ORIGINAL ARTICLE
Bioactive Compounds and Microbial Quality of Stored Fermented Red Beetroots and Red Beetroot Juice
 
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Department of Biotechnology and Food Sciences, Lodz University of Technology, Stefanowskiego 171/173, 09-924 Lodz, Poland
CORRESPONDING AUTHOR
Agata Czyżowska   

Department of Biotechnology and Food Sciences, Lodz University of Technology, Wolczanska 171/173, 90-924, Łódź, Poland
Online publication date: 2020-02-12
Publication date: 2020-02-12
Submission date: 2019-09-22
Final revision date: 2020-01-10
Acceptance date: 2020-01-15
 
Pol. J. Food Nutr. Sci. 2020;70(1):35–44
KEYWORDS
TOPICS
ABSTRACT
The aim of this study was to investigate the effect of long-term cold storage of fermented beetroots and fermented beetroot juice on the content of biologically active compounds and microorganisms. Contents of total phenolics, as well as red and yellow betalains were determined. Total phenolics content in fermented grated beetroot was 920 mg/kg after 7 months of cold storage, while in juice it was 810 mg/L within the same time span. At the end of the experiment, after 10 months of storage, these values decreased to 570 mg/kg and 540 mg/L, respectively. Concentration of red betalains after 7 months of storage was determined at 116 mg/kg for grated beetroot and at 69 mg/L for juice. At the same time, the content of yellow betalains was 14 mg/kg and 19 mg/L for grated beetroot and juice, respectively. In the case of fermented beets and juice, about 3-fold decrease of red pigments was observed during storage. Bioactive compounds were identified using LC-MS. Betanidin was shown to be the major compound among grated beetroot pigments at the beginning of the investigation, the beetroot juice was predominated by isobetanidin and betanidin. At the end of the study, the proportion of pigments changed slightly. Lactic acid bacteria predominated among the bacterial microbiota in the products tested. Enterobacteriaceae were not detected in fermented grated beetroots and investigated juices throughout storage time. To conclude, during long-term cold storage, the content of bioactive compounds decreases, however, remains at a high level.
ACKNOWLEDGEMENTS
The authors would like to thank Agricultural Farm Michał Sznajder/Gospodarstwo Rolne Michał Sznajder for providing samples for research.
 
REFERENCES (60)
1.
Arroyo-Lopez, F.N., Romero-Gil, V., Bautista-Gallego, J., Rodrıguez-Gomez, F., Jimenez-Diaz, R., Garcia-Garcia, P., Querol, A., Garrido-Fernandez, A. (2012). Yeasts in table olive processing: Desirable or spoilage microorganisms? International Journal of Food Microbiology, 160(1), 42–49.
 
2.
Belhadj Slimen, I., Najar, T., Abderrabba, M. (2017). Chemical and antioxidant properties of betalains. Journal of Agricultural and Food Chemistry, 65(4), 675-689.
 
3.
Blana, V.A., Grounta, A., Tassou, C.C., Nychas, G.-J.E., Panagou, E.Z. (2014). Inoculated fermentation of green olives with potential probiotic Lactobacillus pentosus and Lactobacillus plantarum starter cultures isolated from industrially fermented olives. Food Microbiology, 38, 208–218.
 
4.
Capozzi, V., Russo, P., Dueñas, M.T., López, P., Spano, G., (2012). Lactic acid bacteria producing B-group vitamins: a great potential for functional cereals products. Applied Microbiology and Biotechnology, 96(6),1383-1394.
 
5.
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.
 
6.
Czyżowska, A., Klewicka, E., Libudzisz, Z. (2006). The influence of lactic acid fermentation process of red beet juice on the stability of biologically active colorants. European Food Research and Technology, 223, 110-116.
 
7.
Czyzowska, A., Klewicka, E., Pogorzelski, E., Nowak, A. (2015). Polyphenols, vitamin C and antioxidant activity in wines from Rosa canina L. and Rosa rugosa Thunb. Journal of Food Composition and Analysis, 39, 62-68.
 
8.
Czyżowska, A., Kucharska, A.Z., Nowak, A., Sokół-Łętowska, A., Motyl, I., Piórecki, N. (2017). Suitability of the probiotic lactic acid bacteria strains as the starter cultures in unripe cornelian cherry (Cornus mas L.) fermentation. Journal of Food Science and Technology, 54(9), 2936–2946.
 
9.
Esquivel, P. (2016) Betalains. In R. Carle, R. Schweiggert (Eds.) Handbook on Natural Pigments in Food and Beverages, Industrial Applications for Improving Food Colour, Woodhead Publishing, Sawston, Cambridge, UK, pp. 81-99.
 
10.
Franco, W., Pérez-Díaz, I.M., Johanningsmeier, S.D., McFeeters, R.F. (2012). Characteristics of spoilage-associated secondary cucumber fermentation. Applied and Environmental Microbiology, 78(4), 1273–1284.
 
11.
Gardner, N.J., Savard, T., Obermeier, P., Caldwell, G., Champagne, C.P. (2001). Selection and characterization of mixed starter cultures for lactic acid fermentation of carrot, cabbage, beet and onion vegetable mixtures. International Journal of Food Microbiology, 64(3), 261-275.
 
12.
Gengatharan, A., Dykes, G.A., Choo, W.S. (2015). Betalains: Natural plant pigments with potential application in functional foods. LWT - Food Science and Technology, 64(2), 645-649.
 
13.
Herbach, K.M., Stintzing, F.C., Carle, R. (2006). Betalain stability and degradation — structural and chromatic aspects. Journal of Food Science, 71(4), R41-R50.
 
14.
ISO 6887 (2010). Microbiology of food and animal feed. Preparation of test samples, initial suspension and decimal dilutions for microbiological examination.
 
15.
Ju, Y.H., Carlson, K.E., Sun, J., Pathak, D., Katzenellenbogen, B.S., Katzenellenbogen, J.A., Helferich, W.G. (2000). Estrogenic effects of extracts from cabbage, fermented cabbage, and acidified brussels sprouts on growth and gene expression of estrogen-dependent human breast cancer (MCF-7) cells. Journal of Agricultural and Food Chemistry, 48(10), 4628-4634.
 
16.
Jung, S.J., Park, S.H., Choi, E.K., Cha, Y.S., Cho, B.H., Kim, Y.G., Kim, M.G., Song, W.O., Park, T.S., Ko, J.K., So, B.O., Chae, S.W. (2014). Beneficial effects of Korean traditional diets in hypertensive and type 2 diabetic patients. Journal of Medicinal Food, 17, 161–171.
 
17.
Kavalcová, P., Bystrická, J., Tomáš, J., Karovičová, J., Kovarovič, J., Lenková, M. (2015). The content of total polyphenols and antioxidant activity in red beetroot. Potravinarstvo, 9(1), 77-83.
 
18.
Kavitake, D., Kandasamy, S., Bruntha, Devi P., Shetty, P.H. (2018). Recent developments on encapsulation of lactic acid bacteria as potential starter culture in fermented foods – a review. Food Bioscience, 21, 34-44.
 
19.
Kazimierczak, R., Hallmann, E., Lipowski, J., Drela, N., Kowalik, A., Püssa, T., Matt, D., Luik, A., Gozdowski, D., Rembiałkowska, E. (2014). Beetroot (Beta vulgaris L.) and naturally fermented beetroot juices from organic and conventional production: metabolomics, antioxidant levels and anticancer activity. Journal of the Science of Food and Agriculture, 94(13), 2618-2629.
 
20.
Khan, M.I., Giridhar, P. (2015). Plant betalains: chemistry and biochemistry. Review. Phytochemistry, 117, 267-295.
 
21.
Kim, E.K., An, S.Y., Lee, M.S., Kim, T.H., Lee, H.K., Hwang, W.S., Choe, S.J., Kim, T.Y., Han, S.J., Kim, H.J., Kim, D.J., Lee, K.W. (2011). Fermented kimchi reduces body weight and improves metabolic parameters in overweight and obese patients. Nutrition Research, 31, 436–443.
 
22.
Klewicka, E., Czyzowska, A. (2011). Biological stability of lactofermented beetroot juice during refrigerated storage. Polish Journal of Food and Nutrition Sciences, 61(4), 251-256.
 
23.
Kujala, T.S., Vienola, M.S., Klika, K.D., Loponen, J.M., Pihlaja, K. (2002). Betalain and phenolic compositions of four beetroot (Beta vulgaris) cultivars. European Food Research and Technology, 214, 505-510.
 
24.
Kusznierewicz, B., Lewandowska, J., Kruszyna, A., Piasek, A., Śmiechowska, A., Namieśnik, J., Bartoszek, A. (2010). The antioxidative properties of white cabbage (Brassica oleracea var. capitata f. alba) fresh and submitted to culinary processing. Journal of Food Biochemistry, 34, 262–285.
 
25.
Lechner, J.F., Stoner, G.D. (2019). Red beetroot and betalains as cancer chemopreventative agents. Molecules, 24(8), art. no. 1602.
 
26.
Licznerska, B.E., Szaefer, H., Murias, M., Bartoszek, A., Baer-Dubowska, W. (2013). Modulation of CYP19 expression by cabbage juices and their active components: indole-3-carbinol and 3,3'-diindolylmethene in human breast epithelial cell lines. European Journal of Nutrition, 52(5), 1483-1492.
 
27.
Lundberg, J.O., Weitzberg, E., Gladwin, M.T. (2008). The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nature Reviews Drug Discovery, 7, 156-167.
 
28.
Maruvada, R., McFeeters, R.F. (2009). Evaluation of enzymatic and non-enzymatic softening in low salt cucumber fermentations. International Journal of Food Science and Technology, 44, 1108–1117.
 
29.
McFeeters, R.F. (2004). Fermentation microorganisms and flavor changes in fermented foods. Journal of Food Science, 69(1), 35-37.
 
30.
Michlmayr, H., Kneifel, W. (2014). β-Glucosidase activities of lactic acid bacteria: mechanisms, impact of fermented food and human health. FEMS Microbiology Letters, 352(1), 1-10.
 
31.
Mikołajczyk-Bator, K., Błaszczyk, A., Czyżniejewski, M., Kachlicki, P. (2016). Characterisation and identification of triterpene saponins in the roots of red beets (Beta vulgaris L.) using two HPLC–MS systems. Food Chemistry, 192, 979-990.
 
32.
Nemzer, B., Pietrzkowski, Z., Spórna, A., Stalica, P., Thresher, W., Michałowski, T., Wybraniec, S. (2011). Betalainic and nutritional profiles of pigment – enriched red beet root (Beta vulgaris L.) dried extracts. Food Chemistry, 127, 42-53.
 
33.
Nilsson, T. (1970). Studies into the pigments in beetroot (Beta vulgaris L. ssp. vulgaris var. rubra L.). Lantbrukshogskolans Annaler, 36, 179–219.
 
34.
Ninfali, P., Antonini, E., Frati, A., Scarpa, E.‐S. (2017). C‐glycosyl flavonoids from Beta vulgaris Cicla and betalains from Beta vulgaris rubra: Antioxidant, anticancer and antiinflammatory activities — A review. Phytotherapy Research, 31(6), 871-884.
 
35.
Nowak, A., Czyzowska, A., Efenberger, M., Krala, L. (2016). Polyphenolic extracts of cherry (Prunus cerasus L.) and blackcurrant (Ribes nigrum L.) leaves as natural preservatives in meat products. Food Microbiology, 59, 142–149.
 
36.
Panek, K. (1905). Mikroby oraz chemizm kiśnienia barszczu. Spółka Wydawnicza Polska, Kraków, pp. 1-42 (in Polish).
 
37.
Parada, J., Aguilera, J.M. (2007). Food microstructure affects the bioavailability of several nutrients. Journal of Food Science, 72, R21–R32.
 
38.
Park, J.A., Tirupathi Pichiah, P.B., Yu, J.J., Oh, S.H., Daily, J.W. III, Cha, Y.S. (2012). Anti-obesity effect of kimchi fermented with Weissella koreensis OK1-6 as starter in high-fat diet-induced obese C57BL/6J mice. Journal of Applied Microbiology, 113, 1507–1516.
 
39.
Park, J.E., Moon, Y.J., Cha, Y.S. (2008). Effect of functional materials producing microbial strains isolated from Kimchi on antiobesity and inflammatory cytokines in 3T3-L1 preadipocytes. FASEB Journal, 23, 111-112.
 
40.
Peñas, E., Frias, J., Sidro, B., Vidal-Valverde, C. (2010). Impact of fermentation conditions and refrigerated storage on microbial quality and biogenic amine content of sauerkraut. Food Chemistry, 123, 143-150.
 
41.
Perez Diaz, I.M., Breidt, F., Buescher, R.W., Arroyo-Lopez, F.N., Jimenez-Diaz, R., Bautista-Gallego, J., Garrido-Fernandez, A., Yoon, S., Johanningsmeier, S.D. (2014). Fermented and acidified vegetables. Compendium of Methods for the Microbiological Examination of Foods. Chapter 51, APHA Press, Washington, USA, pp. 1-22.
 
42.
Preczenhak, A.P., Orsi, B., Pereira Lima, G.P., Tezotto-Uliana, J.V., Minatel, I.O., Kluge, R.A. (2019). Cysteine enhances the content of betalains and polyphenols in fresh-cut red beet. Food Chemistry, 286, 600-607.
 
43.
Ravichandran, K., Ahmed, A.R., Knorr, D., Smetanska, I. (2012). The effect of different processing methods on phenolic acid content and antioxidant activity of red beet. Food Research International, 48, 16–20.
 
44.
Sawicki, T., Bączek, N., Wiczkowski, W. (2016). Betalain profile, content and antioxidant capacity of red beetroot dependent on the genotype and root part. Journal of Functional Foods, 27, 249-261.
 
45.
Sawicki, T., Juśkiewicz, J., Wiczkowski, W. (2017). Using the SPE and Micro-HPLC-MS/MS method for the analysis of betalains in rat plasma after red beet administration. Molecules, 22, art. no. 2137.
 
46.
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.
 
47.
Sawicki, T., Topolska, J., Romaszko, E., Wiczkowski, W. (2018). Profile and content of betalains in plasma and urine of volunteers after long-term exposure to fermented red beet juice. Journal of Agricultural and Food Chemistry, 66(16), 4155-4163.
 
48.
Sawicki, T., Wiczkowski, W. (2018). The effects of boiling and fermentation of betalain profiles and antioxidant capacities of red beetroot products. Food Chemistry, 259, 292-303.
 
49.
Septembre-Malaterre, A., Remize, F., Poucheret, P. (2018). Fruits and vegetables, as a source of nutritional compounds and phytochemicals: Changes in bioactive compounds during lactic fermentation. Food Research International, 104, 86-99.
 
50.
Slatnar, A., Stampar, F., Veberic, R., Jakopic, J. (2015). HPLC-MSn identification of betalain profile of different beetroot (Beta vulgaris L. ssp. vulgaris) parts and cultivars. Journal of Food Science, 80(9), C1952-C1958.
 
51.
Starzak, K., Szot, D., Skopińska, A., Swiergosz, T., Wybraniec, S. (2016). Enzymatic oxidation of neobetanin monitored by liquid chromatography with mass spectrometric detection. Challenges of Modern Technology, 7(1), 29-31.
 
52.
Swain, M.R., Anandharaj, M., Ray, R.C., Rani, R.P. (2014). Fermented fruits and vegetables of Asia: A potential source of probiotics. Review article. Biotechnology Research International, 2014, art. no. 250424.
 
53.
Szaefer, H., Krajka-Kuźniak, V., Licznerska, B., Bartoszek, A., Baer-Dubowska, W. (2015). Cabbage juices and indoles modulate the expression profile of AhR, ERα, and Nrf2 in human breast cell lines. Nutrition and Cancer, 67(8), 1344-1356.
 
54.
Thapa, N., Tamang, J.P. (2015). Functionality and Therapeutic Values of Fermented Foods. In J.P. Tamang (Ed.), Microorganisms in Fermented Foods and Beverages, CRC Press Inc., Boca Raton, Florida, USA, pp. 111-168.
 
55.
Waterhouse, A.L. (2001). Determination of total phenolics. In R.E. Wrolstad (Ed.), Current Protocols in Food Analytical Chemistry, Wiley, Hoboken, New Jersey, USA, pp. I1.1.1–I1.1.8.
 
56.
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.
 
57.
Wruss, J., Waldenberger, G., Huemer, S., Uygun, P., Lanzerstorfer, P., Müller, U., Höglinger, 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.
 
58.
Wybraniec, S., Michałowski, T. (2011). New pathways of betanidin and betanin enzymatic oxidation, Journal of Agricultural and Food Chemistry. 59, 9612-9622.
 
59.
Yoon, K.Y., Woodams, E.E., Hang, Y.D. (2005). Fermentation of beet juice by beneficial lactic acid bacteria. LWT - Food Science and Technology, 38, 73–75.
 
60.
Zieliński, H., Surma, M., Zielińska, D. (2017). The naturally fermented sour pickled cucumbers. In J. Frias, C. Martinez-Villaluenga, E. Peñas (Eds.), Fermented Foods in Health and Disease Prevention, Elsevier Inc., Academic Press, Cambridge, Massachusetts, USA, pp. 503-516.
 
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