaydir F.A. Oxidative stress and antioxidant mechanisms in human body. J. Appl. Biotechnol. Bioeng. 2019;6:43–47. doi: 10.15406/jabb.2019.06.00173. DOI
Manna P., Jain S.K. Obesity, Oxidative Stress, Adipose Tissue Dysfunction, and the Associated Health Risks: Causes and Therapeutic Strategies. Metab. Syndr. Relat. Disord. 2015;13:423–444. doi: 10.1089/met.2015.0095. PubMed DOI PMC
Adebooye O.C., Alashi A.M., Aluko R.E. A brief review on emerging trends in global polyphenol research. J. Food Biochem. 2018;42:e12519. doi: 10.1111/jfbc.12519. DOI
Sinha M., Sachan D.K., Bhattacharya R., Singh P., Parthasarathi R. ToxDP2 Database: Toxicity prediction of dietary polyphenols. Food Chem. 2022;370:131350. doi: 10.1016/j.foodchem.2021.131350. PubMed DOI
Majumdar S., Srirangam R. Solubility, Stability, Physicochemical Characteristics and In Vitro Ocular Tissue Permeability of Hesperidin: A Natural Bioflavonoid. Pharm. Res. 2009;26:1217–1225. doi: 10.1007/s11095-008-9729-6. PubMed DOI PMC
p-Coumaric Acid Datasheet. [(accessed on 7 April 2025)]. Available online: https://www.selleckchem.com/datasheet/p-coumaric-acid-S475902-DataSheet.html.
Trans-Ferulic Acid CAS#: 537-98-4. [(accessed on 7 April 2025)]. Available online: https://www.chemicalbook.com/ProductChemicalPropertiesCB3337152_EN.htm.
PubChem Quercetin. [(accessed on 7 April 2025)]; Available online: https://pubchem.ncbi.nlm.nih.gov/compound/5280343.
PubChem Kaempferol. [(accessed on 7 April 2025)]; Available online: https://pubchem.ncbi.nlm.nih.gov/compound/5280863.
(−)-Epigallocatechin Gallate|989-51-5. [(accessed on 7 April 2025)]. Available online: https://www.chemicalbook.com/ChemicalProductProperty_EN_CB2227188.htm.
Stasiłowicz-Krzemień A., Gołębiewski M., Płazińska A., Płaziński W., Miklaszewski A., Żarowski M., Adamska-Jernaś Z., Cielecka-Piontek J. The Systems of Naringenin with Solubilizers Expand Its Capability to Prevent Neurodegenerative Diseases. Int. J. Mol. Sci. 2022;23:755. doi: 10.3390/ijms23020755. PubMed DOI PMC
Cuevas-Valenzuela J., González-Rojas Á., Wisniak J., Apelblat A., Pérez-Correa J.R. Solubility of (+)-catechin in water and water-ethanol mixtures within the temperature range 277.6–331.2 K: Fundamental data to design polyphenol extraction processes. Fluid Phase Equilibria. 2014;382:279–285. doi: 10.1016/j.fluid.2014.09.013. DOI
Fernandes P.A.R., Coimbra M.A. The antioxidant activity of polysaccharides: A structure-function relationship overview. Carbohydr. Polym. 2023;314:120965. doi: 10.1016/j.carbpol.2023.120965. PubMed DOI
Fukumoto L.R., Mazza G. Assessing Antioxidant and Prooxidant Activities of Phenolic Compounds. J. Agric. Food Chem. 2000;48:3597–3604. doi: 10.1021/jf000220w. PubMed DOI
Chen J., Yang J., Ma L., Li J., Shahzad N., Kim C.K. Structure-antioxidant activity relationship of methoxy, phenolic hydroxyl, and carboxylic acid groups of phenolic acids. Sci. Rep. 2020;10:2611. doi: 10.1038/s41598-020-59451-z. PubMed DOI PMC
Robards K., Prenzler P.D., Tucker G., Swatsitang P., Glover W. Phenolic compounds and their role in oxidative processes in fruits. Food Chem. 1999;66:401–436. doi: 10.1016/S0308-8146(99)00093-X. DOI
Rice-Evans C.A., Miller N.J., Paganga G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic. Biol. Med. 1996;20:933–956. doi: 10.1016/0891-5849(95)02227-9. PubMed DOI
Cirillo G., Puoci F., Iemma F., Curcio M., Parisi O.I., Spizzirri U.G., Altimari I., Picci N. Starch-quercetin conjugate by radical grafting: Synthesis and biological characterization. Pharm. Dev. Technol. 2012;17:466–476. doi: 10.3109/10837450.2010.546413. PubMed DOI
Liu J., Wang X., Yong H., Kan J., Zhang N., Jin C. Preparation, characterization, digestibility and antioxidant activity of quercetin grafted Cynanchum auriculatum starch. Int. J. Biol. Macromol. 2018;114:130–136. doi: 10.1016/j.ijbiomac.2018.03.101. PubMed DOI
Lv X., Ye F., Li J., Ming J., Zhao G. Synthesis and characterization of a novel antioxidant RS4 by esterifying carboxymethyl sweetpotato starch with quercetin. Carbohydr. Polym. 2016;152:317–326. doi: 10.1016/j.carbpol.2016.07.023. PubMed DOI
Hu H., Yong H., Yao X., Yun D., Huang J., Liu J. Highly efficient synthesis and characterization of starch aldehyde-catechin conjugate with potent antioxidant activity. Int. J. Biol. Macromol. 2021;173:13–25. doi: 10.1016/j.ijbiomac.2021.01.119. PubMed DOI
Yong H., Hu H., Wang Z., Yun D., Kan J., Liu J. Structure, stability and antioxidant activity of dialdehyde starch grafted with epicatechin, epicatechin gallate, epigallocatechin and epigallocatechin gallate. J. Sci. Food Agric. 2022;102:6373–6386. doi: 10.1002/jsfa.12003. PubMed DOI
Shahidi F., Wanasundara P.K. Phenolic antioxidants. Crit. Rev. Food Sci. Nutr. 1992;32:67–103. doi: 10.1080/10408399209527581. PubMed DOI
Cuvelier M.-E., Richard H., Berset C. Comparison of the Antioxidative Activity of Some Acid-phenols: Structure-Activity Relationship. Biosci. Biotechnol. Biochem. 1992;56:324–325. doi: 10.1271/bbb.56.324. DOI
Deng N., Bian X., Luo S., Liu C., Hu X. The starch-polyphenol inclusion complex: Preparation, characterization and digestion. Food Biosci. 2023;53:102655. doi: 10.1016/j.fbio.2023.102655. DOI
Wu Y., Liu Y., Jia Y., Zhang H., Ren F. Formation and Application of Starch–Polyphenol Complexes: Influencing Factors and Rapid Screening Based on Chemometrics. Foods. 2024;13:1557. doi: 10.3390/foods13101557. PubMed DOI PMC
Wheat Starch-Tannic Acid Complexes Modulate Physicochemical and Rheological Properties of Wheat Starch and Its Digestibility—ScienceDirect. [(accessed on 15 May 2025)]. Available online: https://www.sciencedirect.com/science/article/pii/S0268005X21008754?via%3Dihub.
Amoako D.B., Awika J.M. Resistant starch formation through intrahelical V-complexes between polymeric proanthocyanidins and amylose. Food Chem. 2019;285:326–333. doi: 10.1016/j.foodchem.2019.01.173. PubMed DOI
Tan L., Kong L. Starch-guest inclusion complexes: Formation, structure, and enzymatic digestion. Crit. Rev. Food Sci. Nutr. 2020;60:780–790. doi: 10.1080/10408398.2018.1550739. PubMed DOI
Chang R., Xiong L., Li M., Wang Y., Lin M., Qiu L., Bian X., Sun C., Sun Q. Interactions between debranched starch and emulsifiers, polyphenols, and fatty acids. Int. J. Biol. Macromol. 2020;150:644–653. doi: 10.1016/j.ijbiomac.2020.02.130. PubMed DOI
Database on Polyphenol Content in Foods—Phenol-Explorer. [(accessed on 15 May 2025)]. Available online: http://phenol-explorer.eu/
Liu B., Zhong F., Yokoyama W., Huang D., Zhu S., Li Y. Interactions in starch co-gelatinized with phenolic compound systems: Effect of complexity of phenolic compounds and amylose content of starch. Carbohydr. Polym. 2020;247:116667. doi: 10.1016/j.carbpol.2020.116667. PubMed DOI
Du J., Yang Z., Xu X., Wang X., Du X. Effects of tea polyphenols on the structural and physicochemical properties of high-hydrostatic-pressure-gelatinized rice starch. Food Hydrocoll. 2019;91:256–262. doi: 10.1016/j.foodhyd.2019.01.035. DOI
Lea T. Caco-2 Cell Line. In: Verhoeckx K., Cotter P., López-Expósito I., Kleiveland C., Lea T., Mackie A., Requena T., Swiatecka D., Wichers H., editors. The Impact of Food Bioactives on Health: In vitro and ex vivo Models. Springer International Publishing; Cham, Switzerland: 2015. pp. 103–111. PubMed
Martínez-Maqueda D., Miralles B., Recio I. HT29 Cell Line. In: Verhoeckx K., Cotter P., López-Expósito I., Kleiveland C., Lea T., Mackie A., Requena T., Swiatecka D., Wichers H., editors. The Impact of Food Bioactives on Health: In Vitro and Ex Vivo Models. Springer International Publishing; Cham, Switzerland: 2015. pp. 113–124.
Strzelecka M., Wiatrak B., Jawień P., Czyżnikowska Ż., Świątek P. New Schiff bases derived from dimethylpyridine-1,2,4-triazole hybrid as cytotoxic agents targeting gastrointestinal cancers: Design, synthesis, biological evaluation and molecular docking studies. Bioorg. Chem. 2023;139:106758. doi: 10.1016/j.bioorg.2023.106758. PubMed DOI
Volstatova T., Marchica A., Hroncova Z., Bernardi R., Doskocil I., Havlik J. Effects of chlorogenic acid, epicatechin gallate, and quercetin on mucin expression and secretion in the Caco-2/HT29-MTX cell model. Food Sci. Nutr. 2019;7:492–498. doi: 10.1002/fsn3.818. PubMed DOI PMC
Schantz M., Mohn C., Baum M., Richling E. Antioxidative efficiency of an anthocyanin rich bilberry extract in the human colon tumor cell lines Caco-2 and HT-29. J. Berry Res. 2010;1:25–33. doi: 10.3233/BR-2010-003. DOI
Kuntz S., Wenzel U., Daniel H. Comparative analysis of the effects of flavonoids on proliferation, cytotoxicity, and apoptosis in human colon cancer cell lines. Eur. J. Nutr. 1999;38:133–142. doi: 10.1007/s003940050054. PubMed DOI
Ye Y.-S., Duan Y.-T., Zhou Z., Thepkaysone K., Douangdeuane B., Xu G. Structurally Diverse Cytotoxic Polyphenols from Garcinia gracilis. J. Nat. Prod. 2023;86:2206–2215. doi: 10.1021/acs.jnatprod.3c00498. PubMed DOI
Ramos S., Rodríguez-Ramiro I., Martín M.A., Goya L., Bravo L. Dietary flavanols exert different effects on antioxidant defenses and apoptosis/proliferation in Caco-2 and SW480 colon cancer cells. Toxicol. Vitr. 2011;25:1771–1781. doi: 10.1016/j.tiv.2011.09.007. PubMed DOI
Agullo G., Gamet-Payrastre L., Fernandez Y., Anciaux N., Demigné C., Rémésy C. Comparative effects of flavonoids on the growth, viability and metabolism of a colonic adenocarcinoma cell line (HT29 cells) Cancer Lett. 1996;105:61–70. doi: 10.1016/0304-3835(96)04262-0. PubMed DOI
Dihal A.A., Woutersen R.A., van Ommen B., Rietjens I.M.C.M., Stierum R.H. Modulatory effects of quercetin on proliferation and differentiation of the human colorectal cell line Caco-2. Cancer Lett. 2006;238:248–259. doi: 10.1016/j.canlet.2005.07.007. PubMed DOI
Fernández-Blanco C., Font G., Ruiz M.-J. Role of quercetin on Caco-2 cells against cytotoxic effects of alternariol and alternariol monomethyl ether. Food Chem. Toxicol. 2016;89:60–66. doi: 10.1016/j.fct.2016.01.011. PubMed DOI
Raja S.B., Rajendiran V., Kasinathan N.K., Venkatabalasubramanian S., Murali M.R., Devaraj H., Devaraj S.N. Differential cytotoxic activity of Quercetin on colonic cancer cells depends on ROS generation through COX-2 expression. Food Chem. Toxicol. 2017;106:92–106. doi: 10.1016/j.fct.2017.05.006. PubMed DOI
Uesato S., Kitagawa Y., Kamishimoto M., Kumagai A., Hori H., Nagasawa H. Inhibition of green tea catechins against the growth of cancerous human colon and hepatic epithelial cells. Cancer Lett. 2001;170:41–44. doi: 10.1016/S0304-3835(01)00571-7. PubMed DOI
Benzie I.F., Strain J.J. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Anal. Biochem. 1996;239:70–76. doi: 10.1006/abio.1996.0292. PubMed DOI
Brand-Williams W., Cuvelier M.E., Berset C. Use of a free radical method to evaluate antioxidant activity. LWT Food Sci. Technol. 1995;28:25–30. doi: 10.1016/S0023-6438(95)80008-5. DOI
Hillis W.E., Swain T. The phenolic constituents of Prunus domestica. II.—The analysis of tissues of the Victoria plum tree. J. Sci. Food Agric. 1959;10:135–144. doi: 10.1002/jsfa.2740100211. DOI
Mosmann T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods. 1983;65:55–63. doi: 10.1016/0022-1759(83)90303-4. PubMed DOI