Enhancement in Bioaccessibility and Bioavailability of Phenolic Compounds during Black Glutinous Rice Tape Fermentation

https://doi.org/10.22146/agritech.92729

Mita Nurul Azkia(1), Widiastuti Setyaningsih(2), Yunika Mayangsari(3), Muhammad Nur Cahyanto(4*)

(1) Department of Agricultural Products Technology, Faculty of Agricultural Technology, Universitas Semarang, Semarang, Central Java 50196
(2) Departement of Food and Agricultural Product Technology, Faculty of Agricultural Technology, Universitas Gadjah Mada, Jl. Flora No. 1, Bulaksumur, Yogyakarta 55281
(3) Departement of Food and Agricultural Product Technology, Faculty of Agricultural Technology, Universitas Gadjah Mada, Jl. Flora No. 1, Bulaksumur, Yogyakarta 55281
(4) Departement of Food and Agricultural Product Technology, Faculty of Agricultural Technology, Universitas Gadjah Mada, Jl. Flora No. 1, Bulaksumur, Yogyakarta 55281
(*) Corresponding Author

Abstract


Black glutinous rice (Oryza sativa var. glutinosa) tape fermented with various yeast, mold, and bacteria is often rich in phenolics compounds and can contribute positively to health through its antioxidants activity. Despite the potential, these compounds have limited bioavailability value due to their structure, degree of glycosylation or polymerization, and interactions with other components. Therefore, this study aims to determine the effect of fermentation on bioavailability and bioaccessibility of phenolics compounds in black glutinous rice tape. During the procedures, cooked black glutinous rice was inoculated with ragi tape for 72 hours. Sampling was then performed every 24 hours to analyze bioaccessibility of phenolics compounds, flavonoids, and antioxidants activity. Subsequently, absorption was carried out using an everted gut sac model. The results showed that phenolics compounds were released from the food matrix during gastric and small intestine digestion. Fermentation was shown to increase the content of accessible phenolics compounds from 19.89% to 27.31%, flavonoids from 68.88% to 81.72%, and antioxidants activity from 13.56% to 22.89%. During fermentation, the highest increments were obtained after 72 hours, with 27.31% for total phenolics compounds, 81.72% for flavonoid compounds, and 22.89% for antioxidants activity. The products obtained after 72 hours of fermentation exhibited significantly highest absorption, but no significant differences were observed between the duodenum and ileum segments. The absorption of these compounds in the jejunum from the extract was significantly higher in fermented samples. Therefore, fermentation significantly enhanced bioavailability of phenolics compounds in black glutinous rice tape.

Keywords


Antioxidants; bioavailability; black glutinous rice; phenolics; tape

Full Text:

PDF


References

Abduh, M. Y., Ramadhan, C. R., Fadhlilah, A. P., Abdul, S. D. N., & Burhan, K. H. (2022). Solid-state fermentation of groundnut (Arachis hypogaea) shell using Trichoderma sp., tape yeast, and tempeh yeast to produce cellulase. Journal of Applied Biology and Biotechnology, 10(4), 153–160. https://doi.org/10.7324/JABB.2022.100421

Adebo, O. A., & Medina-Meza, I. G. (2020). Impact of fermentation on the phenolic compounds and antioxidants activity of whole cereal grains: a mini review. Molecules, 25(4), 1–19. https://doi.org/10.3390/molecules25040927

Arruda, H. S., Pereira, G. A., de Morais, D. R., Eberlin, M. N., & Pastore, G. M. (2018). Determination of free, esterified, glycosylated and insoluble-bound phenolics composition in the edible part of araticum fruit (Annona crassiflora Mart.) and its by-products by HPLC-ESI-MS/MS. Food Chemistry, 245, 738–749. https://doi.org/10.1016/j.foodchem.2017.11.120

Arts, M. J. T. J., Haenen, G. R. M. M., Wilms, L. C., Beetstra, S. A. J. N., Heijnen, C. G. M., Voss, H. P., & Bast, A. (2002). Interactions between flavonoids and proteins: Effect on the total antioxidants capacity. Journal of Agricultural and Food Chemistry, 50(5), 1184–1187. https://doi.org/10.1021/jf010855a

Aryanta, W. R. (2000). Traditional fermented foods in Indonesia. Japanese Journal of Lactic Acid Bacteria, 10(2), 90–102. https://doi.org/10.4109/jslab1997.10.90

Azkia, M. N., Cahyanto, M. N., Mayangsari, Y., Briliantama, A., Palma, M., & Setyaningsih, W. (2023). Enhancement of phenolics profile and antioxidants activity of black glutinous rice (Oryza sativa var. glutinosa) due to tape fermentation. Arabian Journal of Chemistry, 16(11). https://doi.org/10.1016/j.arabjc.2023.105275

Babotă, M., Frumuzachi, O., Gâvan, A., Iacoviță, C., Pinela, J., Barros, L., Ferreira, I. C. F. R., Zhang, L., Lucini, L., Rocchetti, G., Tanase, C., Crișan, G., & Mocan, A. (2022). Optimized ultrasound-assisted extraction of phenolic compounds from Thymus comosus Heuff. ex Griseb. et Schenk (wild thyme) and their bioactive potential. Ultrasonics Sonochemistry, 84, 1–10. https://doi.org/10.1016/j.ultsonch.2022.105954

Balakrishnan, G., & Schneider, R. G. (2020). Quinoa flavonoids and their bioaccessibility during in vitro gastrointestinal digestion. Journal of Cereal Science, 9. https://doi.org/10.1016/j.jcs.2020.103070

Berton, A., Rouvellac, S., Robert, B., Rousseau, F., Lopez, C., & Crenon, I. (2012). Effect of the size and interface composition of milk fat globules on their in vitro digestion by the human pancreatic lipase: Native versus homogenized milk fat globules. Food Hydrocolloids, 29(1), 123–134. https://doi.org/10.1016/j.foodhyd.2012.02.016

Brand-Williams, W., Cuvelier, M. E., & Berset, C. (1995). Use of a free radical method to evaluate antioxidants activity. LWT - Food Science and Technology, 28(1), 25–30. https://doi.org/10.1016/S0023-6438(95)80008-5

Cañas, S., Rebollo-Hernanz, M., Braojos, C., Benítez, V., Ferreras-Charro, R., Dueñas, M., Aguilera, Y., & Martín-Cabrejas, M. A. (2022). Understanding the gastrointestinal behavior of the coffee pulp phenolics compounds under simulated conditions. Antioxidants, 11(9). https://doi.org/10.3390/antiox11091818

Casteleyn, C., Rekecki, A., Van Der Aa, A., Simoens, P., & Van Den Broeck, W. (2010). Surface area assessment of the murine intestinal tract as a prerequisite for oral dose translation from mouse to man. Laboratory Animals, 44(3), 176–183. https://doi.org/10.1258/la.2009.009112

Cervantes, L., Martínez-Ferri, E., Soria, C., & Ariza, M. T. (2020). Bioavailability of phenolic compounds in strawberry, raspberry and blueberry: Insights for breeding programs. Food Bioscience, 37, 100680. https://doi.org/10.1016/j.fbio.2020.100680

Chen, Y., Ma, Y., Dong, L., Jia, X., Liu, L., Huang, F., Chi, J., Xiao, J., Zhang, M., & Zhang, R. (2019). Extrusion and fungal fermentation change the profile and antioxidants activity of free and bound phenolics in rice bran together with the phenolics bioaccessibility. Lwt, 115. https://doi.org/10.1016/j.lwt.2019.108461

Cosme, P., Rodríguez, A. B., Espino, J., & Garrido, M. (2020). Plant phenolics: bioavailability as a key determinant of their potential health-promoting applications. Antioxidants, 9(12), 1–20. https://doi.org/10.3390/antiox9121263

Cuvas-Limon, R. B., Ferreira-Santos, P., Cruz, M., Teixeira, J. A., Belmares, R., & Nobre, C. (2022). Effect of gastrointestinal digestion on the bioaccessibility of phenolic compounds and antioxidants activity of fermented aloe vera juices. Antioxidants, 11(12). https://doi.org/10.3390/antiox11122479

Day, A. J., Cañada, F. J., Díaz, J. C., Kroon, P. A., McLauchlan, R., Faulds, C. B., Plumb, G. W., Morgan, M. R. A., & Williamson, G. (2000). Dietary flavonoid and isoflavone glycosides are hydrolysed by the lactase site of lactase phlorizin hydrolase. FEBS Letters, 468(2–3), 166–170. https://doi.org/10.1016/S0014-5793(00)01211-4

Gawlik-Dziki, U., Dziki, D., Baraniak, B., & Lin, R. (2009). The effect of simulated digestion in vitro on bioactivity of wheat bread with Tartary buckwheat flavones addition. Lwt, 42(1), 137–143. https://doi.org/10.1016/j.lwt.2008.06.009

Guo, N., Zhu, Y. W., Jiang, Y. W., Li, H. K., Liu, Z. M., Wang, W., Shan, C. H., & Fu, Y. J. (2020). Improvement of flavonoid aglycone and biological activity of mulberry leaves by solid-state fermentation. Industrial Crops and Products, 148(November 2019). https://doi.org/10.1016/j.indcrop.2020.112287

Janarny, G., & Gunathilake, K. D. P. P. (2020). Changes in rice bran bioactives, their bioactivity, bioaccessibility and bioavailability with solid-state fermentation by Rhizopus oryzae. Biocatalysis and Agricultural Biotechnology, 23, 1–9. https://doi.org/10.1016/j.bcab.2020.101510

Kamiloglu, S., Tomas, M., Ozdal, T., & Capanoglu, E. (2021). Effect of food matrix on the content and bioavailability of flavonoids. Trends in Food Science and Technology, 117, 15–33. https://doi.org/10.1016/j.tifs.2020.10.030

Khan, S. A., Zhang, M., Liu, L., Dong, L., Ma, Y., Wei, Z., Chi, J., & Zhang, R. (2020). Co-culture submerged fermentation by lactobacillus and yeast more effectively improved the profiles and bioaccessibility of phenolics in extruded brown rice than single-culture fermentation. Food Chemistry, 326, 1–8. https://doi.org/10.1016/j.foodchem.2020.126985

Kumar, N., & Goel, N. (2019). Phenolic acids: Natural versatile molecules with promising therapeutic applications. Biotechnology Reports, 24. https://doi.org/10.1016/j.btre.2019.e00370

Leksono, B. Y., Cahyanto, M. N., Rahayu, E. S., Yanti, R., & Utami, T. (2022). Enhancement of antioxidants activities in black soy milk through isoflavone aglycone production during indigenous lactic acid bacteria fermentation. Fermentation, 8(7). https://doi.org/10.3390/fermentation8070326

Liu, Y., Liu, J., Tang, C., Uyanga, V. A., Xu, L., Zhang, F., Sun, J., & Chen, Y. (2023). Flavonoids‑targeted metabolomic analysis following rice yellowing. Food Chemistry, 430. https://doi.org/10.1016/j.foodchem.2023.136984

Liu, Y., Sui, X., Zhao, X., Wang, S., & Yang, Q. (2022). Antioxidative Activity evaluation of high purity and micronized tartary buckwheat flavonoids prepared by antisolvent recrystallization. Foods, 11(9). https://doi.org/10.3390/foods11091346

Maia, I. da C., D’Almeida, C. T. dos S., Freire, D. M. G., Cavalcanti, E. d’Avila C., Cameron, L. C., Dias, J. F., & Ferreira, M. S. L. (2020). Effect of solid-state fermentation over the release of phenolics compounds from brewer’s spent grain revealed by UPLC-MSE. Lwt, 133. https://doi.org/10.1016/j.lwt.2020.110136

Marniza, Syafnil, & Fitria, S. (2020). Characterization of tapai ketan hitam with various cooking methods. Jurnal Teknologi Agro-Industri, 7(2), 112–120.

McGhie, T. K., & Walton, M. C. (2007). The bioavailability and absorption of anthocyanins: towards a better understanding. Molecular Nutrition and Food Research, 51(6), 702–713. https://doi.org/10.1002/mnfr.200700092

Mishra, D., Rout, S. K., & Kar, G. A. (2020). Evaluation of antimicrobial and antioxidants activity of crude methanol extract and its fractions of mussaenda philippica leaves. International Journal of General Medicine and Pharmacy (IJGMP), 9(2), 1–14.

Muñoz-González, I., Jiménez-Girón, A., Martín-Álvarez, P. J., Bartolomé, B., & Moreno-Arribas, M. V. (2013). Profiling of microbial-derived phenolics metabolites in human feces after moderate red wine intake. Journal of Agricultural and Food Chemistry, 61(39), 9470–9479. https://doi.org/10.1021/jf4025135

Novelina, Nazir, N., Fiana, R. M., & Putra, D. P. (2019). Characteristics of black glutinous rice vinegar as traditionally fermented product of yeast tapai and Acetobacter aceti. IOP Conference Series: Earth and Environmental Science, 347(1). https://doi.org/10.1088/1755-1315/347/1/012049

Olthof, M. R., Hollman, P. C. H., & Katan, M. B. (2001). Chlorogenic acid and caffeic acid are absorbed in humans. Journal of Nutrition, 131(1), 66–71. https://doi.org/10.1093/jn/131.1.66

Qin, W., Ketnawa, S., & Ogawa, Y. (2022). Effect of digestive enzymes and pH on variation of bioavailability of green tea during simulated in vitro gastrointestinal digestion. Food Science and Human Wellness, 11(3), 669–675. https://doi.org/10.1016/j.fshw.2021.12.024

Schmidt, C. G., Gonçalves, L. M., Prietto, L., Hackbart, H. S., & Furlong, E. B. (2014). Antioxidants activity and enzyme inhibition of phenolic acids from fermented rice bran with fungus Rizhopus oryzae. Food Chemistry, 146, 371–377. https://doi.org/10.1016/j.foodchem.2013.09.101

Seraglio, S. K. T., Valese, A. C., Daguer, H., Bergamo, G., Azevedo, M. S., Nehring, P., Gonzaga, L. V., Fett, R., & Costa, A. C. O. (2017). Effect of in vitro gastrointestinal digestion on the bioaccessibility of phenolic compounds, minerals, and antioxidants capacity of Mimosa scabrella bentham honeydew honeys. Food Research International, 99, 670–678. https://doi.org/10.1016/j.foodres.2017.06.024

Shahidi, F., & Ambigaipalan, P. (2015). Phenolics and polyphenolics in foods, beverages and spices: antioxidants activity and health effects - a review. Journal of Functional Foods, 18, 820–897. https://doi.org/10.1016/j.jff.2015.06.018

Shahidi, F., & Peng, H. (2018). Bioaccessibility and bioavailability of phenolic compounds. Journal of Food Bioactives, 4, 11–68. https://doi.org/10.31665/jfb.2018.4162

Siebenhandl, S., Lestario, L. N., Trimmel, D., & Berghofer, E. (2001). Studies on tape ketan - an Indonesian fermented rice food. International Journal of Food Sciences and Nutrition, 52(4), 347–357. https://doi.org/10.1080/09637480120057585

Tanaka, T., Takase, S., & Goda, T. (1997). A possible role of a nuclear factor NF-LPH1 in the regional expression of lactase-phlorizin hydrolase along the small intestine. Journal of Nutritional Science and Vitaminology, 43(5), 565–573. https://doi.org/10.3177/jnsv.43.565

Teng, H., & Chen, L. (2019). Polyphenols and bioavailability: an update. Critical Reviews in Food Science and Nutrition, 59(13), 2040–2051. https://doi.org/10.1080/10408398.2018.1437023

Velioglu, Y. S., Mazza, G., Gao, L., & Oomah, B. D. (1998). Antioxidants activity and total phenolics in selected fruits, vegetables, and grain products. Journal of Agricultural and Food Chemistry, 46(10), 4113–4117. https://doi.org/10.1021/jf9801973

Wilson, T. H., & Wiseman, G. (1954). The use of sacs of everted small intestine for the study of the transference of substances from the mucosal to the serosal surface. The Journal of Physiology, 123(1), 116–125. https://doi.org/10.1113/jphysiol.1954.sp005036

Xiong, Q., Zhang, J., Sun, C., Wang, R., Wei, H., He, H., Zhou, D., Zhang, H., & Zhu, J. (2023). Metabolomics revealed metabolite biomarkers of antioxidants properties and flavonoid metabolite accumulation in purple rice after grain filling. Food Chemistry: X, 18. https://doi.org/10.1016/j.fochx.2023.100720

Xue, Y., Wang, X., Chen, X., Hu, J., Gao, M. T., & Li, J. (2017). Effects of different cellulases on the release of phenolic acids from rice straw during saccharification. Bioresource Technology, 234, 208–216. https://doi.org/10.1016/j.biortech.2017.02.127

Yang, F., Chen, C., Ni, D., Yang, Y., Tian, J., Li, Y., Chen, S., Ye, X., & Wang, L. (2023). Effects of fermentation on bioactivity and the composition of polyphenols contained in polyphenol-rich foods: a review. Foods, 12(17). https://doi.org/10.3390/foods12173315

Yilmaz, H., Gultekin Subasi, B., Celebioglu, H. U., Ozdal, T., & Capanoglu, E. (2022). Chemistry of protein-phenolic interactions toward the microbiota and microbial infections. Frontiers in Nutrition, 9(July), 1–16. https://doi.org/10.3389/fnut.2022.914118

Zeb, A. (2020). Concept, mechanism, and applications of phenolic antioxidants in foods. Journal of Food Biochemistry, 44(9), 1–22. https://doi.org/10.1111/jfbc.13394

Zhang, B., Zhang, Y., Li, H., Deng, Z., & Tsao, R. (2020). A review on insoluble-bound phenolics in plant-based food matrix and their contribution to human health with future perspectives. Trends in Food Science and Technology, 105, 347–362. https://doi.org/10.1016/j.tifs.2020.09.029

Zheng, J., Xiong, H., Li, Q., He, L., Weng, H., Ling, W., & Wang, D. (2019). Protocatechuic acid from chicory is bioavailable and undergoes partial glucuronidation and sulfation in healthy humans. Food Science and Nutrition, 7(9), 3071–3080. https://doi.org/10.1002/fsn3.1168

Zhishen, J., Mengcheng, T., & Jianming, W. (1999). The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. In Food Chemistry, 64 (4), 555–559. https://doi.org/10.1016/S0308-8146(98)00102-2

Zhong, H., Xue, Y., Lu, X., Shao, Q., Cao, Y., Wu, Z., & Chen, G. (2018). The effects of different degrees of procyanidin polymerization on the nutrient absorption and digestive enzyme activity in mice. Molecules, 23(11), 1–11. https://doi.org/10.3390/molecules23112916

Zieliński, H., Wiczkowski, W., Topolska, J., Piskuła, M. K., & Wronkowska, M. (2022). Bioaccessibility of phenolic acids and flavonoids from buckwheat biscuits prepared from flours fermented by lactic acid bacteria. Molecules, 27(19). https://doi.org/10.3390/molecules27196628



DOI: https://doi.org/10.22146/agritech.92729

Article Metrics

Abstract views : 125 | views : 11

Refbacks

  • There are currently no refbacks.


Bookmark and Share


Copyright (c) 2024 Muhammad Nur Cahyanto, Mita Nurul Azkia, Widiastuti Setyaningsih, Yunika Mayangsari

Creative Commons License
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.

agriTECH has been Indexed by:

Emerging Source Citation Index Directory of Open Access Journals CABI.org Dimensions Google Scholar Sinta Garuda

agriTECH (print ISSN 0216-0455; online ISSN 2527-3825) is published by Faculty of Agricultural Technology, Universitas Gadjah Mada in colaboration with Indonesian Association of Food Technologies.

website statisticsView My Stats