Abstract
The aim of this study was to perform solid-state fermentation of bee collected pollen by lactic acid bacteria and evaluate the impact of fermentation to total phenolic compounds content, total flavonoid content and radical scavenging activity of fermented and non-fermented bee pollen. Natural fermentation of bee pollen in the hive, done by bees, results in well-known product—bee bread. This study was the first attempt to produce artificial “bee bread”. To our knowledge literature date about bee pollen artificial fermentation are scarce. Five different bee pollen samples were fermented with Lactobacillus rhamnosus GG and without bacteria. Obtained fermented samples were analyzed for total phenolic compound content, total flavonoid content and free radical (DPPH) scavenging capacity by spectrophotometric methods; phenolic profile was evaluated by HPLC. Fermentation revealed positive impact on the total flavonoid content (amount of flavonoids increased by 55–135%). The results were compared with the antioxidant activity of natural bee bread. Acquired data were processed with Matlab software carrying out calculations of various similarity measures between each pollen and fermented pollen sample and bee bread sample.
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References
Adetuyi FO, Ibrahim TA (2014) Effect of fermentation time on the phenolic, flavonoid and vitamin C contents and antioxidant activities of okra (Abelmoschus esculentus) seeds. Niger Food J 32:128–137. https://doi.org/10.1016/S0189-7241(15)30128-4
Belhadj H, Harzallah D, Bouamra D, Khennouf S, Dahamna S, Ghadbane M (2014) Phenotypic and genotypic characterization of some lactic acid bacteria isolated from bee pollen: a preliminary study. Biosci Microbiota Food Health 33:11–23. https://doi.org/10.12938/bmfh.33.11
Bogdanov S (2016) Pollen: production, nutrition and health: a review. Bee product science. http://www.bee-hexagon.net/. Accessed 30 Oct 2016
Cha S-H (2007) Comprehensive survey on distance/similarity measures between probability density functions. MMMAS 1:300–307
Chu SC, Chen C (2006) Effects of origins and fermentation time on the antioxidant activities of kombucha. Food Chem 98:502–507. https://doi.org/10.1016/j.foodchem.2005.05.080
Denisow B, Denisow-Pietrzyk M (2016) Biological and therapeutic properties of bee pollen: a review. J Sci Food Agric 96:4303–4309. https://doi.org/10.1002/jsfa.7729
Di Mattia C, Martuscelli M, Sacchetti G, Scheirlinck I, Beheydt B, Mastrocola D, Pittia P (2013) Effect of fermentation and drying on procyanidins, antiradical activity and reducing properties of cocoa beans. Food Bioprocess Tech 6:3420–3432. https://doi.org/10.1007/s11947-012-1028-x
Dulf FV, Vodnar DC, Socaciu C (2016) Effects of solid-state fermentation with two filamentous fungi on the total phenolic contents, flavonoids, antioxidant activities and lipid fractions of plum fruit (Prunus domestica L.) by-products. Food Chem 209:27–36. https://doi.org/10.1016/j.foodchem.2016.04.016
Evans JD (2015) Bee bread. Books, health and history. The New York Academy of Medicine, New York
Ibukun EO (2012) Fermentation attenuates the free radical scavenging and antioxidant activities of sesame seed (Sesanum indicum). Int J Pharm Appl 3:324–331
Jayabalan R, Subathradevi P, Marimuthu S, Sathishkumar M, Swaminathan K (2008) Changes in free-radical scavenging ability of kombucha tea during fermentation. Food Chem 109:227–234. https://doi.org/10.1016/j.foodchem.2007.12.037
Juan MY, Chou CC (2010) Enhancement of antioxidant activity, total phenolic and flavonoid content of black soybeans by solid state fermentation with Bacillus subtilis BCRC 14715. Food Microbiol 27:586–591. https://doi.org/10.1016/j.fm.2009.11.002
Kaškonas P, Stanius Ž, Kaškonienė V, Obelevičius K, Ragažinskienė O, Žilinskas A, Maruška A (2016) Clustering analysis of different hop varieties according to their essential oil composition measured by GC/MS. Chem Pap 70:1568–1577. https://doi.org/10.1515/chempap-2016-0092
Kaškonienė V, Kaškonas P, Maruška A (2015a) Volatile compounds composition and antioxidant activity of bee pollen collected in Lithuania. Chem Pap 69:291–299. https://doi.org/10.1515/chempap-2015-0033
Kaškonienė V, Stankevičius M, Drevinskas T, Akuneca I, Kaškonas P, Bimbiraitė-Survilienė K, Maruška A, Ragažinskienė O, Kornyšova O, Briedis V, Ugenskienė R (2015b) Evaluation of phytochemical composition of fresh and dried raw material of introduced Chamerion angustifolium L. using chromatographic, spectrophotometric and chemometric techniques. Phytochemistry 115:184–193. https://doi.org/10.1016/j.phytochem.2015.02.005
Krell R (1996) Value-added products from beekeeping. FAO agricultural services bulletin No. 124, Food and Agriculture Organization of the United Nations Roma, p 395
Lee IH, Hung YH, Chou CC (2008) Solid-state fermentation with fungi to enhance the antioxidative activity, total phenolic and anthocyanin contents of black bean. Int J Food Microbiol 121:150–156. https://doi.org/10.1016/j.ijfoodmicro.2007.09.008
Mărgăoan R, Mărghitaş LA, Dezmirean DS, Dulf FV, Bunea A, Socaci SA, Bobiş O (2014) Predominant and secondary pollen botanical origins influence the carotenoid and fatty acid profile in fresh honeybee-collected pollen. J Agric Food Chem 62:6306–6316. https://doi.org/10.1021/jf5020318
Oboh G, Alabi KB, Akindahunsi AA (2008) Fermentation changes the nutritive value, polyphenol distribution, and antioxidant properties of Parkia biglobosa seeds (African locust beans). Food Biotechnol 22:363–376. https://doi.org/10.1080/08905430802463404
Olofsson TC, Alsterfjord M, Nilson B, Butler È, Vásquez A (2014) Lactobacillus apinorum sp. nov., Lactobacillus mellifer sp. nov., Lactobacillus mellis sp. nov., Lactobacillus melliventris sp. nov., Lactobacillus kimbladii sp. nov., Lactobacillus helsingborgensis sp. nov. and Lactobacillus kullabergensis sp. nov., isolated from the honey stomach of the honeybee Apis mellifera. Int J Syst Evol Microbiol 64:3109–3119. https://doi.org/10.1099/ijs.0.059600-0
Othman NB, Roblain D, Chammen N, Thonart P, Hamdi M (2009) Antioxidant phenolic compounds loss during the fermentation of Chétoui olives. Food Chem 116:662–669. https://doi.org/10.1016/j.foodchem.2009.02.084
Pan M, Wu Q, Tao X, Wan C, Shah NP, Wei H (2015) Fermentation of Allium chinense bulbs with Lactobacillus plantarum ZDY 2013 shows enhanced biofunctionalities, and nutritional and chemical properties. J Food Sci 80:M2272–M2278. https://doi.org/10.1111/1750-3841.12994
Salazar-González C, Díaz-Moreno C (2016) The nutritional and bioactive aptitude of bee pollen for a solid-state fermentation process. J Apic Res 55:161–175. https://doi.org/10.1080/00218839.2016.1205824
Stimbirys A, Bartkiene E, Siugzdaite J, Augeniene D, Vidmantiene D, Juodeikiene G, Maruska A, Stankevicius M, Cizeikiene D (2015) Safety and quality parameters of ready-to-cook minced pork meat products supplemented with Helianthus tuberosus L. tubers fermented by BLIS producing lactic acid bacteria. J Food Sci Technol 52:4306–4314. https://doi.org/10.1007/s13197-014-1328-4
Svensson L, Sekwati-Monang B, Lutz DL, Schieber A, Gänzle MG (2010) Phenolic acids and flavonoids in nonfermented and fermented red sorghum (Sorghum bicolor (L.) Moench). J Agric Food Chem 58:9214–9220. https://doi.org/10.1021/jf101504v
Vásquez A, Olofsson TC (2009) The lactic acid bacteria involved in the production of bee pollen and bee bread. J Apicult Res 48:189–195. https://doi.org/10.3896/IBRA.1.48.3.07
Vattem DA, Lin Y-T, Labbe RG, Shetty K (2004) Phenolic antioxidant mobilization in cranberry pomace by solid-state bioprocessing using food grade fungus Lentinus edodes and effect on antimicrobial activity against select food borne pathogens. Innov Food Sci Emerg Technol 5:81–91. https://doi.org/10.1016/j.ifset.2003.09.002
Zhao D, Shah NP (2015) Lactic acid bacterial fermentation modified phenolic composition in tea extracts and enhanced their antioxidant activity and cellular uptake of phenolic compounds following in vitro digestion. J Funct Foods 20:182–194. https://doi.org/10.1016/j.jff.2015.10.033
Zuluaga CM, Serrato JC, Quicazan MC (2015) Bee-pollen structure modification by physical and biotechnological processing: influence on the availability of nutrients and bioactive compounds. Chem Eng Trans 43:79–84. https://doi.org/10.3303/CET1543014
Acknowledgements
Authors would like to thank G. Naujokaitytė and J. Mikašauskaitė for their valuable input in the areas of HPLC/UV and microbiological analyses. Authors are grateful to Apiproduktai, Ltd. for providing bee pollen and bee bread samples.
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Kaškonienė, V., Katilevičiūtė, A., Kaškonas, P. et al. The impact of solid-state fermentation on bee pollen phenolic compounds and radical scavenging capacity. Chem. Pap. 72, 2115–2120 (2018). https://doi.org/10.1007/s11696-018-0417-7
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DOI: https://doi.org/10.1007/s11696-018-0417-7