Double use of highly concentrated sweet whey to improve the biomass production and viability of spray-dried probiotic bacteria

Journal of Functional Foods

Volumn 23, Issue , 2016, Pages 453-463

  Huang, Song ^a,b,c   Cauty, Chantal ^b,c   Dolivet, Anne ^b,c   Le Loir, Yves ^b,c   Chen, Xiao Dong ^a,d   Schuck, Pierre ^b,c   Jan, Gwénaël ^b,c   Jeantet, Romain ^b,c  

^a SOOCHOW UNIVERSITY   (China)

^b UMR1253   (France)

^c AGROCAMPUS OUEST   (France)

^d XIAMEN UNIVERSITY   (China)

Author keywords

Probiotics; Spray drying; Storage; Stress tolerance; Sweet whey

Indexed keywords

EID: 84961178963     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2016.02.050     Document Type: Article

References (69)

1. Alcántara C., Blasco A., Zúñiga M., Monedero V. Accumulation of polyphosphate in lactobacillus spp. and its involvement in stress resistance. Applied and Environmental Microbiology 2014, 80(5):1650-1659. http://doi.org/10.1128/AEM.03997-13.
2. Anal A.K., Singh H. Recent advances in microencapsulation of probiotics for industrial applications and targeted delivery. Trends in Food Science & Technology 2007, 18(5):240-251. http://doi.org/10.1016/j.tifs.2007.01.004.
3. Ananta E., Volkert M., Knorr D. Cellular injuries and storage stability of spray-dried Lactobacillus rhamnosus GG. International Dairy Journal 2005, 15(4):399-409. http://doi.org/10.1016/j.idairyj.2004.08.004.
4. Barbosa J., Borges S., Teixeira P. Influence of sub-lethal stresses on the survival of lactic acid bacteria after spray-drying in orange juice. Food Microbiology 2015, 52:77-83. http://doi.org/10.1016/j.fm.2015.06.010.
5. Betoret E., Betoret N., Vidal D., Fito P. Functional foods development: Trends and technologies. Trends in Food Science & Technology 2011, 22(9):498-508. http://doi.org/10.1016/j.tifs.2011.05.004.
6. Boyaval P., Deborde C., Corre C., Blanco C., Bégué É. Stress and osmoprotection in propionibacteria. Le Lait 1999, 79(1):59-69. http://doi.org/10.1051/lait:199914.
7. Cardoso F.S., Castro R.F., Borges N., Santos H. Biochemical and genetic characterization of the pathways for trehalose metabolism in Propionibacterium freudenreichii, and their role in stress response. Microbiology (Reading, England) 2007, 153(1):270-280. http://doi.org/10.1099/mic.0.29262-0.
8. Champagne C.P., Gardner N.J., Roy D. Challenges in the addition of probiotic cultures to foods. Critical Reviews in Food Science and Nutrition 2005, 45(1):61-84. http://doi.org/10.1080/10408690590900144.
9. Chirife J., Herszage L., Joseph A., Kohn E.S. In vitro study of bacterial growth inhibition in concentrated sugar solutions: Microbiological basis for the use of sugar in treating infected wounds. Antimicrobial Agents and Chemotherapy 1983, 23(5):766-773. http://doi.org/10.1128/AAC.23.5.766.
10. Cook M.T., Tzortzis G., Charalampopoulos D., Khutoryanskiy V.V. Microencapsulation of probiotics for gastrointestinal delivery. Journal of Controlled Release 2012, 162(1):56-67. http://doi.org/10.1016/j.jconrel.2012.06.003.
11. Cousin F.J., Louesdon S., Maillard M.-B., Parayre S., Falentin H., Deutsch S.-M., Boudry G., Jan G. The first dairy product exclusively fermented by Propionibacterium freudenreichii: A new vector to study probiotic potentialities in vivo. Food Microbiology 2012, 32(1):135-146. http://doi.org/10.1016/j.fm.2012.05.003.
12. Cousin F.J., Mater D.D.G., Foligné B., Jan G. Dairy propionibacteria as human probiotics: A review of recent evidence. Dairy Science & Technology 2010, 91(1):1-26. http://doi.org/10.1051/dst/2010032.
13. De Man J.C., Rogosa M., Sharpe M.E. A medium for the cultivation of lactobacilli. Journal of Applied Bacteriology 1960, 23(1):130-135. http://doi.org/10.1111/j.1365-2672.1960.tb00188.x.
14. Desmond C., Stanton C., Fitzgerald G.F., Collins K., Paul Ross R. Environmental adaptation of probiotic lactobacilli towards improvement of performance during spray drying. International Dairy Journal 2001, 11(10):801-808. http://doi.org/10.1016/S0958-6946(01)00121-2.
15. Elversson J., Millqvist-Fureby A., Alderborn G., Elofsson U. Droplet and particle size relationship and shell thickness of inhalable lactose particles during spray drying. Journal of Pharmaceutical Sciences 2003, 92(4):900-910. http://doi.org/10.1002/jps.10352.
16. Falentin H., Deutsch S.-M., Jan G., Loux V., Thierry A., Parayre S., Maillard M.B., Dherbécourt J., Cousin F.J., Jardin J., Siguier P., Couloux A., Barbe V., Vacherie B., Wincker P., Gibrat J.F., Gaillardin C., Lortal S. The complete genome of propionibacterium freudenreichii CIRM-BIA1T, a hardy actinobacterium with food and probiotic applications. PLoS ONE 2010, 5(7):e11748. http://doi.org/10.1371/journal.pone.0011748.
17. Fang S.-B., Lee H.-C., Hu J.-J., Hou S.-Y., Liu H.-L., Fang H.-W. Dose-dependent effect of Lactobacillus rhamnosus on quantitative reduction of faecal rotavirus shedding in children. Journal of Tropical Pediatrics 2009, 55(5):297-301. http://doi.org/10.1093/tropej/fmp001.
18. FAO/WHO Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria 2001, 1-34.
19. Foligné B., Breton J., Mater D., Jan G. Tracking the microbiome functionality: Focus on Propionibacterium species. Gut 2013, gutjnl-2012-304393. http://doi.org/10.1136/gutjnl-2012-304393.
20. Foligné B., Deutsch S.-M., Breton J., Cousin F.J., Dewulf J., Samson M., Pot B., Jan G. Promising immunomodulatory effects of selected strains of dairy propionibacteria as evidenced in vitro and in vivo. Applied and Environmental Microbiology 2010, 76(24):8259-8264. http://doi.org/10.1128/AEM.01976-10.
21. Fox P.F., McSweeney P.L.H., Cogan T.M., Guinee T.P. Cheese: Chemistry, physics and microbiology: Major cheese groups 2004, Academic Press.
22. Fu N., Chen X.D. Towards a maximal cell survival in convective thermal drying processes. Food Research International 2011, 44(5):1127-1149. http://doi.org/10.1016/j.foodres.2011.03.053.
23. Fu N., Woo M.W., Selomulya C., Chen X.D. Inactivation of Lactococcus lactis ssp. cremoris cells in a droplet during convective drying. Biochemical Engineering Journal 2013, 79:46-56. http://doi.org/10.1016/j.bej.2013.06.015.
24. Fu W.-Y., Etzel M.R. Spray drying of lactococcus lactis ssp. lactis C2 and cellular injury. Journal of Food Science 1995, 60(1):195-200. http://doi.org/10.1111/j.1365-2621.1995.tb05636.x.
25. Gaucher I., Boubellouta T., Beaucher E., Piot M., Gaucheron F., Dufour E. Investigation of the effects of season, milking region, sterilisation process and storage conditions on milk and UHT milk physico-chemical characteristics: A multidimensional statistical approach. Dairy Science and Technology 2008, 88(3):291-312. http://doi.org/10.1051/dst:2007022.
26. Golowczyc M.A., Gerez C.L., Silva J., Abraham A.G., Antoni G.L.D., Teixeira P. Survival of spray-dried Lactobacillus kefir is affected by different protectants and storage conditions. Biotechnology Letters 2010, 33(4):681-686. http://doi.org/10.1007/s10529-010-0491-6.
27. Huang S., Chen X.D. Significant effect of Ca2+ on improving the heat resistance of lactic acid bacteria. FEMS Microbiology Letters 2013, 344(1):31-38. http://doi.org/10.1111/1574-6968.12151.
28. Huang S., Yang Y., Fu N., Qin Q., Zhang L., Chen X.D. Calcium-aggregated milk: A potential new option for improving the viability of lactic acid bacteria under heat stress. Food and Bioprocess Technology 2014, 7(11):3147-3155. http://doi.org/10.1007/s11947-014-1331-9.
29. Hwang C.-F., Chang J.-H., Houng J.-Y., Tsai C.-C., Lin C.-K., Tsen H.-Y. Optimization of medium composition for improving biomass production of Lactobacillus plantarum Pi06 using the Taguchi array design and the Box-Behnken method. Biotechnology and Bioprocess Engineering 2012, 17(4):827-834. http://doi.org/10.1007/s12257-012-0007-4.
30. Jeantet R., Ducept F., Dolivet A., Méjean S., Schuck P. Residence time distribution: A tool to improve spray-drying control. Dairy Science and Technology 2008, 88(1):31-43. http://doi.org/10.1051/dst:2007006.
31. Johansson M.E.V., Jakobsson H.E., Holmén-Larsson J., Schütte A., Ermund A., Rodríguez-Piñeiro A.M., Arike L., Wising C., Svensson F., Bäckhed F., Hansson G.C. Normalization of host intestinal mucus layers requires long-term microbial colonization. Cell Host & Microbe 2015, 18(5):582-592. http://doi.org/10.1016/j.chom.2015.10.007.
32. Kamada N., Seo S.-U., Chen G.Y., Núñez G. Role of the gut microbiota in immunity and inflammatory disease. Nature Reviews. Immunology 2013, 13(5):321-335. http://doi.org/10.1038/nri3430.
33. Kets E.P.W., Teunissen P.J.M., Debont J.A.M. Effect of compatible solutes on survival of lactic acid bacteria subjected to drying. Applied and Environmental Microbiology 1996, 62(1):259-261.
34. Lavari L., Páez R., Cuatrin A., Reinheimer J., Vinderola G. Use of cheese whey for biomass production and spray drying of probiotic lactobacilli. Journal of Dairy Research 2014, 81(03):267-274. http://doi.org/10.1017/S0022029914000156.
35. Lee B., Yin X., Griffey S.M., Marco M.L. Attenuation of colitis by Lactobacillus casei BL23 is dependent on the dairy delivery matrix. Applied and Environmental Microbiology 2015, AEM.01360-15. http://doi.org/10.1128/AEM.01360-15.
36. Lian W.C., Hsiao H.C., Chou C.C. Survival of bifidobacteria after spray-drying. International Journal of Food Microbiology 2002, 74(1-2):79-86. http://doi.org/10.1016/S0168-1605(01)00733-4.
37. Lievense L.C., van't Riet K. Convective drying of bacteria II. Factors influencing survival. Advances in Biochemical Engineering, Biotechnology 1994, 51:71-89.
38. Liu H., Gong J., Chabot D., Miller S.S., Cui S.W., Ma J., Zhong F., Wang Q. Protection of heat-sensitive probiotic bacteria during spray-drying by sodium caseinate stabilized fat particles. Food Hydrocolloids 2015, 51:459-467. http://doi.org/10.1016/j.foodhyd.2015.05.015.
39. Malik A.C., Reinbold G.W., Vedamuthu E.R. An evaluation of the taxonomy of Propionibacterium. Canadian Journal of Microbiology 1968, 14(11):1185-1191.
40. Mattila-Sandholm T., Myllärinen P., Crittenden R., Mogensen G., Fondén R., Saarela M. Technological challenges for future probiotic foods. International Dairy Journal 2002, 12(2-3):173-182. http://doi.org/10.1016/S0958-6946(01)00099-1.
41. Mäyrä-Mäkinen A., Bigret M. Industrial use and production of lactic acid bacteria 1993, 65-95.
42. Paéz R., Lavari L., Vinderola G., Audero G., Cuatrin A., Zaritzky N., Reinheimer J. Effect of heat treatment and spray drying on lactobacilli viability and resistance to simulated gastrointestinal digestion. Food Research International 2012, 48(2):748-754. http://doi.org/10.1016/j.foodres.2012.06.018.
43. Peighambardoust S.H., Golshan Tafti A., Hesari J. Application of spray drying for preservation of lactic acid starter cultures: A review. Trends in Food Science & Technology 2011, 22(5):215-224. http://doi.org/10.1016/j.tifs.2011.01.009.
44. Perdana J., Fox M.B., Siwei C., Boom R.M., Schutyser M.A.I. Interactions between formulation and spray drying conditions related to survival of Lactobacillus plantarum WCFS1. Food Research International 2014, 56:9-17. http://doi.org/10.1016/j.foodres.2013.12.007.
45. Pessione E. Interactive probiotics 2014, CRC Press.
46. Picot A., Lacroix C. Encapsulation of bifidobacteria in whey protein-based microcapsules and survival in simulated gastrointestinal conditions and in yoghurt. International Dairy Journal 2004, 14(6):505-515. http://doi.org/10.1016/j.idairyj.2003.10.008.
47. Rajam R., Karthik P., Parthasarathi S., Joseph G.S., Anandharamakrishnan C. Effect of whey protein - Alginate wall systems on survival of microencapsulated Lactobacillus plantarum in simulated gastrointestinal conditions. Journal of Functional Foods 2012, 4(4):891-898. http://doi.org/10.1016/j.jff.2012.06.006.
48. Rochat T., Bermúdez-Humarán L., Gratadoux J.-J., Fourage C., Hoebler C., Corthier G., Langella P. Anti-inflammatory effects of Lactobacillus casei BL23 producing or not a manganese-dependant catalase on DSS-induced colitis in mice. Microbial Cell Factories 2007, 6(1):1-10. http://doi.org/10.1186/1475-2859-6-22.
49. Rodgers S. Novel applications of live bacteria in food services: Probiotics and protective cultures. Trends in Food Science & Technology 2008, 19(4):188-197. http://doi.org/10.1016/j.tifs.2007.11.007.
50. Ross R.P., Desmond C., Fitzgerald G.F., Stanton C. Overcoming the technological hurdles in the development of probiotic foods. Journal of Applied Microbiology 2005, 98(6):1410-1417.
51. Santivarangkna C., Kulozik U., Foerst P. Alternative drying processes for the industrial preservation of lactic acid starter cultures. Biotechnology Progress 2007, 23(2):302-315.
52. Sawatari Y., Hirano T., Yokota A. Development of food grade media for the preparation of Lactobacillus plantarum starter culture. The Journal of General and Applied Microbiology 2006, 52(6):349-356.
53. Schuck P., Dolivet A., Jeantet R. Analytical methods for food and dairy powders: Schuck/analytical methods for food and dairy powders 2012, Wiley-Blackwell., Oxford, UK, Retrieved from. http://doi.wiley.com/10.1002/9781118307397.
54. Schuck P., Dolivet A., Méjean S., Hervé C., Jeantet R. Spray drying of dairy bacteria: New opportunities to improve the viability of bacteria powders. International Dairy Journal 2013, 31(1):12-17. http://doi.org/10.1016/j.idairyj.2012.01.006.
55. Schuck P., Dolivet A., Méjean S., Zhu P., Blanchard E., Jeantet R. Drying by desorption: A tool to determine spray drying parameters. Journal of Food Engineering 2009, 94(2):199-204. http://doi.org/10.1016/j.jfoodeng.2008.08.014.
56. Selmer-Olsen E., Birkeland S.E., Sorhaug T. Effect of protective solutes on leakage from and survival of immobilized Lactobacillus subjected to drying, storage and rehydration. Journal of Applied Microbiology 1999, 87(3):429-437.
57. Semyonov D., Ramon O., Kaplun Z., Levin-Brener L., Gurevich N., Shimoni E. Microencapsulation of Lactobacillus paracasei by spray freeze drying. Food Research International 2009, In Press, Corrected Proof. http://doi.org/10.1016/j.foodres.2009.09.028.
58. Stoklosa A.M., Lipasek R.A., Taylor L.S., Mauer L.J. Effects of storage conditions, formulation, and particle size on moisture sorption and flowability of powders: A study of deliquescent ingredient blends. Food Research International 2012, 49(2):783-791. http://doi.org/10.1016/j.foodres.2012.09.034.
59. Sunny-Roberts E.O., Knorr D. The protective effect of monosodium glutamate on survival of Lactobacillus rhamnosus GG and Lactobacillus rhamnosus E-97800 (E800) strains during spray-drying and storage in trehalose-containing powders. International Dairy Journal 2009, 19(4):209-214. http://doi.org/10.1016/j.idairyj.2008.10.008.
60. Teixeira P.C., Castro M.H., Malcata F.X., Kirby R.M. Survival of Lactobacillus delbrueckii ssp. bulgaricus following spray-drying. Journal of Dairy Science 1995, 78(5):1025-1031. http://doi.org/10.3168/jds.S0022-0302(95)76718-2.
61. Thierry A., Deutsch S.-M., Falentin H., Dalmasso M., Cousin F.J., Jan G. New insights into physiology and metabolism of Propionibacterium freudenreichii. International Journal of Food Microbiology 2011, 149(1):19-27. http://doi.org/10.1016/j.ijfoodmicro.2011.04.026.
62. Tripathi M.K., Giri S.K. Probiotic functional foods: Survival of probiotics during processing and storage. Journal of Functional Foods 2014, 9:225-241. http://doi.org/10.1016/j.jff.2014.04.030.
63. Van De Guchte M., Serror P., Chervaux C., Smokvina T., Ehrlich S.D., Maguin E. Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek 2002, 82(1-4):187-216. http://doi.org/10.1023/A:1020631532202.
64. Vasseur C., Baverel L., Hébraud M., Labadie J. Effect of osmotic, alkaline, acid or thermal stresses on the growth and inhibition of Listeria monocytogenes. Journal of Applied Microbiology 1999, 86(3):469-476. http://doi.org/10.1046/j.1365-2672.1999.00686.x.
65. Walter R.P., Morris J.G., Kell D.B. The roles of osmotic stress and water activity in the inhibition of the growth, glycolysis and glucose phosphotransferase system of Clostridium pasteurianum. Microbiology (Reading, England) 1987, 133(2):259-266. http://doi.org/10.1099/00221287-133-2-259.
66. Watterlot L., Rochat T., Sokol H., Cherbuy C., Bouloufa I., Lefèvre F., Gratadoux J.J., Honvo-Hueto E., Chilmonczyk S., Blugeon S., Corthier G., Langella P., Bermúdez-Humarán L.G. Intragastric administration of a superoxide dismutase-producing recombinant Lactobacillus casei BL23 strain attenuates DSS colitis in mice. International Journal of Food Microbiology 2010, 144(1):35-41. http://doi.org/10.1016/j.ijfoodmicro.2010.03.037.
67. Wood J.M. Bacterial osmoregulation: A paradigm for the study of cellular homeostasis. Annual Review of Microbiology 2011, 65(1):215-238. http://doi.org/10.1146/annurev-micro-090110-102815.
68. Wu W.D., Liu W., Gengenbach T., Woo M.W., Selomulya C., Chen X.D., Weeks M. Towards spray drying of high solids dairy liquid: Effects of feed solid content on particle structure and functionality. Journal of Food Engineering 2014, 123:130-135. http://doi.org/10.1016/j.jfoodeng.2013.05.013.
69. Yonekura L., Sun H., Soukoulis C., Fisk I. Microencapsulation of Lactobacillus acidophilus NCIMB 701748 in matrices containing soluble fibre by spray drying: Technological characterization, storage stability and survival after in vitro digestion. Journal of Functional Foods 2014, 6:205-214. http://doi.org/10.1016/j.jff.2013.10.008.