Abstract
Microencapsulation of partially purified microbial transglutaminase (mTG) was investigated using ultrasonic spray-freeze drying (USFD), and the optimum coating materials (gum arabic, maltodextrin, inulin) ratio and the process parameters (flow rate and nozzle frequency) were determined using a D-optimal combined design. Also, the microencapsulated samples by USFD were compared with microencapsulated samples by conventional freeze drying (CFD) and conventional spray drying (CSD) in terms of microencapsulation efficiency, enzyme stability at extreme pH and high temperature conditions, and the presence of metal ions, physical (moisture content, particle morphology, particle and pore size, surface area, pore volume distribution, density and flow properties, caking degree, color), and reconstitution (wettability and solubility) properties. As a result, the optimum coating materials composition was determined as 60% gum arabic and 40% inulin, and process conditions were found to be flow rate of 6.83 ml/min and nozzle frequency of 48 kHz applying desirability function method. Microcapsules with smaller particle size, pore volume, and porosity, with lower moisture content and good reconstitution characteristics, were obtained by USFD with a maximum microencapsulation efficiency of ~ 97%.
Similar content being viewed by others
References
Aghbashlo, M., Mobli, H., Madadlou, A., & Rafiee, S. (2013). Influence of wall material and inlet drying air temperature on the microencapsulation of fish oil by spray drying. Food and Bioprocess Technology, 6(6), 1561–1569.
Allison, S. D., Chang, B., Randolph, T. W., & Carpenter, J. F. (1999). Hydrogen bonding between sugar and protein is responsible for inhibition of dehydration-induced protein unfolding. Archives of Biochemistry and Biophysics, 365(2), 289–298.
Amid, M., Manap, Y., & Zohdi, K. N. (2014). Microencapsulation of purified amylase enzyme from pitaya (hylocereus polyrhizus) peel in arabic gum-chitosan using freeze drying. Molecules, 19, 3731–3743.
Amine, K. M., Champagne, C. P., Salmeri, S., Britten, M., St-Gelais, D., Fustier, P., & Lacroix, M. (2014). Effect of palmitoylated alginate microencapsulation on viability of Bifidobacterium longum during freeze-drying. LWT - Food Science and Technology, 56, 111–117.
Anchordoquy, T. J., Izutsu, K. I., Randolph, T. W., & Carpenter, J. F. (2001). Maintenance of quaternary structure in the frozen state stabilizes lactate dehydrogenase during freeze–drying. Archives of Biochemistry and Biophysics, 390(1), 35–41.
AOAC. (1990). Official methods for analysis (15th ed.). Arlington: Association of Official Analytical Chemists.
Bourneow, C., Benjakul, S., & H-Kittikun, A. (2012). Impact of some additives on the stability of microbial transglutaminase from Providencia sp. C1112. Asian Journal of Food and Agro-Industry, 5(3), 226–233.
Breda, M., Vitolo, M., Duranti, M. A., & Pitombo, R. N. (1992). Effect of freezing-thawing on invertase activity. Cryobiology, 29(2), 281–290.
Cano-Chauca, M., Stringheta, P. C., Ramos, A. M., & Cal-Vidal, J. (2005). Effect of the carriers on the microstructure of mango powder obtained by spray drying and its functional characterization. Innovative Food Science and Emerging Technologies, 6(4), 420–428.
Carpenter, J. F., & Crowe, J. H. (1989). An infrared spectroscopic study of the interactions of carbohydrates with dried proteins. Biochemistry, 28(9), 3916–3922.
Carr, R. L. (1965). Evaluating flow properties of solids. Chemical Engineering Journal, 72, 163–168.
Constantino, H. R., Firouzabadian, L., Wu, C., Carrasquillo, K. G., Griebenow, K., Zale, S. E., & Tracy, M. A. (2000). Protein spray freeze drying: effect of formulation variables on particle size and stability. Journal of Pharmaceutical Science, 17(11), 1374–1383.
D’Addio, S. M., Chan, J. G. Y., Kwok, P. C. L., Prud’homme, R. K., & Chan, H. K. (2012). Constant size, variable density aerosol particles by ultrasonic spray freeze drying. International Journal of Pharmaceutics, 427(2), 185–191.
De Boer, J. H. (1958). The structure and properties of porous materials. In Proceedings of the Tenth Symposium of the Colston Research Society Held in the University of Bristol (pp. 68–94). London: Butterworths.
Desai, K. G. H., & Park, H. J. (2005). Recent developments in microencapsulation of food ingredients. Drying Technology, 23, 1361–1394.
Dima, C., Pătraşcu, L., Cantaragiu, A., Alexe, P., & Dima, Ş. (2016). The kinetics of the swelling process and the release mechanisms of Coriandrum sativum L. essential oil from chitosan/alginate/inulin microcapsules. Food Chemistry, 195, 39–48.
Dolly, P., Anishaparvin, A., Joseph, G. S., & Anandharamakrishnan, C. (2011). Microencapsulation of Lactobacillus plantarum (MTCC 5422) by spray-freeze-drying method and evaluation of survival in simulated gastrointestinal conditions. Journal of Microencapsulation, 28(6), 568–574.
Eriksson, H. J. C., Hinrichs, W. L. J., van Veen, B., Somsen, G. W., de Jong, G. J., & Frijlink, H. W. (2002). Investigations into the stabilisation of drugs by sugar glasses: I. Tablets prepared from stabilised alkaline phosphatase. International Journal of Pharmaceutics, 249(1), 59–70.
Ezhilarasi, P. N., Karthik, P., Chhanwal, N., & Anandharamakrishnan, C. (2013). Nanoencapsulation techniques for food bioactive components: a review. Food and Bioprocess Technology, 6(3), 628–647.
Feng, H., Barbosa-Cánovas, G. V., & Weiss, J. (2011). Ultrasound technologies for food and bioprocessing. New York: Springer Science and Business Media, 599p.
Furlán, L. T. R., Lecot, J., Padilla, A. P., Campderrós, M. E., & Zaritzky, N. (2012). Stabilizing effect of saccharides on bovine plasma protein: A calorimetric study. Meat Science, 91(4), 478–485.
Gaspar, A. L. C., & de Góes-Favoni, S. P. (2015). Action of microbial transglutaminase (MTGase) in the modification of food proteins: A review. Food Chemistry, 171, 315–322.
Grasmeijer, N., Stankovic, M., de Waard, H., Frijlink, H. W., & Hinrichs, W. L. (2013). Unraveling protein stabilization mechanisms: vitrification and water replacement in a glass transition temperature controlled system. BBA Proteins and Proteomics, 1834(4), 763–769.
Gregg, S. J., & Sing, K. S. W. (1982). Adsorption, surface area and porosity (2nd ed.). London: Academic.
Hausner, H. H. (1967). Friction conditions in a mass of metal powder. Powder Metallurgy, 13, 7–13.
Heidebach, T., Först, P., & Kulozik, U. (2009). Influence of casein-based microencapsulation on freeze-drying and storage of probiotic cells. Journal of Food Engineering, 98, 309–316.
Heinrich, Z. (2003). Colour chemistry: syntheses, properties and applications of organic dyes and pigments. Weinheim: Wiley-VCH GmbH & Co. KGaA.
Her, J. Y., Kim, M. S., & Lee, K. G. (2015). Preparation of probiotic powder by the spray freeze-drying method. Journal of Food Engineering, 150, 70–74.
Hundre, S. Y., Karthik, P., & Anandharamakrishnan, C. (2015). Effect of whey protein isolate and β-cyclodextrin wall systems on stability of microencapsulated vanillin by spray–freeze drying method. Food Chemistry, 174, 16–24.
Ishwarya, S. P., & Anandharamakrishnan, C. (2015). Spray-freeze-drying approach for soluble coffee processing and its effect on quality characteristics. Journal of Food Engineering, 149, 171–180.
Ishwarya, S. P., Anandharamakrishnan, C., & Stapley, A. G. F. (2015). Spray-freeze-drying: a novel process for the drying of foods and bioproducts. Trends in Food Science and Technology, 41(2), 161–181.
Isleroglu, H., Turker, I., Tokatli, M., & Koc, B. (2018). Ultrasonic spray-freeze drying of partially purified microbial transglutaminase. Food and Bioproducts Processing, 111, 153–164.
Jinapong, N., Suphantharika, M., & Jamnong, P. (2008). Production of instant soymilk powders by ultrafiltration, spray drying and fluidized bed agglomeration. Journal of Food Engineering, 84(2), 194–205.
Karthik, P., & Anandharamakrishnan, C. (2013). Microencapsulation of docosahexaenoic acid by spray-freeze drying method and comparison of its stability with spray-drying and freeze-drying methods. Food and Bioprocess Technology, 6, 2780–2790.
Kumar, R., & Kar, A. (2014). Microencapsulation of nutraceuticals using spray freeze drying method: a brief review. Indo Global Journal of Pharmaceutical Sciences, 4(2), 47–51.
Kurozawa, L. E., Morassi, A. G., Vanzo, A. A., Park, K. J., & Hubinger, M. D. (2009). Influence of spray drying conditions on physicochemical properties of chicken meat powder. Drying Technology, 27(11), 1248–1257.
Labani, M. M., Rezaee, R., Saeedi, A., & Hinai, A. A. (2013). Evaluation of pore size spectrum of gas shale reservoirs using low pressure nitrogen adsorption, gas expansion and mercury porosimetry: a case study from the Perth and Canning Basins, Western Australia. Journal of Petroleum Science and Engineering, 112, 7–16.
Maa, Y. F., Nguyen, P. A., Sweeney, T., Shire, S. J., & Hsu, C. C. (1999). Protein inhalation powders: spray drying vs spray freeze drying. Pharmaceutical Research, 16(2), 249–254.
MacLeod, C., McKittrick, J., Hindmarsh, J., Johns, M., & Wilson, D. (2006). Fundamentals of spray freezing of instant coffee. Journal of Food Engineering, 74(4), 451–461.
Motoki, M., & Seguro, K. (1998). Transglutaminase and its use for food processing. Trends in Food Science and Technology, 9(5), 204–210.
Mujumdar, A. S. (2014). Handbook of Industrial Drying. Boca Raton: CRC Press.
Nesterenko, A., Alric, I., Violleau, F., Silvestre, F., & Durrieu, V. (2013). A new way of valorizing biomaterials: the use of sunflower protein for α-tocopherol microencapsulation. Food Research International, 53(1), 115–124.
Nguyen, C. X., Herberger, J. D., & Burke, A. D. (2004). Protein powders for encapsulation: a comparison of spray-freeze drying and spray drying of darbepoetin alfa. Pharmaceutical Research, 21(3), 507–513.
Niwa, T., Shimabara, H., & Danjo, K. (2010). Novel spray freeze-drying technique using four-fluid nozzle-development of organic solvent system to expand its application to poorly water soluble drugs. Chemical and Pharmaceutical Bulletin, 58(2), 195–200.
Pang, Y., Duan, X., Ren, G., & Liu, W. (2017). Comparative study on different drying methods of fish oil microcapsules. Journal of Food Quality, 2017, 1–7.
Parthasarathi, S., & Anandharamakrishnan, C. (2016). Enhancement of oral bioavailability of vitamin E by spray-freeze drying of whey protein microcapsules. Food Bioproducts and Processing, 100, 469–476.
Popović, L. M., Peričin, D. M., Vaštag, Ž. G., & Popović, S. Z. (2013). Optimization of transglutaminase cross-linking of pumpkin oil cake globulin; improvement of the solubility and gelation properties. Food and Bioprocess Technology, 6(4), 1105–1111.
Rajam, R., & Anandharamakrishnan, C. (2015). Microencapsulation of Lactobacillus plantarum (MTCC 5422) with fructooligosaccharide as wall material by spray drying. LWT-Food Science and Technology, 60(2), 773–780.
Ramos, A., Raven, N., Sharp, R. J., Bartolucci, S., Rossi, M., Cannio, R., Lebbing, J., Oost, J. V. D., de Vos, W. M., & Santos, H. (1997). Stabilization of enzymes against thermal stress and freeze-drying by mannosylglycerate. Applied and Environmental Microbiology, 63(10), 4020–4025.
Ratti, C. (2001). Hot air and freeze-drying of high-value foods: a review. Journal of Food Engineering, 49(4), 311–319.
Semyonov, D., Ramon, O., Kaplun, Z., Levin-Brener, L., Gurevich, N., & Shimoni, E. (2010). Microencapsulation of Lactobacillus paracasei by spray freeze drying. Food Research International, 43(1), 193–202.
Sonner, C., Maa, Y. F., & Lee, G. (2002). Spray-freeze-drying for protein powder preparation: particle characterization and a case study with trypsinogen stability. Journal of Pharmaceutical Sciences, 91(10), 2122–2139.
Stapley, A. G. F. (2008). Freeze drying. In J. A. Blackwell (Ed.), Frozen food science technology. Oxford: Evans.
Sun-Waterhouse, D., Wadhwa, S. S., & Waterhouse, G. I. N. (2013). Spray-drying microencapsulation of polyphenol bioactives: a comparative study using different natural fibre polymers as encapsulants. Food and Bioprocess Technology, 6(9), 2376–2388.
Tonnis, W. F., Amorij, J. P., Vreeman, M. A., Frijlink, H. W., Kersten, G. F., & Hinrichs, W. L. J. (2014). Improved storage stability and immunogenicity of hepatitis B vaccine after spray-freeze drying in presence of sugars. European Journal of Pharmaceutical Sciences, 55, 36–45.
Tonnis, W. F., Mensink, M. A., de Jager, A., van der Voort Maarschalk, K., Frijlink, H. W., & Hinrichs, W. L. J. (2015). Size and molecular flexibility of sugars determine the storage stability of freeze-dried proteins. Molecular Pharmaceutics, 12(3), 684–694.
Turker, I., Domurcuk, G., Tokatli, M., Isleroglu, H., & Koc, B. (2016). Enhancement of microbial transglutaminase production from Streptomyces sp. Ukrainian Food Journal, 5(2), 306–417.
van Drooge, D. J., Hinrichs, W. L., Dickhoff, B. H., Elli, M. N., Visser, M. R., Zijlstra, G. S., & Frijlink, H. W. (2005). Spray freeze drying to produce a stable Δ9-tetrahydrocannabinol containing inulin-based solid dispersion powder suitable for inhalation. European Journal of Pharmaceutical Sciences, 26(2), 231–240.
Wanning, S., Süverkrüp, R., & Lamprecht, A. (2015). Pharmaceutical spray freeze drying. International Journal of Pharmaceutics, 488(1), 136–153.
Yu, Z., Johnston, K. P., & Williams, R. O. (2006). Spray freezing into liquid versus spray-freeze drying: influence of atomization on protein aggregation and biological activity. European Journal of Pharmaceutical Sciences, 27(1), 9–18.
Zhang, D., Zhu, Y., & Chen, J. (2009). Microbial transglutaminase production: understanding the mechanism. Biotechnology and Genetic Engineering Reviews, 26(1), 205–222.
Funding
This study was financially supported by the Scientific and Technological Research Council of Turkey (TUBITAK, Project Number: 115O216) and Tokat Gaziosmanpasa University Scientific Research Projects (Project Number: 2016/62).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Isleroglu, H., Turker, I., Koc, B. et al. Microencapsulation of Microbial Transglutaminase by Ultrasonic Spray-Freeze Drying. Food Bioprocess Technol 12, 2004–2017 (2019). https://doi.org/10.1007/s11947-019-02353-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11947-019-02353-4