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Microencapsulation of Propolis in Protein Matrix Using Spray Drying for Application in Food Systems

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Abstract

Propolis presents several health benefits due to the presence of bioactive compounds, mainly phenolic compounds; however, its application in food is limited due to undesirable odor and low water solubility. The bioactive compounds are usually susceptible to degradation by exposure to light, heat, or oxygen or by interaction with other compounds, which may limit its biological activity. The study aimed the propolis extract microencapsulation using rice, pea, soybean, and ovoalbumin proteins as wall material by spray drying and to analyze their in vitro digestion. The propolis extract presented a high concentration of apigenin. Encapsulation efficiency was greater than 70%, and it was maintained the antioxidant activity of propolis (88% inhibition of DPPH for propolis extract and > 73% for the microparticles). The DSC, ATR-FTIR, and X-ray diffraction techniques confirmed the encapsulation. The microparticles showed different shapes, sizes, and physical characteristics. The microparticles encapsulated with pea protein could be used in formulations of Minas Frescal cheese due to the controlled released, whereas the other microparticles could be used in pudding formulations.

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References

  • Ahn, M. R., Kumazawa, S., Usui, Y., Nakamura, J., Matsuka, M., Zhu, F., & Nakayama, T. (2007). Antioxidant activity and constituents of propolis collected in various areas of China. Food Chemistry, 101(4), 1383–1392.

    Article  CAS  Google Scholar 

  • Alishahi, A., Mirvaghefi, A., Tehrani, M. R., Farahmand, H., Shojaosadati, S. A., Dorkoosh, F. A., & Elsabee, M. Z. (2011). Shelf life and delivery enhancement of vitamin C using chitosan nanoparticles. Food Chemistry, 126(3), 935–940.

    Article  CAS  Google Scholar 

  • Amagliani, L., O’Regan, J., Kelly, A. L., & O’Mahony, J. A. (2017). Composition and protein profile analysis of rice protein ingredients. Journal of Food Composition and Analysis, 59, 18–26.

    Article  CAS  Google Scholar 

  • Andrade, J. K. S., Denadai, M., de Oliveira, C. S., Nunes, M. L., & Narain, N. (2017). Evaluation of bioactive compounds potential and antioxidant activity of brown, green and red propolis from Brazilian northeast region. Food Research International, 101, 129–138.

    Article  CAS  PubMed  Google Scholar 

  • AOAC (1995). Official methods of analysis of the Association of Official Analytical Chemistry (16th Ed). In In AOAC International, 1141. Washington.

  • Bhandari, B. R., Senoussi, A., Dumoulin, E. D., & Lebert, A. (1993). Spray drying of concentrated fruit juices. Drying Technology, 11(5), 1081–1092.

    Article  CAS  Google Scholar 

  • Brand-Williams, W., Cuvelier, M.-E., & Berset, C. (1995). Use of a free radical method to evaluate antioxidant activity. Lebens Wiss Techn (LWT), 28(1), 25–30.

    Article  CAS  Google Scholar 

  • Bruschi, M. L., Cardoso, M. L. C., Lucchesi, M. B., & Gremião, M. P. D. (2003). Gelatin microparticles containing propolis obtained by spray-drying technique: preparation and characterization. International Journal of Pharmaceutics, 264(1-2), 45–55.

    Article  CAS  PubMed  Google Scholar 

  • Busch, V. M., Pereyra-Gonzalez, A., Šegatin, N., Santagapita, P. R., Poklar Ulrih, N., & Buera, M. P. (2017). Propolis encapsulation by spray drying: characterization and stability. Lebens Wiss Techn (LWT), 75, 227–235.

    Article  CAS  Google Scholar 

  • Çam, M., Içyer, N. C., & Erdoğan, F. (2014). Pomegranate peel phenolics: microencapsulation, storage stability and potential ingredient for functional food development. Lebens Wiss Techn (LWT), 55(1), 117–123.

    Article  CAS  Google Scholar 

  • Choi, K. O., Ryu, J., Kwak, H. S., & Ko, S. (2010). Spray-dried conjugated linoleic acid encapsulated with Maillard reaction products of whey proteins and maltodextrin. Food Science and Biotechnology, 19(4), 957–965.

    Article  CAS  Google Scholar 

  • Costa, A. M. M., Nunes, J. C., Lima, B. N. B., Pedrosa, C., Calado, V., Torres, A. G., & Pierucci, A. P. T. R. (2015). Effective stabilization of CLA by microencapsulation in pea protein. Food Chemistry, 168, 157–166.

    Article  CAS  PubMed  Google Scholar 

  • Do Nascimento, T. G., da Silva, P. F., Azevedo, L. F., da Rocha, L. G., Porto, I. C. C. de M., Lima e Moura, T. F. A. et al. (2016). Polymeric nanoparticles of Brazilian red propolis extract: preparation, characterization, antioxidant and Leishmanicidal activity. Nanoscale Research Letters, 11 (301). DOI https://doi.org/10.1186/s11671-016-1517-3.

  • Donhowe, E. G., Flores, F. P., Kerr, W. L., Wicker, L., & Kong, F. (2014). Characterization and in vitro bioavailability of β-carotene: effects of microencapsulation method and food matrix. Lebens Wiss Techn (LWT), 57(1), 42–48.

    Article  CAS  Google Scholar 

  • dos Reis, A. S., Diedrich, C., de Moura, C., Pereira, D., Almeida, J. d. F., da Silva, L. D., et al. (2017). Physico-chemical characteristics of microencapsulated propolis co-product extract and its effect on storage stability of burger meat during storage at 15 °C. Lebens Wiss Techn (LWT), 76 (B), 76, 306–313.

    Article  CAS  Google Scholar 

  • Elbaz, N. M., Khalil, I. A., Abd-Rabou, A. A., & El-Sherbiny, I. M. (2016). Chitosan-based nano-in-microparticle carriers for enhanced oral delivery and anticancer activity of propolis. International Journal of Biological Macromolecules, 92, 254–269.

    Article  CAS  PubMed  Google Scholar 

  • Fang, Z., & Bhandari, B. (2012). Comparing the efficiency of protein and maltodextrin on spray drying of bayberry juice. Food Research International, 48(2), 478–483.

    Article  CAS  Google Scholar 

  • Ghorbanzade, T., Jafari, S. M., Akhavan, S., & Hadavi, R. (2017). Nano-encapsulation of fish oil in nano-liposomes and its application in fortification of yogurt. Food Chemistry, 216, 146–152.

    Article  CAS  PubMed  Google Scholar 

  • Graikou, K., Popova, M., Gortzi, O., Bankova, V., & Chinou, I. (2016). Characterization and biological evaluation of selected Mediterranean propolis samples. Is it a new type? Lebens Wiss Techn (LWT), 65, 261–267.

    Article  CAS  Google Scholar 

  • Gutiérrez, T. J., Álvarez, K. (2017). Biopolymers as microencapsulation materials in the food industry. In: Advances in Physicochemical Properties of Biopolymers: Part 2. Martin Masuelli, and Denis Renard (Eds). Bentham Science Publishers. EE.UU. ISBN: 978–1–68108-545-6. E ISBN: 978–1–68108-544-9, 2017. pp. 296–322. doi: https://doi.org/10.2174/9781681085449117010009.

  • Hao, Z., Yuying, F., Fuge, N., Zeya, L., Chujie, B., Bing, J., Guowen, C., & Xiaomeng, L. (2018). Enhanced antioxidant activity and in vitro release of propolis by acid-induced aggregation using heat-denatured zein and carboxymethyl chitosan. Food Hydrocolloids, 81, 104–112.

    Article  CAS  Google Scholar 

  • Hoffmann, J. F., Zandoná, G. P., Santos, P. S. D., Dallmann, C. M., Madruga, F. B., Rombaldi, C. V., & Chaves, F. C. (2017). Stability of bioactive compounds in butiá (Butia odorata) fruit pulp and nectar. Food Chemistry, 237, 638–644.

    Article  CAS  PubMed  Google Scholar 

  • IBGE - Brazilian Institute of Geography and Statistics. Apiculture. (2013). http://www.ibge.gov.br/home/estatistica/pesquisas/sintese.php./ Accessed 11 May 2017.

  • Jayasundera, M., Adhikari, B., Adhikari, R., & Aldred, P. (2011a). The effect of protein types and low molecular weight surfactants on spray drying of sugar-rich foods. Food Hydrocolloids, 25(3), 459–469.

    Article  CAS  Google Scholar 

  • Jayasundera, M., Adhikari, B., Adhikari, R., & Aldred, P. (2011b). The effects of proteins and low molecular weight surfactants on spray drying of model sugar-rich foods: powder production and characterisation. Journal of Food Engineering, 104(2), 259–271.

    Article  CAS  Google Scholar 

  • Jia, Z., Dumont, M.-J., & Orsat, V. (2016). Encapsulation of phenolic compounds presentin plants using protein matrices. Food Bioscience, 15, 87–104.

    Article  CAS  Google Scholar 

  • Joye, I. J., & McClements, D. J. (2014). Biopolymer-based nanoparticles and microparticles: fabrication, characterization, and application. Current Opinionin Colloid InterfaceScience, 19(5), 417–427.

    Article  CAS  Google Scholar 

  • Kuck, L. S., & Noreña, C. P. Z. (2016). Microencapsulation of grape (Vitis labrusca var. Bordo) skin phenolic extract using gum Arabic, polydextrose, and partially hydrolyzed guar gum as encapsulating agents. Food Chemistry, 194, 569–576.

    Article  CAS  PubMed  Google Scholar 

  • Kuck, L. S., Wesolowski, J. L., & Noreña, C. P. Z. (2017). Effect of temperature and relative humidity on stability following simulated gastro-intestinal digestion of microcapsules of Bordo grape skin phenolic extract produced with different carrier agents. Food Chemistry, 230, 257–264.

    Article  CAS  PubMed  Google Scholar 

  • Malheiros, P. d. S., Sant’Anna, V., Barbosa, M. d. S., Brandelli, A., & Franco, B. D. G. d. M. (2012). Effect of liposome-encapsulated nisin and bacteriocin-like substance P34 on Listeria monocytogenes growth in minas frescal cheese. International Journal of Food Microbiology, 156(3), 272–277.

    Article  CAS  Google Scholar 

  • Maruf, A., Mst., S. A., Jin-Cheol, L., & Jong-Bang, E. (2010). Encapsulation by spray drying of bioactive components, physicochemical and morphological properties from purple sweet potato. Lebens Wiss Techn (LWT), 43, 1307–1312.

  • Moser, P., Telis, V. R. N., Neves, N. d. A., García-Romero, E., Gómez-Alonso, S., & Hermosín-Gutiérrez, I. (2017). Storage stability of phenolic compounds in powdered BRS Violeta grape juice microencapsulated with protein and maltodextrin blends. Food Chemistry, 214, 308–318.

    Article  CAS  PubMed  Google Scholar 

  • Nesterenko, A., Alric, I., Silvestre, F., & Durrieu, V. (2013). Review. Vegetable proteins in microencapsulation: a review of recent interventions and their effectiveness. Industrial Crops and Products, 42, 469–479.

    Article  CAS  Google Scholar 

  • Neto, R. M. S., Tintino, S. R., da Silva, A. R. P., Costa, M. d. S., Boligon, A. A., Matias, E. F. F., et al. (2017). Seasonal variation of Brazilian red propolis: antibacterial activity, synergistic effect and phytochemical screening. Food and Chemical Toxicology, 107, 572–580.

    Article  CAS  Google Scholar 

  • Nori, M. P., Favaro-Trindade, C. S., Alencar, S. M., Thomazini, M., Balieiro, J. C. C., & Castillo, C. J. C. (2011). Microencapsulation of propolis extract by complex coacervation. Lebens Wiss Techn (LWT), 44(2), 429–435.

    Article  CAS  Google Scholar 

  • Pierucci, P. T. R., Andrade, L. R., Farina, M., Pedrosa, C., & Rocha-Leão, M. H. M. (2007). Comparison of α-tocopherol microparticles produced with different wall materials: pea protein a new interesting alternative. Journal of Microencapsulation, 24(3), 201–213.

    Article  CAS  PubMed  Google Scholar 

  • Rosseto, H. C., de Toledo, L. de A. S., de Francisco, L. M. B., Esposito, E., Lim, Y., Valacchi, G. et al. (2017). Nanostructured lipid systems modified with waste material of propolis for wound healing: design, in vitro and in vivo evaluation. Colloids and Surfaces B: Biointerfaces, 158, 441–452.

  • Shang-Jung, Y., Jia-Jiuan, W., Yuan-Chuen, W., Chih-Feng, H., Tzong-Ming, W., Chwen-Jen, S., & Chieh-Ming, J. C. (2014). Encapsulation of propolis flavonoids in a water soluble polymer using pressurized carbon dioxide anti-solvent crystallization. The Journal of Supercritical Fluids, 94, 138–146.

    Article  CAS  Google Scholar 

  • Silva, J. C., Rodrigues, S., Feás, X., & Estevinho, L. M. (2012). Antimicrobial activity, phenolic profile and role in the inflammation of propolis. Food and Chemical Toxicology, 50(5), 1790–1795.

    Article  CAS  PubMed  Google Scholar 

  • da Silva, F. C., da Fonseca, C. R., de Alencar, S. M., Thomazini, M., Balieiro, J. C. d. C., Pittia, P., & Favaro-Trindade, C. S. (2013). Assessment of production efficiency, physicochemical properties and storage stability of spray-dried propolis, a natural food additive, using gum Arabic and OSA starch-based carrier systems. Food and Bioproducts Processing, 91(1), 28–36.

    Article  CAS  Google Scholar 

  • Singleton, V. L., Orthofer, R., & Lamuela-Raventós, R. M. (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods in Enzymology, 299, 152–178.

    Article  CAS  Google Scholar 

  • Siripatrawan, U., & Vitchayakitti, W. (2016). Improving functional properties of chitosan films as active food packaging by incorporating with propolis. Food Hydrocolloids, 61, 695–702.

    Article  CAS  Google Scholar 

  • Spinelli, S., Conte, A., Lecce, L., Incoronato, A. L., & Nobile, A. D. M. (2015). Microencapsulated propolis to enhance the antioxidant properties of fresh fish burgers. Journal of Food Process Engineering, 38(6), 527–535.

    Article  CAS  Google Scholar 

  • Sritham, E., & Gunasekaran, S. (2016). Thermal evaluation of sucrose-maltodextrin-sodium citrate bioglass: glass transition temperature. Food Hydrocolloids, 60, 589–597.

    Article  CAS  Google Scholar 

  • Stone, A. K., Karalash, A., Tyler, R. T., Warkentin, T. D., & Nickerson, M. T. (2015). Functional attributes of pea protein isolates prepared using different extraction methods and cultivars. Food Research International, 76, 31–38.

    Article  CAS  Google Scholar 

  • Tan, C., Zhang, Y., Abbas, S., Feng, B., Zhang, X., & Xia, S. (2014). Modulation of the carotenoid bioaccessibility through liposomal encapsulation. Colloids and Surfaces B: Biointerfaces, 123, 692–700.

    Article  CAS  PubMed  Google Scholar 

  • Tarhinia, M., Greige-Gerges, H., & Elaissaria, A. (2017). Review. Protein-based nanoparticles: from preparation to encapsulation of active molecules. International Journal of Pharmaceutics, 522, 172–197.

    Article  CAS  Google Scholar 

  • Visentini, F. F., Sponton, O. E., Perez, A. A., & Santiago, L. G. (2017). Formation and colloidal stability of ovalbumin-retinol nanocomplexes. Food Hydrocolloids, 67, 130–138.

    Article  CAS  Google Scholar 

  • Waller, S. B., Peter, C. M., Hoffmann, J. S., Picoli, T., Osorio, L. d. G., Chaves, F., et al. (2017). Chemical and cytotoxic analyses of brown Brazilian propolis (Apis mellifera) and its in vitro activity against itraconazole resistant Sporothrix brasiliensis. Microbial Pathogenesis, 105, 117–121.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank CAPES for granting the doctoral scholarship, FAPERGS for the financial support, to the CEME-SUL (FURG) by the SEM analysis and Center for Development, and to the Control of Biomaterials (CDC-Bio/UFPel) by the ATR-FTIR.

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Authors and Affiliations

  1. Department of Agroindustril Science and Technology, Faculty of Agronomy Eliseu Maciel, Federal University of Pelotas, PO Box 96010-900, Pelotas, RS, Brazil

    Cristina Jansen-Alves, Karina F. Fernandes, Michele M. Crizel-Cardozo & Fernanda D. Krumreich

  2. Center of Chemical, Pharmaceuticals and Food Sciences, Federal University of Pelotas, Pelotas, RS, Brazil

    Caroline D. Borges & Rui C. Zambiazi

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  1. Cristina Jansen-Alves
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  2. Karina F. Fernandes
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  3. Michele M. Crizel-Cardozo
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Correspondence to Cristina Jansen-Alves.

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Jansen-Alves, C., Fernandes, K.F., Crizel-Cardozo, M.M. et al. Microencapsulation of Propolis in Protein Matrix Using Spray Drying for Application in Food Systems. Food Bioprocess Technol 11, 1422–1436 (2018). https://doi.org/10.1007/s11947-018-2115-4

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  • DOI: https://doi.org/10.1007/s11947-018-2115-4

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