ORIGINAL ARTICLE
Red Beetroot Juice Phytochemicals Bioaccessibility: an In Vitro Approach
| 1 | Department of Analytical Chemistry and Physical Chemistry, University of Food Technologies, 26 Maritza Blvd., Plovdiv, Bulgaria |
| 2 | Department of Organic Chemistry and Inorganic Chemistry, University of Food Technologies, 26 Maritza Blvd., Plovdiv, Bulgaria |
| 3 | Department of Biotechnology, University of Food Technologies, 26 Maritza Blvd., Plovdiv, Bulgaria |
CORRESPONDING AUTHOR
Ivelina Deseva
Department of Analytical chemistry and physical chemistry, University of Food Technologies, 26, Maritza, 4002, Plovdiv, Bulgaria
Department of Analytical chemistry and physical chemistry, University of Food Technologies, 26, Maritza, 4002, Plovdiv, Bulgaria
Submission date: 2019-08-21
Final revision date: 2020-01-10
Acceptance date: 2020-01-14
Online publication date: 2020-02-12
Publication date: 2020-02-12
Pol. J. Food Nutr. Sci. 2020;70(1):45–53
KEYWORDS
TOPICS
Liquid chromatographyFunctional propertiesBioavailabilityDigestionFood bioactivesVegetablesBeveragesPhenolic compoundsPigments
ABSTRACT
Beetroot, the cultivated form of Beta vulgaris subsp. vulgaris, is known for its various beneficial properties but more critical data about its bioactive compounds digestion is needed. In the present research, the bioaccessibility of phytochemicals in freshly prepared red beetroot juice was studied. Changes in total phenolics content, total flavonoids content, contents of betacyanins and betaxanthins, phenolic acids profile as well as the antioxidant activity were monitored before and after simulated gastrointestinal digestion. Several parameters that provide interrelated information about food quality were additionally evaluated, including oxalic acid and individual sugars content, total titratable acidity, and acetylcholinesterase inhibitory activity. Significant loss of contents of total phenolics and flavonoids measured after digestion resulted in the recovery of 27.07 and 36.4%, respectively. The same negative tendency was observed for betalains bioaccessibility. While nearly 27% of betaxanthins were present after the simulated digestion, almost all betacyanins (96.07%) have been lost. The HPLC analysis of phenolic acids of beetroot juice revealed the presence of chlorogenic, caffeic, p-coumaric, and sinapic acids. After digestion, a 2.5-fold higher concentration of chlorogenic acid was found, however caffeic and p-coumaric acids were no longer detected. The results concerning the antioxidant activity of digested juice were inexplicit. According to the DPPH assay, there was a complete recovery of antioxidant activity, while no activity was detected employing the ABTS assay. Following the cupric ion reducing antioxidant capacity (CUPRAC) and ferric-reducing antioxidant power (FRAP), approximately half of the initial activity was retained. Despite the losses, red beetroot remains a valuable source of biologically active substances. Better understanding of their transformation during digestion is further needed.
FUNDING
The authors gratefully acknowledge financial support from the University of Food Technologies’ Scientific Research Fund, project 03/19-H.
REFERENCES (56)
1.
Alminger, M., Aura, A.-M., Bohn, T., Dufour, C., El, S.N., Gomes, A., Karakaya, S., Martínez-Cuesta, M.C., McDougall, G.J., Requena, T., Santos, C.N. (2014). In vitro models for studying secondary plant metabolite digestion and bioaccessibility. Comprehensive Reviews in Food Science and Food Safety, 13(4), 413-436.
2.
Apak, R., Güçlü, K., Özyürek, M., Karademir, E. (2004). Novel total antioxidant capacity index for dietary polyphenols and vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. Journal of Agricultural and Food Chemistry, 52(26), 7970-7981.
3.
Apak, R., Güçlü, K., Demirata, B., Özyürek, M., Çelik, S.E., Bektaşoğlu, B., Berker, K.I., Özyurt, D. (2007). Comparative evaluation of various total antioxidant capacity assays applied to phenolic compounds with the CUPRAC assay. Molecules, 12(7), 1496-1547.
4.
Bavec, M., Turinek, M., Grobelnik-Mlakar, S., Slatnar, A., Bavec, F. (2010). Influence of industrial and alternative farming systems on contents of sugars, organic acids, total phenolic content, and the antioxidant activity of red beet (Beta vulgaris L. ssp. vulgaris Rote Kugel). Journal of Agricultural and Food Chemistry, 58(22), 11825-11831.
5.
Bazaria, B., Kumar, P. (2016). Compositional changes in functional attributes of vacuum concentrated beetroot juice. Journal of Food Processing and Preservation, 40(6), 1215–1222.
6.
Benzie, F., Strain, J. (1999). Ferric reducing/antioxidant power assay: Direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods in Enzymology, 299, 15- 27.
7.
Bermúdez-Soto, M.-J., Tomás-Barberán, F.-A., García-Conesa, M.-T. (2007). Stability of polyphenols in chokeberry (Aronia melanocarpa) subjected to in vitro gastric and pancreatic digestion. Food Chemistry, 102(3), 865-874.
8.
Bouayed, J., Deußer, H., Hoffmann, L., Bohn, T. (2012). Bioaccessible and dialysable polyphenols in selected apple varieties following in vitro digestion vs. their native patterns. Food Chemistry, 131(4), 1466-1472.
9.
Bouayed, J., Hoffmann, L., Bohn, T. (2011). Total phenolics, flavonoids, anthocyanins and antioxidant activity following simulated gastro-intestinal digestion and dialysis of apple varieties: Bioaccessibility and potential uptake. Food Chemistry, 128(1), 14-21.
10.
Brand-Williams, W., Cuvelier, E., Berset, C. (1995). Use of a free radical method to evaluate antioxidant activity. LWT - Food Sciencce and Technology, 28(1), 25-30.
11.
Carrillo, C., Rey, R., Hendrickx, M., Del Mar Cavia, M., Alonso-Torre, S. (2017) Antioxidant capacity of beetroot: Traditional vs novel approaches. Plant Foods for Human Nutrition, 72(3), 266-273.
12.
Chhikara, N., Kushwaha, K., Sharma, P., Gat, Y., Panghal, A. (2019). Bioactive compounds of beetroot and utilization in food processing industry: A critical review. Food Chemistry, 272, 192-200.
13.
Clifford, T., Howatson, G., West, D.J., Stevenson, E.J. (2015). The potential benefits of red beetroot supplementation in health and disease. Nutrients, 7(4), 2801–2822.
14.
Correa-Betanzo, J., Allen-Vercoe, E., McDonald, J., Schroeter, K., Corredig, M., Paliyath, G. (2014). Stability and biological activity of wild blueberry (Vaccinium angustifolium) polyphenols during simulated in vitro gastrointestinal digestion. Food Chemistry, 165, 522–531.
15.
Czapski, J., Mikołajczyk, K., Kaczmarek, M. (2009). Relationship between antioxidant capacity of red beet juice and contents of its betalain pigments. Polish Journal of Food and Nutrition Sciences, 59(2), 119–122.
16.
Dalmau, M.E., Llabrés, P.J., Eim, V.S., Rosselló. C., Simal, S. (2019). Influence of freezing on the bioaccessibility of beetroot (Beta vulgaris) bioactive compounds during in vitro gastric digestion. Journal of the Science of Food and Agriculture, 99(3), 1055-1065.
17.
da Silva, D.V.T., de Oliveira Silva, F., Perrone, D., Pierucci, A.P.T.R., Conte-Junior, C.A., da Silveira Alvares, Th., del Aguila, E.M., Paschoalin, V.M.F. (2016). Physicochemical, nutritional, and sensory analyses of a nitrate-enriched beetroot gel and its effects on plasmatic nitric oxide and blood pressure. Food and Nutrition Research, 60, art. no. 29909.
18.
Duke, J.A. (2000). Handbook of Phytochemical Constituents of GRAS Herbs and Other Economic Plants. 2nd edition. CRC Press Inc., Boca Raton, Florida, USA, p. 404.
19.
Gandía-Herrero, F., Escribano, J., García-Carmona, F. (2010). Structural implications on color, fluorescence, and antiradical activity in betalains. Planta, 232(2), 449-460.
20.
Georgiev, V.G., Weber, J., Kneschke, E.M., Denev, P.N., Bley, T., Pavlov, A.I. (2010). Antioxidant activity and phenolic content of betalain extracts from intact plants and hairy root cultures of the red beetroot Beta vulgaris cv. Detroit dark red. Plant Foods for Human Nutrition, 65(2), 105-111.
21.
Granato, D., Karnopp, A.R., van Ruth, S.M. (2015). Characterization and comparison of phenolic composition, antioxidant capacity and instrumental taste profile of juices from different botanical origins. Journal of the Science of Food and Agriculture, 95(10), 1997–2006.
22.
Guldiken, B., Toydemir, T., Memis, K.N., Okur, S., Boyacioglu, D., Capanoglu, E. (2016). Home-processed red beetroot (Beta vulgaris L.) products: Changes in antioxidant properties and bioaccessibility. International Journal of Molecular Sciences, 17(6), art. no. 858.
23.
Haida, Z., Hakiman, M. (2019). A comprehensive review on the determination of enzymatic assay and nonenzymatic antioxidant activities. Food Science and Nutrition, 7(5), 1555–1563.
24.
Holmes, R.P., Assimos, D.G. (2004). The impact of dietary oxalate on kidney stone formation. Urological Research, 32(5), 311–316.
25.
Kapadia, G.J., Rao, G.S. (2013). Anticancer effects of red beet pigments. In B. Neelwarne B. (Ed.), Red Beet Biotechnology, Springer, Boston, MA, USA, pp. 132, 140.
26.
Karam, J., Bibiloni, M.D.M., Tur, J.A. (2018). Polyphenol estimated intake and dietary sources among older adults from Mallorca Island. PLoS ONE, 13(1), art. no. e0191573.
27.
Kujala, T.S., Vienola, M.S., Klika, K.D., Loponen, J.M., Pihlaja, K. (2002). Betalain and phenolic composition of four beetroot (Beta vulgaris) cultivars. European Food Research and Technology, 214(6), 505–510.
28.
Lobbens, E.S., Vissing, K.J., Jorgensen, L., de Weert, M., Jäger, A.K. (2017). Screening of plants used in the European traditional medicine to treat memory disorders for acetylcholinesterase inhibitory activity and anti amyloidogenic activity. Journal of Ethnopharmacology, 200, 66-73.
29.
Mihaylova, D., Popova, A., Alexieva, I., Krastanov, A., Lante, A. (2018). Polyphenols as suitable control for obesity and diabetes. Open Biotechnology Journal, 12, 219–228.
30.
Mihaylova, D., Vrancheva, R., Desseva, I., Ivanov, I., Dincheva, I., Popova, M., Popova, A. (2019). Analysis of the GC-MS of volatile compounds and the phytochemical profile and antioxidant activities of some Bulgarian medicinal plants. Zeitschrift für Naturforschung C – Journal of Biosciences, 74(1-2), 45-54.
31.
Minekus, M., Alminger, M., Alvito, P., Ballance, S., Bohn, T., Bourlieu, C., Carriere, F., Boutrou, R., Corredig, M., Dupont, D., Dufour, C., Egger, L., Golding, M., Karakaya, S., Kirkhus, B., le Feunteun, S., Lesmes, U., Macierzanka, A., Mackie, A., Marze, S., McClements, D.J., Ménard, O., Recio, I.; Santos, C.N., Singh, R.P., Vegarud, G.E., Wickham, M.S.J., Weitschies, W., Brodkorb, A. (2014). A standardised static in vitro digestion method suitable for food - an international consensus. Food and Function, 5(6), 1113–1124.
32.
Murthy, K.N.C., Manchali, S. (2013). Anti-diabetic potentials of red beet pigments and other constituents. In B. Neelwarne B. (Ed.). Red Beet Biotechnology. Springer, Boston, MA, USA, p. 168.
33.
Olumese, F.E., Oboh, H.A. (2016). Antioxidant and antioxidant capacity of raw and processed Nigerian beetroot (Beta vulgaris). Nigerian Journal of Basic and Applied Sciences, 24(1), 35-40.
34.
Ou, B., Huang, D., Hampsch-Woodill, M., Flanagan, J.A., Deemer, E.K. (2002). Analysis of antioxidant activities of common vegetables employing oxygen radical absorbance capacity (ORAC) and ferric reducing antioxidant power (FRAP) assays: A comparative study. Journal of Agricultural and Food Chemistry, 50(11), 3122–3128.
35.
Ovando-Martínez, M., Gámez-Meza, N., Molina-Domínguez, C.C., Hayano-Kanashiro, C., Medina-Juárez, L.A. (2018). Simulated gastrointestinal digestion, bioaccessibility and antioxidant capacity of polyphenols from red chiltepin (Capsicum annuum L. var. glabriusculum) grown in Northwest Mexico. Plant Foods for Human Nutrition, 73(2), 116–121.
36.
Parada, J., Aguilera, J.M. (2007). Food microstructure affects the bioavailability of several nutrients. Journal of Food Science, 72(2), R21–32.
37.
Park, Y.K., Koo, M.H., Ikegaki, M., Contado, J.L. (1997). Comparison of the flavonoid aglycone contents of Apis mellifera propolis from various regions of Brazil. Brazilian Archives of Biology and Technology, 40(1), 97–106.
38.
Pavan, V., Sancho, R.A.S., Pastore, G.M. (2014). The effect of in vitro digestion on the antioxidant activity of fruit extracts (Carica papaya, Artocarpus heterophillus and Annona marcgravii). LWT - Food Science and Technology, 59(2/2), SI, 1247-1251.
39.
Petkova, N., Vrancheva, R., Denev, P., Ivanov, I., Pavlov, A. (2014). HPLC-RID method for determination of inulin and fructooligosacharides. Acta Scientifica Naturalis, 1, 99-107.
40.
Porto, M.R.A., Okina, V.S., Pimentel, T.C., Prudencio, S.H. (2017). Physicochemical stability, antioxidant activity, and acceptance of beet and orange mixed juice during refrigerated storage. Beverages, 3(3), art no. 36.
41.
Ravichandran, K., Saw, N.M.M.T., Mohdaly, A.A.A., Gabr, A.M.M., Kastell, A., Riedel, H., Cai, Zh., Knorr, D., Smetanska, I. (2013). Impact of processing of red beet on betalain content and antioxidant activity. Food Research International, 50(2), 670-675.
42.
Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine, 26(9-10), 1231-1237.
43.
Sawicki, T., Martinez-Villaluenga, C., Frias, J., Wiczkowski, W, Peñas, E, Bączek, N, Zieliński, H. (2019). The effect of processing and in vitro digestion on the betalain profile and ACE inhibition activity of red beetroot products. Journal of Functional Foods, 55, 229-237.
44.
Shahidi, F., Peng, H. (2018). Bioaccessibility and bioavailability of phenolic compounds. Journal of Food Bioactivities, 4, 11–68.
45.
Sengul, H., Surek, E., Nilufer Erdil, D. (2014). Investigating the effects of food matrix and food components on bioaccessibility of pomegranate (Punica granatum) phenolics and anthocyanins using an in-vitro gastrointestinal digestion model. Food Research International, 62, 1069-1079.
46.
Singleton, V.L., Rossi, J.A. (1965). Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture, 16, 144-158.
47.
Solovchenko, A., Yahia, E., Chen, C. (2018). Pigments. In E. Yahia, A. Carrilo (Eds.), Postharvest Physiology and Biochemistry of Fruits and Vegetables, Woodhead Publishing, pp. 225–252.
48.
Stintzing, F.C., Carle, R. (2004). Functional properties of anthocyanins and betalains in plants, food, and in human nutrition. Trends in Food Science and Technology, 15(1), 19–38.
49.
Stintzing, F.C., Schieber, A., Carle, R. (2003). Evaluation of colour properties and chemical quality parameters of cactus juices. European Food Research and Technology, 216(4) 303-311.
50.
Szwajgier, D., Borowiec, K. (2012). Screening for cholinesterase inhibitors in selected fruits and vegetables. Electronic Journal of Polish Agricultural Universities, 15(2), #06.
51.
Tesoriere, L., Fazzari, M., Angileri, F., Gentile, C., Livrea, M.A. (2008). In vitro digestion of betalainic foods. Stability and bioaccessibility of betaxanthins and betacyanins and antioxidative potential of food digesta. Journal of Agricultural and Food Chemistry, 56(2), 10487–10492.
52.
Vasconcellos, J., Conte-Junior, C., Silva, D., Pierucci, A.P., Paschoalin, V., Alvares, T.S. (2016). Comparison of total antioxidant potential, and total phenolic, nitrate, sugar, and organic acid contents in beetroot juice, chips, powder, and cooked beetroot. Food Science and Biotechnology, 25(1), 79–84.
53.
Wettasinghe, M., Bolling, B., Plhak, L., Xiao, H., Parkin, K. (2002). Phase II enzyme-inducing and antioxidant activities of beetroot (Beta vulgaris L.) extracts from phenotypes of different pigmentation. Journal of Agricultural and Food Chemistry, 50(23), 6704-Ð6707.
54.
Wong, Y.H., Lau, H.W., Tan, C.P., Long, K., Nyam, K.L. (2014). Binary solvent extraction system and extraction time effects on phenolic antioxidants from kenaf seeds (Hibiscus cannabinus L.) extracted by a pulsed ultrasonic-assisted extraction. Scientific World Journal, 2014, art. no. 789346.
55.
Wootton-Beard, P.C., Ryan, L. (2011). A beetroot juice shot is a significant and convenient source of bioaccessible antioxidants. Journal of Functional Foods, 3(4), 329–334.
56.
Wruss, J., Waldenberger, G., Huemer, S., Uygun, P., Lanzerstorfer, P., Muller, U., Hoglinger, O., Weghuber, J. (2015). Compositional characteristics of commercial beetroot products and beetroot juice prepared from seven beetroot varieties grown in Upper Austria. Journal of Food Composition and Analysis, 42, 46–55.
CITATIONS (5):
1.
Thematic Issue on “Red Beetroot as a Source of Nutrients, Bioactive Compounds and Pigments”
Wiesław Wiczkowski
Polish Journal of Food and Nutrition Sciences
Wiesław Wiczkowski
Polish Journal of Food and Nutrition Sciences
2.
Three Types of Red Beetroot and Sour Cherry Based Marmalades with Enhanced Functional Properties
Oana Nistor, (Ceclu) Șeremet, Gabriel Mocanu, Vasilica Barbu, Doina Andronoiu, Nicoleta Stănciuc
Molecules
Oana Nistor, (Ceclu) Șeremet, Gabriel Mocanu, Vasilica Barbu, Doina Andronoiu, Nicoleta Stănciuc
Molecules
3.
Red Beetroot. A Potential Source of Natural Additives for the Meat Industry
Rubén Domínguez, Paulo Munekata, Mirian Pateiro, Aristide Maggiolino, Benjamin Bohrer, José Lorenzo
Applied Sciences
Rubén Domínguez, Paulo Munekata, Mirian Pateiro, Aristide Maggiolino, Benjamin Bohrer, José Lorenzo
Applied Sciences
4.
A Novel Process for the Recovery of Betalains from Unsold Red Beets by Low-Temperature Enzyme-Assisted Extraction
Claudio Lombardelli, Ilaria Benucci, Caterina Mazzocchi, Marco Esti
Foods
Claudio Lombardelli, Ilaria Benucci, Caterina Mazzocchi, Marco Esti
Foods
5.
Impact of In Vitro Gastrointestinal Digestion on the Bioaccessibility of Phytochemical Compounds from Eight Fruit Juices
Dasha Mihaylova, Ivelina Desseva, Magdalena Stoyanova, Nadezhda Petkova, Margarita Terzyiska, Anna Lante
Molecules
Dasha Mihaylova, Ivelina Desseva, Magdalena Stoyanova, Nadezhda Petkova, Margarita Terzyiska, Anna Lante
Molecules
RELATED ARTICLE
Digitalization of scientific manuscripts published in PJFNS quarterly to enable open access to them in the Internet – task financed under the agreement no. 607/P-DUN/2019 from funds of the Minister of Science and Higher Education intended for science dissemination activities.
Utrzymanie procedur zabezpieczających oryginalność artykułów naukowych publikowanych w kwartalniku PJFNS - zadanie finansowane w ramach umowy 607/P-DUN/2019 ze środków Ministra Nauki i Szkolnictwa Wyższego przeznaczonych na działalność upowszechniającą naukę.
Maintenance of procedures assuring originality of scientific manuscripts published in PJFNS quarterly – task financed under the agreement no. 607/P-DUN/2019 from funds of the Minister of Science and Higher Education intended for science dissemination activities.