Abstract
The aim of this study was to evaluate and compare the efficiency of bovine (CW) and buffalo cheese whey (BCW) as encapsulating agents for the spray-drying (SD) of endogenous Lactobacillus pentosus ML 82 and the reference strain Lactobacillus plantarum ATCC 8014. Their protective features were also tested for resistance to storage (90 days, 25 °C), simulated gastrointestinal tract (GIT) conditions, and for their application in orange juice. Survival rates after SD were approximately 95% in all samples tested, meaning both CW and BCW performed satisfactorily. After 90 days of storage, both species remained above 7 log Colony Forming Units (CFU)/g. However, CW generally enabled higher bacterial viability throughout this period. CW microcapsule characteristics were also more stable, which is indicated by the fact that BCW had higher moist content. Under GIT conditions, encapsulated lactobacilli had higher survival rates than free cells regardless of encapsulating agent. Even so, results indicate that CW and BCW perform better under gastric conditions than intestinal conditions. Regarding their use in orange juice, coating materials were probably dissolved due to low pH, and both free and encapsulated bacteria had similar survival rates. Overall, CW and BCW are suitable encapsulating agents for lactic acid bacteria, as they provided protection during storage and against harmful GIT conditions.
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References
Agostini C, Eckert C, Vincenzi A et al (2018) Characterization of technological and probiotic properties of indigenous Lactobacillus spp. from south Brazil. 3 Biotech 8:451. https://doi.org/10.1007/s13205-018-1469-7
Angmo K, Kumari A, Savitri BTC (2016) Probiotic characterization of lactic acid bacteria isolated from fermented foods and beverage of Ladakh. LWT Food Sci Technol 66:428–435. https://doi.org/10.1016/J.LWT.2015.10.057
AOAC International (2012) Official methods of analysis of AOAC International, 19th edn. AOAC International, Gaithersburg
Asteri I-A, Kittaki N, Tsakalidou E (2010) The effect of wild lactic acid bacteria on the production of goat’s milk soft cheese. Int J Dairy Technol 63:234–242. https://doi.org/10.1111/j.1471-0307.2010.00564.x
Behboudi-Jobbehdar S, Soukoulis C, Yonekura L, Fisk I (2013) Optimization of spray-drying process conditions for the production of maximally viable microencapsulated L. acidophilus NCIMB 701748. Dry Technol 31:1274–1283. https://doi.org/10.1080/07373937.2013.788509
Brinques GB, Peralba MC, Ayub MAZ (2010) Optimization of probiotic and lactic acid production by Lactobacillus plantarum in submerged bioreactor systems. J Ind Microbiol Biotechnol 37:205–212. https://doi.org/10.1007/s10295-009-0665-1
Buffoni JN, Bonizzi I, Pauciullo A et al (2011) Characterization of the major whey proteins from milk of Mediterranean water buffalo (Bubalus bubalis). Food Chem 127:1515–1520. https://doi.org/10.1016/J.FOODCHEM.2011.02.008
Buzi KA, Pinto JPAN, Ramos PRR, Biondi GF (2009) Microbiological analysis and electrophoretic characterization of mozzarella cheese made from buffalo milk. Ciência e Tecnol Aliment 29:07–11. https://doi.org/10.1590/S0101-20612009000100002
Caggia C, De Angelis M, Pitino I et al (2015) Probiotic features of Lactobacillus strains isolated from Ragusano and Pecorino Siciliano cheeses. Food Microbiol 50:109–117. https://doi.org/10.1016/J.FM.2015.03.010
Carvalho F, Prazeres AR, Rivas J (2013) Cheese whey wastewater: characterization and treatment. Sci Total Environ 445–446:385–396. https://doi.org/10.1016/J.SCITOTENV.2012.12.038
Champagne CP, Gomes da Cruz A, Daga M (2018) Strategies to improve the functionality of probiotics in supplements and foods. Curr Opin Food Sci 22:160–166. https://doi.org/10.1016/J.COFS.2018.04.008
Chlebowska-Smigiel A, Gniewosz M, Kieliszek M, Bzducha-Wrobel A (2017) The effect of pullulan on the growth and acidifying activity of selected stool microflora of human. Curr Pharm Biotechnol 18:121–126. https://doi.org/10.2174/1389201017666161229154324
Chlebowska-Śmigiel A, Kycia K, Neffe-Skocińska K et al (2019) Effect of pullulan on physicochemical, microbiological, and sensory quality of yogurts. Curr Pharm Biotechnol 20:489–496. https://doi.org/10.2174/1389201020666190416151129
Chudy S, Pikul J, Rudzińska M (2015) Effects of storage on lipid oxidation in milk and egg mixed powder. J Food Nutr Res 54:31–40
da Silva PT, Fries LLM, de Menezes CR et al (2014) Microencapsulation: concepts, mechanisms, methods and some applications in food technology. Ciência Rural 44:1304–1311. https://doi.org/10.1590/0103-8478cr20130971
de Andrade DP, Ramos CL, Botrel DA et al (2019) Stability of microencapsulated lactic acid bacteria under acidic and bile juice conditions. Int J Food Sci Technol 54:2355–2362. https://doi.org/10.1111/ijfs.14114
De Castro-Cislaghi FP, Silva CDRE, Fritzen-Freire CB et al (2012) Bifidobacterium Bb-12 microencapsulated by spray drying with whey: survival under simulated gastrointestinal conditions, tolerance to NaCl, and viability during storage. J Food Eng 113:186–193. https://doi.org/10.1016/j.jfoodeng.2012.06.006
Del Piano M, Carmagnola S, Ballarè M et al (2011) Is microencapsulation the future of probiotic preparations? The increased efficacy of gastro-protected probiotics. Gut Microbes 2:120–123. https://doi.org/10.4161/gmic.2.2.15784
Domingos-Lopes MFP, Stanton C, Ross PR et al (2017) Genetic diversity, safety and technological characterization of lactic acid bacteria isolated from artisanal Pico cheese. Food Microbiol 63:178–190. https://doi.org/10.1016/J.FM.2016.11.014
Đorđević V, Balanč B, Belščak-Cvitanović A et al (2014) Trends in encapsulation technologies for delivery of food bioactive compounds. Food Eng Rev 7:452–490. https://doi.org/10.1007/s12393-014-9106-7
Duongthingoc D, George P, Katopo L et al (2013) Effect of whey protein agglomeration on spray dried microcapsules containing Saccharomyces boulardii. Food Chem 141:1782–1788. https://doi.org/10.1016/J.FOODCHEM.2013.04.093
Eckert C, Agnol WD, Dallé D et al (2018) Development of alginate-pectin microparticles with dairy whey using vibration technology: effects of matrix composition on the protection of Lactobacillus spp. from adverse conditions. Food Res Int 113:65–73. https://doi.org/10.1016/j.foodres.2018.07.001
Eckert C, Serpa VG, Felipe dos Santos AC et al (2017) Microencapsulation of Lactobacillus plantarum ATCC 8014 through spray drying and using dairy whey as wall materials. LWT Food Sci Technol 82:176–183. https://doi.org/10.1016/j.lwt.2017.04.045
Euromonitor International (2016) Probiotics: Evolution of digestion and immune support probiotics. Euromonitor International Global Head of Health and Wellness Research. https://www.euromonitor.com/probiotics-evolution-of-digestion-and-immune-support-probiotics-part-one/report. Accessed 17 Sept 2019
FAO/WHO (2002) Guidelines for the evaluation of probiotics in food. Joint FAO/WHO Work Group Rep Draft Guide Eval Probiot Food. https://doi.org/10.1111/j.1469-0691.2012.03873
Farimani RH, Najafi MBH, Bazzaz BSF et al (2016) Identification, typing and functional characterization of dominant lactic acid bacteria strains from Iranian traditional yoghurt. Eur Food Res Technol 242:517–526. https://doi.org/10.1007/s00217-015-2562-3
Favaro-Trindade CS, Santana AS, Monterrey-Quintero ES et al (2010) The use of spray drying technology to reduce bitter taste of casein hydrolysate. Food Hydrocoll 24:336–340. https://doi.org/10.1016/J.FOODHYD.2009.10.012
Ferrando V, Quiberoni A, Reinheimer J, Suárez V (2016) Functional properties of Lactobacillus plantarum strains: a study in vitro of heat stress influence. Food Microbiol 54:154–161. https://doi.org/10.1016/J.FM.2015.10.003
Fox PF, Uniacke-Lowe T, McSweeney PLH, O’Mahony JA (2015) Heat-induced changes in milk. In: Dairy Chemistry and Biochemistry. Springer International Publishing, Cham, pp 345–375. https://doi.org/10.1007/978-3-319-14892-2_9
Gallego-Schmid A, Tarpani RRZ (2019) Life cycle assessment of wastewater treatment in developing countries: a review. Water Res 153:63–79. https://doi.org/10.1016/J.WATRES.2019.01.010
Ghandi A, Powell IB, Chen XD, Adhikari B (2012) The Effect of dryer inlet and outlet air temperatures and protectant solids on the survival of Lactococcus lactis during spray drying. Dry Technol 30:1649–1657. https://doi.org/10.1080/07373937.2012.703743
Golowczyc MA, Silva J, Teixeira P et al (2011) Cellular injuries of spray-dried Lactobacillus spp. isolated from kefir and their impact on probiotic properties. Int J Food Microbiol 144:556–560. https://doi.org/10.1016/j.ijfoodmicro.2010.11.005
Greifová G, Májeková H, Greif G et al (2017) Analysis of antimicrobial and immunomodulatory substances produced by heterofermentative Lactobacillus reuteri. Folia Microbiol (Praha) 62:515–524. https://doi.org/10.1007/s12223-017-0524-9
Guergoletto KB, Busanello M, Garcia S (2017) Influence of carrier agents on the survival of Lactobacillus reuteri LR92 and the physicochemical properties of fermented juçara pulp produced by spray drying. LWT 80:321–327. https://doi.org/10.1016/J.LWT.2017.02.038
Guerreiro J, Monteiro V, Ramos C et al (2014) Lactobacillus pentosus B231 isolated from a Portuguese PDO cheese: production and partial characterization of its bacteriocin. Probiotics Antimicrob Proteins 6:95–104. https://doi.org/10.1007/s12602-014-9157-3
Heidebach T, Först P, Kulozik U (2012) Microencapsulation of probiotic cells for food applications. Crit Rev Food Sci Nutr 52:291–311. https://doi.org/10.1080/10408398.2010.499801
Ho TM, Chan S, Yago AJE et al (2019) Changes in physicochemical properties of spray-dried camel milk powder over accelerated storage. Food Chem 295:224–233. https://doi.org/10.1016/J.FOODCHEM.2019.05.122
Huang S, Rabah H, Jardin J et al (2016) Hyperconcentrated sweet whey, a new culture medium that enhances Propionibacterium freudenreichii stress tolerance. Appl Environ Microbiol 82:4641–4651. https://doi.org/10.1128/AEM.00748-16
Huang S, Méjean S, Rabah H et al (2017) Double use of concentrated sweet whey for growth and spray drying of probiotics: towards maximal viability in pilot scale spray dryer. J Food Eng 196:11–17. https://doi.org/10.1016/j.jfoodeng.2016.10.017
Hugo AA, Bruno F, Golowczyc M (2016) Whey permeate containing galacto-oligosaccharides as a medium for biomass production and spray drying of Lactobacillus plantarum CIDCA 83114. LWT Food Sci Technol 69:185–190. https://doi.org/10.1016/j.lwt.2016.01.031
ITAL (2017) Brasil dairy trends 2020: Tendências do mercado de produtos lácteos, 1st edn. ITAL, Campinas
Jeong JJ, Kim KA, Jang SE et al (2015) Orally administrated Lactobacillus pentosus var. plantarum C29 ameliorates age-dependent colitis by inhibiting the nuclear factor-kappa B signaling pathway via the regulation of lipopolysaccharide production by gut microbiota. PLoS ONE 10:e0116533. https://doi.org/10.1371/journal.pone.0116533
Khem S, Small DM, May BK (2016a) The behaviour of whey protein isolate in protecting Lactobacillus plantarum. Food Chem 190:717–723. https://doi.org/10.1016/j.foodchem.2015.06.020
Khem S, Bansal V, Small DM, May BK (2016b) Comparative influence of pH and heat on whey protein isolate in protecting Lactobacillus plantarum A17 during spray drying. Food Hydrocoll 54:162–169. https://doi.org/10.1016/j.foodhyd.2015.09.029
Kim S-J, Cho SY, Kim SH et al (2008) Effect of microencapsulation on viability and other characteristics in Lactobacillus acidophilus ATCC 43121. LWT Food Sci Technol 41:493–500. https://doi.org/10.1016/J.LWT.2007.03.025
Lavari L, Ianniello R, Páez R et al (2015) Growth of Lactobacillus rhamnosus 64 in whey permeate and study of the effect of mild stresses on survival to spray drying. LWT Food Sci Technol 63:322–330. https://doi.org/10.1016/j.lwt.2015.03.066
Li L, Han NS (2018) Application of lactic acid bacteria for food biotechnology. In: Emerging Areas in Bioengineering. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany, pp 375–398. https://doi.org/10.1002/9783527803293.ch22
Liao LK, Wei XY, Gong X et al (2017) Microencapsulation of Lactobacillus casei LK-1 by spray drying related to its stability and in vitro digestion. LWT Food Sci Technol 82:82–89. https://doi.org/10.1016/j.lwt.2017.03.065
Lima ACD, Cecatti C, Fidélix MP et al (2019) Effect of daily consumption of orange juice on the levels of blood glucose, lipids, and gut microbiota metabolites: controlled clinical trials. J Med Food 22:202–210. https://doi.org/10.1089/jmf.2018.0080
Lira HL, da Silva MCD, Vasconcelos MRS et al (2009) Microfiltração do soro de leite de búfala utilizando membranas cerâmicas como alternativa ao processo de pasteurização. Ciência e Tecnol Aliment 29:33–37. https://doi.org/10.1590/s0101-20612009000100006
Liu Y, Xie XX, Ibrahim SA et al (2016) Characterization of Lactobacillus pentosus as a starter culture for the fermentation of edible oyster mushrooms (Pleurotus spp.). LWT Food Sci Technol 68:21–26. https://doi.org/10.1016/j.lwt.2015.12.008
Maciel GM, Chaves KS, Grosso CRF, Gigante ML (2014) Microencapsulation of Lactobacillus acidophilus La-5 by spray-drying using sweet whey and skim milk as encapsulating materials. J Dairy Sci 97:1991–1998. https://doi.org/10.3168/jds.2013-7463
Mangia NP, Murgia MA, Garau G et al (2013) Suitability of selected autochthonous lactic acid bacteria cultures for Pecorino Sardo Dolce cheese manufacturing: influence on microbial composition, nutritional value and sensory attributes. Int J Dairy Technol 66:543–551. https://doi.org/10.1111/1471-0307.12072
Marco ML, Heeney D, Binda S et al (2017) Health benefits of fermented foods: microbiota and beyond. Curr Opin Biotechnol 44:94–102. https://doi.org/10.1016/j.copbio.2016.11.010
MarketResearch (2016) The world cheese market report 2000–2023. https://pmfood.dk/upl/9735/WCMINFORMATION.pdf. Accessed 17 Sept 2019
Martín MJ, Lara-Villoslada F, Ruiz MA, Morales ME (2015) Microencapsulation of bacteria: a review of different technologies and their impact on the probiotic effects. Innov Food Sci Emerg Technol 27:15–25. https://doi.org/10.1016/j.ifset.2014.09.010
Mollea C, Marmo L, Bosco F (2013) Valorisation of cheese whey, a by-product from the dairy industry. Food Ind. https://doi.org/10.5772/53159
Moncmanová A (2007) Environmental factors that influence the deterioration of materials. In: Environmental Deterioration of Materials. WIT Press, United Kingdom, pp 1–25. https://doi.org/10.2495/978-1-84564-032-3/01
Motta ADS, Gomes MDSM (2015) Technological and functional properties of lactic acid bacteria: the importance of these microorganisms for food. Rev do Inst Laticínios Cândido Tostes 70:172. https://doi.org/10.14295/2238-6416.v70i3.403
Nunes GL, Motta MH, Cichoski AJ et al (2018) Encapsulation of lactobacillus acidophilus la-5 and bifidobacterium bb-12 by spray drying and evaluation of its resistance in simulated gastrointestinal conditions, thermal treatments and storage conditions. Cienc Rural 48:1–11. https://doi.org/10.1590/0103-8478cr20180035
Palombo R, Gertler A, Saguy I (1984) A simplified method for determination of browning in dairy powders. J Food Sci 49:1609–1609. https://doi.org/10.1111/j.1365-2621.1984.tb12855.x
Pérez-Chabela ML, Lara-Labastida R, Rodriguez-Huezo E, Totosaus A (2013) Effect of spray drying encapsulation of thermotolerant lactic acid bacteria on meat batters properties. Food Bioprocess Technol 6:1505–1515. https://doi.org/10.1007/s11947-012-0865-y
Pérez Montoro B, Benomar N, Caballero Gómez N et al (2018) Proteomic analysis of Lactobacillus pentosus for the identification of potential markers of adhesion and other probiotic features. Food Res Int 111:58–66. https://doi.org/10.1016/j.foodres.2018.04.072
Picon A, Garde S, Ávila M, Nuñez M (2016) Microbiota dynamics and lactic acid bacteria biodiversity in raw goat milk cheeses. Int Dairy J 58:14–22. https://doi.org/10.1016/j.idairyj.2015.09.010
Pinto SS, Fritzen-Freire CB, Benedetti S et al (2015a) Potential use of whey concentrate and prebiotics as carrier agents to protect Bifidobacterium-BB-12 microencapsulated by spray drying. Food Res Int 67:400–408. https://doi.org/10.1016/J.FOODRES.2014.11.038
Pinto SS, Verruck S, Vieira CRWW et al (2015b) Influence of microencapsulation with sweet whey and prebiotics on the survival of Bifidobacterium-BB-12 under simulated gastrointestinal conditions and heat treatments. LWT Food Sci Technol 64:1004–1009. https://doi.org/10.1016/j.lwt.2015.07.020
Rajam R, Karthik P, Parthasarathi S et al (2012) Effect of whey protein-alginate wall systems on survival of microencapsulated Lactobacillus plantarum in simulated gastrointestinal conditions. J Funct Foods 4:891–898. https://doi.org/10.1016/j.jff.2012.06.006
Rama G, Kuhn D, Beux S et al (2019a) Cheese whey and ricotta whey for the growth and encapsulation of endogenous lactic acid bacteria. Food Bioprocess Technol 13:308–322. https://doi.org/10.1007/s11947-019-02395-8
Rama GR, Kuhn D, Beux S et al (2019b) Potential applications of dairy whey for the production of lactic acid bacteria cultures. Int Dairy J 98:25–37. https://doi.org/10.1016/j.idairyj.2019.06.012
Ranadheera CS, Evans CA, Adams MC, Baines SK (2014) Effect of dairy probiotic combinations on in vitro gastrointestinal tolerance, intestinal epithelial cell adhesion and cytokine secretion. J Funct Foods 8:18–25. https://doi.org/10.1016/J.JFF.2014.02.022
Ranadheera CS, Evans CA, Adams MC, Baines SK (2015) Microencapsulation of Lactobacillus acidophilus LA-5, Bifidobacterium animalis subsp. lactis BB-12 and Propionibacterium jensenii 702 by spray drying in goat’s milk. Small Rumin Res 123:155–159. https://doi.org/10.1016/j.smallrumres.2014.10.012
Rodríguez-Huezo ME, Durán-Lugo R, Prado-Barragán LA et al (2007) Pre-selection of protective colloids for enhanced viability of Bifidobacterium bifidum following spray-drying and storage, and evaluation of aguamiel as thermoprotective prebiotic. Food Res Int 40:1299–1306. https://doi.org/10.1016/J.FOODRES.2007.09.001
Rokka S, Rantamäki P (2010) Protecting probiotic bacteria by microencapsulation: challenges for industrial applications. Eur Food Res Technol 231:1–12. https://doi.org/10.1007/s00217-010-1246-2
Román A, Wang J, Csanádi J et al (2011) Experimental investigation of the sweet whey concentration by nanofiltration. Food Bioprocess Technol 4:702–709. https://doi.org/10.1007/s11947-009-0192-0
Rushdy AA, Gomaa EZ (2013) Antimicrobial compounds produced by probiotic Lactobacillus brevis isolated from dairy products. Ann Microbiol 63:81–90. https://doi.org/10.1007/s13213-012-0447-2
Sales DC, Rangel AHN, Urbano SA et al (2017) Buffalo milk composition, processing factors, whey constituents recovery and yield in manufacturing Mozzarella cheese. Food Sci Technol 38:328–334. https://doi.org/10.1590/1678-457x.04317
Sansonetti S, Curcio S, Calabrò V, Iorio G (2009) Bio-ethanol production by fermentation of ricotta cheese whey as an effective alternative non-vegetable source. Biomass Bioenerg 33:1687–1692. https://doi.org/10.1016/j.biombioe.2009.09.002
Sasikumar R, Das M, Sahu JK, Deka SC (2020) Qualitative properties of spray-dried blood fruit (Haematocarpus validus) powder and its sorption isotherms. J Food Process Eng. https://doi.org/10.1111/jfpe.13373
Tofalo R, Perpetuini G, Schirone M et al (2014) Lactobacillus pentosus dominates spontaneous fermentation of Italian table olives. LWT Food Sci Technol 57:710–717. https://doi.org/10.1016/j.lwt.2014.01.035
Tonon RV, Brabet C, Pallet D et al (2009) Physicochemical and morphological characterisation of açai (Euterpe oleraceae Mart.) powder produced with different carrier agents. Int J Food Sci Technol 44:1950–1958. https://doi.org/10.1111/j.1365-2621.2009.02012.x
Tripathi MK, Giri SK (2014) Probiotic functional foods: survival of probiotics during processing and storage. J Funct Foods 9:225–241. https://doi.org/10.1016/J.JFF.2014.04.030
Wang G, Li D, Ma X et al (2015) Functional role of oppA encoding an oligopeptide-binding protein from Lactobacillus salivarius Ren in bile tolerance. J Ind Microbiol Biotechnol 42:1167–1174. https://doi.org/10.1007/s10295-015-1634-5
Wu C, He G, Zhang J (2014) Physiological and proteomic analysis of Lactobacillus casei in response to acid adaptation. J Ind Microbiol Biotechnol 41:1533–1540. https://doi.org/10.1007/s10295-014-1487-3
Zhu Y-H, Li X-Q, Zhang W et al (2014) Dose-dependent effects of Lactobacillus rhamnosus on serum interleukin-17 production and intestinal T-cell responses in pigs challenged with Escherichia coli. Appl Environ Microbiol 80:1787–1798. https://doi.org/10.1128/AEM.03668-13
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We are grateful to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for providing the scholarship [Grant: 311655/2017-3]. We also thank Launer Química Indústria e Comércio Ltda, Tecnovates, and Universidade do Vale do Taquari—Univates for their financial support.
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All authors contributed with study conception and design. Material preparation, data collection and analysis were performed by AJF and JABSS. The first draft of the manuscript was written by GRRand all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Rama, G.R., Führ, A.J., da Silva, J.A.B.S. et al. Encapsulation of Lactobacillus spp. using bovine and buffalo cheese whey and their application in orange juice. 3 Biotech 10, 263 (2020). https://doi.org/10.1007/s13205-020-02255-9
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DOI: https://doi.org/10.1007/s13205-020-02255-9