Biotechnological processes as means to increase the accessibility and antioxidant activity of phenolic compounds from bread wheat and spelt grains

Authors

  • Marjeta MENCIN Univerza v Ljubljani, Biotehniška fakulteta, Oddelek za živilstvo, Ljubljana

DOI:

https://doi.org/10.14720/aas.2024.120.2.17019

Keywords:

phenolic compounds, antioxidant activity, accessibility, germination, fermentation, enzymatic treatment, LC-MS/MS

Abstract

Cereal grains, especially bran, are a rich source of phenolic compounds with antioxidant activity. The potential positive effects of phenolics from whole grains of spelt and  bread wheat on human health are limited by the poor bioaccessibility and bioavailability of their bound phenolics. Studies have shown that biotechnological processes (germination/fermentation/enzymatic treatment) are an effective strategy for improving the release of bound phenolics from the cell wall matrix of cereal grains. In this review article, the effects of biotechnological processes on the composition, antioxidant activity and bioaccessibility of phenolics from spelt and bread wheat grains are discussed in detail. Existing research indicates the presence of a different phenolics in spelt and bread wheat grains, making whole grains excellent for improving nutritional value of products. It has been shown that biotechnological processes can effectively increase the content of bioaccessible and bioavailable phenolics in cereal grains, which enables improved in vitro antioxidant activity. Currently, there is a lack of in vivo studies to confirm the findings obtained in vitro, so in vivo studies to determine the biological activity of phenolic compounds from pre-treated grains will be crucial in the future.

References

Acosta-Estrada B. A., Gutiérrez-Uribe J. A., Serna-Saldívar S. O. (2014). Bound phenolics in foods, a review. Food Chemistry, 152, 46–55. https://doi.org/10.1016/j.foodchem.2013.11.093

Adebo O. A., Gabriela Medina-Meza I. (2020). Impact of fermentation on the phenolic compounds and antioxidant activity of whole cereal grains: a mini review. Molecules, 25(4), 927, 9 str. https://doi.org/10.3390/molecules25040927

Adom K. K., Liu R. H. (2002). Antioxidant activity of grains. Journal of Agricultural and Food Chemistry, 50(21), 6182–6187. https://doi.org/10.1021/jf0205099

Angelino D., Cossu M., Marti A., Zanoletti M., Chiavaroli L., Brighenti F., Rio D. D., Martini D. (2017). Bioaccessibility and bioavailability of phenolic compounds in bread: a review. Food & Function, 8(7), 2368–2393. https://doi.org/10.1039/C7FO00574A

Anson N. M., Selinheimo E., Havenaar R., Aura A.-M., Mattila I., Lehtinen P., Bast A., Poutanen K., Haenen G. R. M. M. (2009). Bioprocessing of wheat bran improves in vitro bioaccessibility and colonic metabolism of phenolic compounds. Journal of Agricultural and Food Chemistry, 57(14), 6148–6155. https://doi.org/10.1021/jf900492h

Azmir J., Zaidul I. S. M., Rahman M. M., Sharif K. M., Mohamed A., Sahena F., Jahurul M. H. A., Ghafoor K., Norulaini N. A. N., Omar A. K. M. (2013). Techniques for extraction of bioactive compounds from plant materials: a review. Journal of Food Engineering, 117(4), 426–436. https://doi.org/10.1016/j.jfoodeng.2013.01.014

Bei Q., Chen G., Lu F., Wu S., Wu Z. (2018). Enzymatic action mechanism of phenolic mobilization in oats (Avena sativa L.) during solid-state fermentation with Monascus anka. Food Chemistry, 245, 297–304. https://doi.org/10.1016/j.foodchem.2017.10.086

Bojňanská T., Frančáková H. (2011). The use of spelt wheat (Triticum spelta L.) for baking applications. Plant, Soil and Environment, 48(4), 141–147. https://doi.org/10.17221/4212-PSE

Bonafaccia G., Galli V., Francisci R., Mair V., Skrabanja V., Kreft I. (2000). Characteristics of spelt wheat products and nutritional value of spelt wheat-based bread. Food Chemistry, 68(4), 437–441. https://doi.org/10.1016/S0308-8146(99)00215-0

Boskov Hansen H., Andreasen M., Nielsen M., Larsen L., Knudsen B. K., Meyer A., Christensen L., Hansen Å. (2002). Changes in dietary fibre, phenolic acids and activity of endogenous enzymes during rye bread-making. European Food Research and Technology, 214(1), 33–42. https://doi.org/10.1007/s00217-001-0417-6

Brodkorb A., Egger L., Alminger M., Alvito P., Assunção R., Ballance S., Bohn T., Bourlieu-Lacanal C., Boutrou R., Carrière F., Clemente A., Corredig M., Dupont D., Dufour C., Edwards C., Golding M., Karakaya S., Kirkhus B., Le Feunteun S., Lesmes U., Macierzanka A., Mackie R. A., Martins C., Marze S., McClements J. D., Ménard O., Minekus M., Portmann R., Santos C. N., Souchon I., Singh R. P., Vegarud G. E., Wickham M. S. J., Weitschies W., Recio I. (2019). INFOGEST static in vitro simulation of gastrointestinal food digestion. Nature Protocols, 14(4), 991–1014. https://doi.org/10.1038/s41596-018-0119-1

Chait Y. A., Gunenc A., Bendali F., Hosseinian F. (2020). Simulated gastrointestinal digestion and in vitro colonic fermentation of carob polyphenols: bioaccessibility and bioactivity. LWT, 117, 108623, 10 str. https://doi.org/10.1016/j.lwt.2019.108623

Chavarín-Martínez C. D., Gutiérrez-Dorado R., Perales-Sánchez J. X. K., Cuevas-Rodríguez E. O., Milán-Carrillo J., Reyes-Moreno C. (2019). Germination in optimal conditions as effective strategy to improve nutritional and nutraceutical value of underutilized Mexican blue maize seeds. Plant Foods for Human Nutrition, 74(2), 192–199. https://doi.org/10.1007/s11130-019-00717-x

Chen Z. Ma Y., Yang R., Gu Z., Wang P. (2019). Effects of exogenous Ca2+ on phenolic accumulation and physiological changes in germinated wheat (Triticum aestivum L.) under UV-B radiation. Food Chemistry, 288, 368–376. https://doi.org/10.1016/j.foodchem.2019.02.131

Chen Z., Wang P., Weng Y., Ma Y., Gu Z., Yang R. (2017). Comparison of phenolic profiles, antioxidant capacity and relevant enzyme activity of different Chinese wheat varieties during germination. Food Bioscience, 20, 159–167. https://doi.org/10.1016/j.fbio.2017.10.004

Chrzanowski G. (2020). Saccharomyces cerevisiae—an interesting producer of bioactive plant polyphenolic metabolites. International Journal of Molecular Sciences, 21(19), 7343. https://doi.org/10.3390/ijms21197343

Costabile A., Klinder A., Fava F., Napolitano A., Fogliano V., Leonard C., Gibson G. R., Tuohy K. M. (2008). Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study. British Journal of Nutrition, 99(1), 110–120. https://doi.org/10.1017/S0007114507793923

Donkor O. N., Stojanovska L., Ginn P., Ashton J., Vasiljevic T. (2012). Germinated grains – Sources of bioactive compounds. Food Chemistry, 135(3), 950–959. https://doi.org/10.1016/j.foodchem.2012.05.058

Đorđević T. M., Šiler-Marinković S. S., Dimitrijević-Branković S. I. (2010). Effect of fermentation on antioxidant properties of some cereals and pseudo cereals. Food Chemistry, 119(3), 957–963. https://doi.org/10.1016/j.foodchem.2009.07.049

Escarnot E., Aguedo M., Paquot M. (2012). Enzymatic hydrolysis of arabinoxylans from spelt bran and hull. Journal of Cereal Science, 55(2), 243–253. https://doi.org/10.1016/j.jcs.2011.12.009

Falcinelli B., Sileoni V., Marconi O., Perretti G., Quinet M., Lutts S., Benincasa P. (2017). Germination under moderate salinity increases phenolic content and antioxidant activity in rapeseed (Brassica napus var. oleifera Del.) sprouts. Molecules, 22(8), 1377, 13 str. https://doi.org/10.3390/molecules22081377

FAOSTAT. (2023). Crop statistics. https://www.fao.org/faostat/en/#data/QCL (accessible 8.12.2023)

Faulds C. B., Mandalari G., LoCurto R., Bisignano G., Waldron K. W. (2004). Arabinoxylan and mono- and dimeric ferulic acid release from brewers grain and wheat bran by feruloyl esterases and glycosyl hydrolases from Humicola insolens. Applied Microbiology and Biotechnology, 64(5), 644–650. https://doi.org/10.1007/s00253-003-1520-3

Ferri M., Happel A., Zanaroli G., Bertolini M., Chiesa S., Commisso M., Guzzo F., Tassoni A. (2020). Advances in combined enzymatic extraction of ferulic acid from wheat bran. New Biotechnology, 56, 38–45. https://doi.org/10.1016/j.nbt.2019.10.010

Gan R.-Y., Lui W.-Y., Wu K., Chan C.-L., Dai S.-H., Sui Z.-Q., Corke H. (2017). Bioactive compounds and bioactivities of germinated edible seeds and sprouts: an updated review. Trends in Food Science & Technology, 59, 1–14. https://doi.org/10.1016/j.tifs.2016.11.010

Gani A., Sm W., Fa M. (2012). Whole-grain cereal bioactive compounds and their health benefits: a review. Journal of Food Processing & Technology, 3(3), 146, 10 str. https://doi.org/10.4172/2157-7110.1000146

Gänzle M. G. (2014). Enzymatic and bacterial conversions during sourdough fermentation. Food Microbiology, 37, 2–10. https://doi.org/10.1016/j.fm.2013.04.007

Geisslitz S., Longin C. F. H., Scherf K. A., Koehler P. (2019). Comparative study on gluten protein composition of ancient (einkorn, emmer and spelt) and modern wheat species (durum and common wheat). Foods, 8(9), 409. https://doi.org/10.3390/foods8090409

Hübner F., Arendt E. K. (2013). Germination of cereal grains as a way to improve the nutritional value: a review. Critical Reviews in Food Science and Nutrition, 53(8), 853–861. https://doi.org/10.1080/10408398.2011.562060

Katina K., Liukkonen K.-H., Kaukovirta-Norja A., Adlercreutz H., Heinonen S.-M., Lampi A.-M., Pihlava J.-M., Poutanen K. (2007). Fermentation-induced changes in the nutritional value of native or germinated rye. Journal of Cereal Science, 46(3), 348–355. https://doi.org/10.1016/j.jcs.2007.07.006

Kim M. J., Kwak H. S., Kim S. S. (2018). Effects of germination on protein, γ-aminobutyric acid, phenolic acids, and antioxidant capacity in wheat. Molecules, 23(9), 2244, 13 str. https://doi.org/10.3390/molecules23092244

Konopka I., Tańska M., Faron A., Czaplicki S. (2014). Release of free ferulic acid and changes in antioxidant properties during the wheat and rye bread making process. Food Science and Biotechnology, 23(3), 831–840. https://doi.org/10.1007/s10068-014-0112-6

Li M., Bai Q., Zhou J., de Souza T. S. P., Suleria H. A. R. (2022). In vitro gastrointestinal bioaccessibility, bioactivities and colonic fermentation of phenolic compounds in different vigna beans. Foods, 11(23), 3884. https://doi.org/10.3390/foods11233884

Lima K., Silva O., Figueira M. E., Pires C., Cruz D., Gomes S., Maurício E. M., Duarte M. P. (2019). Influence of the in vitro gastrointestinal digestion on the antioxidant activity of Artemisia gorgonum Webb and Hyptis pectinata (L.) Poit. infusions from Cape Verde. Food Research International, 115, 150–159. https://doi.org/10.1016/j.foodres.2018.08.029

Ma Y., Wang P., Wang M., Sun M., Gu Z., Yang R. (2019). GABA mediates phenolic compounds accumulation and the antioxidant system enhancement in germinated hulless barley under NaCl stress. Food Chemistry, 270, 593–601. https://doi.org/10.1016/j.foodchem.2018.07.092

Mathew S., Abraham T. E. (2004). Ferulic acid: an antioxidant found naturally in plant cell walls and feruloyl esterases involved in its release and their applications. Critical Reviews in Biotechnology, 24(2–3), 59–83. https://doi.org/10.1080/07388550490491467

Mencin M., Abramovič H., Jamnik P., Mikulič Petkovšek M., Veberič R., Terpinc P. (2021). Abiotic stress combinations improve the phenolics profiles and activities of extractable and bound antioxidants from germinated spelt (Triticum spelta L.) seeds. Food Chemistry, 344, 128704, 12 str. https://doi.org/10.1016/j.foodchem.2020.128704

Mencin M., Jamnik P., Mikulič Petkovšek M., Veberič R., Terpinc P. (2022a). Improving accessibility and bioactivity of raw, germinated and enzymatic-treated spelt (Triticum spelta L.) seed antioxidants by fermentation. Food Chemistry, 394, 133483, 12 str. https://doi.org/10.1016/j.foodchem.2022.133483

Mencin M., Jamnik P., Mikulič Petkovšek M., Veberič R., Terpinc P. (2022b). Enzymatic treatments of raw, germinated and fermented spelt (Triticum spelta L.) seeds improve accessibility and antioxidant activity of their phenolics. LWT, 169, 114046, 13 str. https://doi.org/10.1016/j.lwt.2022.114046

Mencin M., Mikulič Petkovšek M., Veberič R., Terpinc P. (2022c). Simulated gastrointestinal digestion of bioprocessed spelt seeds: bioaccessibility and bioactivity of phenolics. Antioxidants, 11(9), 1703, 20 str. https://doi.org/10.3390/antiox11091703

Montemurro M., Pontonio E., Gobbetti M., Rizzello C. G. (2019). Investigation of the nutritional, functional and technological effects of the sourdough fermentation of sprouted flours. International Journal of Food Microbiology, 302, 47–58. https://doi.org/10.1016/j.ijfoodmicro.2018.08.005

Moore J., Cheng Z., Su L., Yu L. (2006). Effects of solid-state enzymatic treatments on the antioxidant properties of wheat bran. Journal of Agricultural and Food Chemistry, 54(24), 9032–9045. https://doi.org/10.1021/jf0616715

Ortega N., Macià A., Romero M.-P., Reguant J., Motilva M.-J. (2011). Matrix composition effect on the digestibility of carob flour phenols by an in-vitro digestion model. Food Chemistry, 124(1), 65–71. https://doi.org/10.1016/j.foodchem.2010.05.105

Pang Y., Ahmed S., Xu Y., Beta T., Zhu Z., Shao Y., Bao J. (2018). Bound phenolic compounds and antioxidant properties of whole grain and bran of white, red and black rice. Food Chemistry, 240, 212–221. https://doi.org/10.1016/j.foodchem.2017.07.095

Paucar-Menacho L. M., Martínez-Villaluenga C., Dueñas M., Frias J., Peñas E. (2017). Optimization of germination time and temperature to maximize the content of bioactive compounds and the antioxidant activity of purple corn (Zea mays L.) by response surface methodology. LWT - Food Science and Technology, 76, 236–244. https://doi.org/10.1016/j.lwt.2016.07.064

Peixoto Araujo N. M., Pereira G. A., Arruda H. S., Prado L. G., Ruiz A. L. T. G., Eberlin M. N., Castro R. J. S., Pastore G. M. (2019). Enzymatic treatment improves the antioxidant and antiproliferative activities of Adenanthera pavonina L. seeds. Biocatalysis and Agricultural Biotechnology, 18, 101002, 7 str. https://doi.org/10.1016/j.bcab.2019.01.040

Pruska-Kedzior A., Kedzior Z., Klockiewicz-Kaminska E. (2008). Comparison of viscoelastic properties of gluten from spelt and common wheat. European Food Research and Technology, 227(1), 199–207. https://doi.org/10.1007/s00217-007-0710-0

Rakariyatham K., Liu X., Liu Z., Wu S., Shahidi F., Zhou D., Zhu B. (2020). Improvement of phenolic contents and antioxidant activities of longan (Dimocarpus longan) peel extracts by enzymatic treatment. Waste and Biomass Valorization, 11(8), 3987–4002. https://doi.org/10.1007/s12649-019-00723-9

Ruibal-Mendieta N. L., Delacroix D. L., Mignolet E., Pycke J.-M., Marques C., Rozenberg R., Petitjean G., Habib-Jiwan J.-L., Meurens M., Quetin-Leclercq J., Delzenne N. M., Larondelle Y. (2005). Spelt (Triticum aestivum ssp. spelta) as a source of breadmaking flours and bran naturally enriched in oleic acid and minerals but not phytic acid. Journal of Agricultural and Food Chemistry, 53(7), 2751–2759. https://doi.org/10.1021/jf048506e

Sancho A. I., Bartolomé B., Gómez-Cordovés C., Williamson G., Faulds C. B. (2001). Release of ferulic acid from cereal residues by barley enzymatic extracts. Journal of Cereal Science, 34(2), 173–179. https://doi.org/10.1006/jcrs.2001.0386

Shahidi F., Yeo J. (2016). Insoluble-bound phenolics in food. Molecules, 21(9), 1216, 22 str. https://doi.org/10.3390/molecules21091216

Singh A., Sharma S. (2017). Bioactive components and functional properties of biologically activated cereal grains: a bibliographic review. Critical Reviews in Food Science and Nutrition, 57(14), 3051–3071. https://doi.org/10.1080/10408398.2015.1085828

Singh A., Sharma V., Banerjee R., Sharma S., Kuila A. (2016). Perspectives of cell-wall degrading enzymes in cereal polishing. Food Bioscience, 15, 81–86. https://doi.org/10.1016/j.fbio.2016.05.003

Spaggiari M., Ricci A., Calani L., Bresciani L., Neviani E., Dall’Asta C., Lazzi C., Galaverna G. (2020). Solid state lactic acid fermentation: a strategy to improve wheat bran functionality. LWT, 118, 108668, 9 str. https://doi.org/10.1016/j.lwt.2019.108668

Terpinc P. (2019). Vezane fenolne spojine polnozrnatih žitnih pripravkov kot sestavina funkcionalnih živil: drugi del. Acta agriculturae Slovenica, 114(2), 279–291. https://doi.org/10.14720/aas.2019.114.2.12

Terpinc P., Abramovič H. (2010). A kinetic approach for evaluation of the antioxidant activity of selected phenolic acids. Food Chemistry, 121(2), 366–371. https://doi.org/10.1016/j.foodchem.2009.12.037

Terpinc P., Cigić B., Polak T., Hribar J., Požrl T. (2016). LC–MS analysis of phenolic compounds and antioxidant activity of buckwheat at different stages of malting. Food Chemistry, 210, 9–17. https://doi.org/10.1016/j.foodchem.2016.04.030

Ti H., Zhang R., Zhang M., Li Q., Wei Z., Zhang Y., Tang X., Deng Y., Liu L., Ma Y. (2014). Dynamic changes in the free and bound phenolic compounds and antioxidant activity of brown rice at different germination stages. Food Chemistry, 161, 337–344. https://doi.org/10.1016/j.foodchem.2014.04.024

Vitaglione P., Napolitano A., Fogliano V. (2008). Cereal dietary fibre: a natural functional ingredient to deliver phenolic compounds into the gut. Trends in Food Science & Technology, 19(9), 451–463. https://doi.org/10.1016/j.tifs.2008.02.005

Wang J., Chatzidimitriou E., Wood L., Hasanalieva G., Markellou E., Iversen P. O., Seal C., Baranski M., Vigar V., Ernst L., Willson A., Thapa M., Barkla B. J., Leifert C., Rempelos L. (2020). Effect of wheat species (Triticum aestivum vs T. spelta), farming system (organic vs conventional) and flour type (wholegrain vs white) on composition of wheat flour – Results of a retail survey in the UK and Germany – 2. Antioxidant activity, and phenolic and mineral content. Food Chemistry: X, 6, 100091, 10 str. https://doi.org/10.1016/j.fochx.2020.100091

Wang T., He F., Chen G. (2014). Improving bioaccessibility and bioavailability of phenolic compounds in cereal grains through processing technologies: a concise review. Journal of Functional Foods, 7, 101–111. https://doi.org/10.1016/j.jff.2014.01.033

Xiang N., Guo X., Liu F., Li Q., Hu J., Brennan C. S. (2017). Effect of light- and dark-germination on the phenolic biosynthesis, phytochemical profiles, and antioxidant activities in sweet corn (Zea mays L.) sprouts. International Journal of Molecular Sciences, 18(6), 1246, 13 str. https://doi.org/10.3390/ijms18061246

Xu J. G., Tian C. R., Hu Q. P., Luo J. Y., Wang X. D., Tian X. D. (2009). Dynamic changes in phenolic compounds and antioxidant activity in oats (Avena nuda L.) during steeping and germination. Journal of Agricultural and Food Chemistry, 57(21), 10392–10398. https://doi.org/10.1021/jf902778j

Xu M., Rao J., Chen B. (2020). Phenolic compounds in germinated cereal and pulse seeds: classification, transformation, and metabolic process. Critical Reviews in Food Science and Nutrition, 60(5), 740–759. https://doi.org/10.1080/10408398.2018.1550051

Yang T. K. B., Ooraikul F. (2001). Studies on germination conditions and antioxidant contents of wheat grain. International Journal of Food Sciences and Nutrition, 52(4), 319–330. https://doi.org/10.1080/09637480120057567

Ydjedd S., Bouriche S., López-Nicolás R., Sánchez-Moya T., Frontela-Saseta C., Ros-Berruezo G., Rezgui F., Louaileche H., Kati, D.-E. (2017). Effect of in vitro gastrointestinal digestion on encapsulated and nonencapsulated phenolic compounds of carob (Ceratonia siliqua L.) pulp extracts and their antioxidant capacity. Journal of Agricultural and Food Chemistry, 65(4), 827–835. https://doi.org/10.1021/acs.jafc.6b05103

Zeng Z., Liu C., Luo S., Chen J., Gong E. (2016). The profile and bioaccessibility of phenolic compounds in cereals influenced by improved extrusion cooking treatment. PLOS ONE, 11(8), e0161086, 11 str. https://doi.org/10.1371/journal.pone.0161086

Zörb C., Betsche T., Langenkämper G., Zapp J., Seifert M. (2007). Free sugars in spelt wholemeal and flour. Journal of Applied Botany and Food Quality, 81(2), 172–174.

Žilić S., Delić N., Basić Z., Ignjatović-Micić D., Janković M., Vančetović J. (2015). Effects of alkaline cooking and sprouting on bioactive compounds, their bioavailability and relation to antioxidant capacity of maize flour. Journal of Food & Nutrition Research, 54(2), 155–164.

Živković, A., Gođevac, D., Cigić, B., Polak, T., & Požrl, T. (2023). Identification and quantification of selected benzoxazinoids and phenolics in germinated spelt (Triticum spelta). Foods, 12(9), 9. https://doi.org/10.3390/foods12091769

Downloads

Published

16. 07. 2024

Issue

Section

Review Article

How to Cite

MENCIN, M. (2024). Biotechnological processes as means to increase the accessibility and antioxidant activity of phenolic compounds from bread wheat and spelt grains. Acta Agriculturae Slovenica, 120(2), 1–10. https://doi.org/10.14720/aas.2024.120.2.17019