Microencapsulation of probiotics for gastrointestinal delivery

Journal of Controlled Release

Volumn 162, Issue 1, 2012, Pages 56-67

  Cook, Michael T ^a   Tzortzis, George ^a   Charalampopoulos, Dimitris ^a   Khutoryanskiy, Vitaliy V ^a  

^a UNIVERSITY OF READING   (United Kingdom)

Author keywords

Alginate; Bifidobacterium; Controlled release; Encapsulation; Enteric; Lactobacillus

Indexed keywords

BIFIDOBACTERIUM; BILE SALTS; CONTROL RELEASE; CONTROLLED RELEASE; CONTROLLED RELEASE DEVICES; EMERGING TRENDS; ENTERIC; GLOBAL MARKET; INTESTINAL TRACT; LACTOBACILLUS; MICROCAPSULES; NUTRACEUTICALS; ORAL ADMINISTRATION; PROBIOTIC BACTERIA; PROBIOTICS; SMALL MOLECULES;

ALGINATE; BACTERIA; CELL DEATH; INTERNATIONAL TRADE; UNLOADING;

ENCAPSULATION;

ALGINIC ACID; CHITOSAN; MILK PROTEIN; PALM OIL; POLYLYSINE; POLYMER; PROBIOTIC AGENT; XANTHAN;

BIFIDOBACTERIUM BIFIDUM; BIFIDOBACTERIUM BREVE; CONTROLLED DRUG RELEASE; DIFFUSION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG MARKETING; GASTROINTESTINAL TRACT; HUMAN; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS CASEI; LACTOBACILLUS PLANTARUM; MICROENCAPSULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ALGINATES; ANIMALS; CAPSULES; DELAYED-ACTION PREPARATIONS; DIETARY SUPPLEMENTS; DRUG COMPOUNDING; GASTROINTESTINAL TRACT; HUMANS; PROBIOTICS;

EID: 84864655629     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2012.06.003     Document Type: Review

References (125)

1. R. Fuller Probiotics in man and animals J Appl Bacteriol 66 1989 365 378
2. S. Salminen, C. Bouley, M.C. Boutron-Ruault, J.H. Cummings, A. Franck, G.R. Gibson, E. Isolauri, M.C. Moreau, M. Roberfroid, and I. Rowland Functional food science and gastrointestinal physiology and function Br. J. Nutr. 80 1998 S147 S171
3. L.V. Holdeman, I.J. Good, and W.E.C. Moore Human fecal flora - variation in bacterial composition within individuals and a possible effect of emotional stress Appl. Env. Microbiol. 31 1976 359 375
4. G.R. Gibson, and M.B. Roberfroid Dietary Modulation of the human colonic microbiota - introducing the concept of prebiotics J. Nutr. 125 1995 1401 1412
5. M.H. Saier, and N.M. Mansour Probiotics and prebiotics in human health J. Mol. Microbiol. Biotechnol. 10 2005 22 25
6. T. Mach Clinical usefulness of probiotics in inflammatory bowel diseases J. Physiol. Pharmacol. 57 Suppl. 9 2006 23 33
7. L. O'Mahony, J. McCarthy, P. Kelly, G. Hurley, F.Y. Luo, K.S. Chen, G.C. O'Sullivan, B. Kiely, J.K. Collins, F. Shanahan, and E.M.M. Quigley Lactobacillus and Bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles Gastroenterology 128 2005 541 551
8. P.R. Marteau, M. de Vrese, C.J. Cellier, and J. Schrezenmeir Protection from gastrointestinal diseases with the use of probiotics Am. J. Clin. Nutr. 73 2001 430S 436S
9. B.J. Rembacken, A.M. Snelling, P.M. Hawkey, D.M. Chalmers, and A.T.R. Axon Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial Lancet 354 1999 635 639
10. T. Mimura, F. Rizzello, U. Helwig, G. Poggioli, S. Schreiber, I.C. Talbot, R.J. Nicholls, P. Gionchetti, M. Campieri, and M.A. Kamm Once daily high dose probiotic therapy (VSL#3) for maintaining remission in recurrent or refractory pouchitis Gut 53 2004 108 114
11. K. Kukkonen, E. Savilahti, T. Haahtela, K. Juntunen-Backman, R. Korpela, T. Poussa, T. Tuure, and M. Kuitunen Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial J. Allergy Clin. Immunol. 119 2007 192 198
12. M. Kalliomäki, S. Salminen, H. Arvilommi, P. Kero, P. Koskinen, and E. Isolauri Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial Lancet 357 2001 1076 1079
13. R. Fuller Probiotics in human medicine Gut 32 1991 439 442
14. C.A. Adams The probiotic paradox: live and dead cells are biological response modifiers Nutr. Res. Rev. 23 2010 37 46
15. W.P. Charteris, P.M. Kelly, L. Morelli, and J.K. Collins Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract J. Appl. Microbiol. 84 1998 759 768
16. S. Mandal, A.K. Puniya, and K. Singh Effect of alginate concentrations on survival of microencapsulated Lactobacillus casei NCDC-298 Int. Dairy J. 16 2006 1190 1195
17. T. Heidebach, P. Forst, and U. Kulozik Microencapsulation of probiotic cells for food applications Crit. Rev. Food Sci. Nutr. 52 2012 291 311
18. F. Nazzaro, P. Orlando, F. Fratianni, and R. Coppola Microencapsulation in food science and biotechnology Curr. Opin. Biotechnol. 23 2012 182 186
19. C.P. Champagne, and P. Fustier Microencapsulation for the improved delivery of bioactive compounds into foods Curr. Opin. Biotechnol. 18 2007 184 190
20. S.S. Kuang, J.C. Oliveira, and A.M. Crean Microencapsulation as a tool for incorporating bioactive ingredients into food Crit. Rev. Food Sci. Nutr. 50 2010 951 968
21. W.R. Gombotz, and S.F. Wee Protein release from alginate matrices Adv. Drug Deliv. Rev. 31 1998 267 285
22. M.E. Aulton Aulton's Pharmaceutics Third ed. 2007 Elsevier Amsterdam
23. D.F. Evans, G. Pye, R. Bramley, A.G. Clark, T.J. Dyson, and J.D. Hardcastle Measurement of gastrointestinal pH profiles in normal ambulant human-subjects Gut 29 1988 1035 1041
24. J.S. Fordtran, and J.H. Walsh Gastric-acid secretion rate and buffer content of stomach after eating - results in normal subjects and in patients with duodenal-ulcer J. Clin. Invest. 52 1973 645 657
25. E.L. McConnell, H.M. Fadda, and A.W. Basit Gut instincts: explorations in intestinal physiology and drug delivery Int. J. Pharm. 364 2008 213 226
26. S. Hellmig, F. Von Schoning, C. Gadow, S. Katsoulis, J. Hedderich, U.R. Folsch, and E. Stuber Gastric emptying time of fluids and solids in healthy subjects determined by C-13 breath tests: influence of age, sex and body mass index J. Gastroenterol. Hepatol. 21 2006 1832 1838
27. J. Janssens, G. Vantrappen, and T.L. Peeters The activity front of the migrating motor complex of the human stomach but not of the small intestine is motilin-dependent Regul. Peptides 6 1983 363 369
28. S.S. Davis, J.G. Hardy, and J.W. Fara Transit of pharmaceutical dosage forms through the small-intestine Gut 27 1986 886 892
29. A. Coupe, S. Davis, and I. Wilding Variation in gastrointestinal transit of pharmaceutical dosage forms in healthy subjects Pharm. Res. 8 1991 360 364
30. Press, Hauptmann, Hauptmann, Fuchs, Fuchs, Ewe, and Ramadori Gastrointestinal pH profiles in patients with inflammatory bowel disease Aliment. Pharmacol. Ther. 12 1998 673 678
31. G. Sathyan, S. Hwang, and S.K. Gupta Effect of dosing time on the total intestinal transit time of non-disintegrating systems Int. J. Pharm. 204 2000 47 51
32. M.K. Chourasia, and S.K. Jain Pharmaceutical approaches to colon targeted drug delivery systems J. Pharm. Pharm. Sci. 6 2003 33 66
33. V.R. Sinha, and R. Kumria Microbially triggered drug delivery to the colon Eur. J. Pharm. Sci. 18 2003 3 18
34. E.L. McConnell, M.D. Short, and A.W. Basit An in vivo comparison of intestinal pH and bacteria as physiological trigger mechanisms for colonic targeting in man J. Control. Release 130 2008 154 160
35. I.A. Sogias, A.C. Williams, and V.V. Khutoryanskiy Why is chitosan mucoadhesive? Biomacromolecules 9 2008 1837 1842
36. V.V. Khutoryanskiy Advances in mucoadhesion and mucoadhesive polymers Macromol. Biosci. 11 2011 748 764
37. W.K. Ding, and N.P. Shah An improved method of microencapsulation of probiotic bacteria for their stability in acidic and bile conditions during storage J. Food Sci. 74 2009 M53 M61
38. W.R. Sun, and M.W. Griffiths Survival of bifidobacteria in yogurt and simulated gastric juice following immobilization in gellan-xanthan beads Int. J. Food Microbiol. 61 2000 17 25
39. V. Chandramouli, K. Kailasapathy, P. Peiris, and M. Jones An improved method of microencapsulation and its evaluation to protect Lactobacillus spp. in simulated gastric conditions J. Microbiol. Methods 56 2004 27 35
40. J.H. Cui, J.S. Goh, P.H. Kim, S.H. Choi, and B.J. Lee Survival and stability of bifidobacteria loaded in alginate poly-l-lysine microparticles Int. J. Pharm. 210 2000 51 59
41. Y. Senuma, C. Lowe, Y. Zweifel, J.G. Hilborn, and I. Marison Alginate hydrogel microspheres and microcapsules prepared by spinning disk atomization Biotechnol. Bioeng. 67 2000 616 622
42. J.S. Ryu, Y.J. Lee, S.I. Choi, J.W. Lee, and T.R. Heo Optimization of screw pumping system (SPS) for mass production of entrapped bifidus Food Sci. Biotechnol. 14 2005 566 571
43. R.R. Mokarram, S.A. Mortazavi, M.B.H. Najafi, and F. Shahidi The influence of multi stage alginate coating on survivability of potential probiotic bacteria in simulated gastric and intestinal juice Food Res. Int. 42 2009 1040 1045
44. T. Heidebach, P. Forst, and U. Kulozik Microencapsulation of probiotic cells by means of rennet-gelation of milk proteins Food Hydrocolloids 23 2009 1670 1677
45. A.C. Oliveira, T.S. Moretti, C. Boschini, J.C.C. Baliero, O. Freitas, and C.S. Favaro-Trindade Stability of microencapsulated B. lactis (BI 01) and L. acidophilus (LAC 4) by complex coacervation followed by spray drying J. Microencapsul. 24 2007 673 681
46. A.C. Oliveira, T.S. Moretti, C. Boschini, J.C.C. Baliero, O. Freitas, L.A.P. Freitas, and C.S. Favaro-Trindade Microencapsulation of B. lactis (BI 01) and L. acidophilus (LAC 4) by complex coacervation followed by spouted-bed drying Dry. Technol. 25 2007 1687 1693
47. K. Jono, H. Ichikawa, M. Miyamoto, and Y. Fukumori A review of particulate design for pharmaceutical powders and their production by spouted bed coating Powder Technol. 113 2000 269 277
48. A. Gharsallaoui, G. Roudaut, O. Chambin, A. Voilley, and R. Saurel Applications of spray-drying in microencapsulation of food ingredients: an overview Food Res. Int. 40 2007 1107 1121
49. S. Graff, S. Hussain, J.C. Chaumeil, and C. Charrueaul Increased intestinal delivery of viable Saccharomyces boulardii by encapsulation in microspheres Pharm. Res. 25 2008 1290 1296
50. M. Saarela, I. Virkajarvi, H.L. Alakomi, T. Mattila-Sandholm, A. Vaari, T. Suomalainen, and J. Matto Influence of fermentation time, cryoprotectant and neutralization of cell concentrate on freeze-drying survival, storage stability, and acid and bile exposure of Bifidobacterium animalis ssp lactis cells produced without milk-based ingredients J. Appl. Microbiol. 99 2005 1330 1339
51. A. Siaterlis, G. Deepika, and D. Charalampopoulos Effect of culture medium and cryoprotectants on the growth and survival of probiotic lactobacilli during freeze drying Lett. Appl. Microbiol. 48 2009 295 301
52. A. Faure, P. York, and R.C. Rowe Process control and scale-up of pharmaceutical wet granulation processes: a review Eur. J. Pharm. Biopharm. 52 2001 269 277
53. M.T. Cook, G. Tzortzis, D. Charalampopoulos, and V.V. Khutoryanskiy Production and evaluation of dry alginate-chitosan microcapsules as an enteric delivery vehicle for probiotic bacteria Biomacromolecules 12 2011 2834 2840
54. M. Rinaudo Main properties and current applications of some polysaccharides as biomaterials Polym. Int. 57 2008 397 430
55. B. Thu, P. Bruheim, T. Espevik, O. Smidsrod, P. SoonShiong, and G. SkjakBraek Alginate polycation microcapsules.1. Interaction between alginate and polycation Biomaterials 17 1996 1031 1040
56. S.M.A. Wahab, M.A. Ahmed, F.A. Radwan, R.M. Hassan, and A.M. ElRefae Relative permittivity and electrical conductivity of some divalent metal alginate complexes Mater. Lett. 30 1997 183 188
57. B.T. Stokke, K.I. Draget, O. Smidsrod, Y. Yuguchi, H. Urakawa, and K. Kajiwara Small-angle X-ray scattering and rheological characterization of alginate gels. 1. Ca-alginate gels Macromolecules 33 2000 1853 1863
58. O. Sandoval-Castilla, C. Lobato-Calleros, H.S. García-Galindo, J. Alvarez-Ramírez, and E.J. Vernon-Carter Textural properties of alginate-pectin beads and survivability of entrapped Lb. casei in simulated gastrointestinal conditions and in yoghurt Food Res. Int. 43 2010 111 117
59. T.Y. Sheu, and R.T. Marshall Microentrapment of Lactobacilli in calcium alginate gels J. Food Sci. 58 1993 557 561
60. D. Poncelet, R. Lencki, C. Beaulieu, J.P. Halle, R.J. Neufeld, and A. Fournier Production of alginate beads by emulsification internal gelation Methodology Appl. Microbiol. Biotechnol. 38 1992 39 45
61. O. Smidsrod, and G. Skjakbraek Alginate as immobilization matrix for cells Trends Biotechnol. 8 1990 71 78
62. A. Martinsen, G. Skjakbraek, and O. Smidsrod Alginate as immobilization material. 1. Correlation between chemical and physical-properties of alginate gel beads Biotechnol. Bioeng. 33 1989 79 89
63. G. Skjakbraek, H. Grasdalen, and O. Smidsrod Inhomogeneous polysaccharide ionic gels Carbohydr. Polym. 10 1989 31 54
64. I.T. Tai, and A.M. Sun Microencapsulation of recombinant cells - a new delivery system for gene-therapy FASEB J. 7 1993 1061 1069
65. M. Weber, A. Steinert, A. Jork, A. Dimmler, F. Thurmer, N. Schutze, C. Hendrich, and U. Zimmermann Formation of cartilage matrix proteins by BMP-transfected murine mesenchymal stem cells encapsulated in a novel class of alginates Biomaterials 23 2002 2003 2013
66. B. Wright, R.A. Cave, J.P. Cook, V.V. Khutoryanskiy, S. Mi, B. Chen, M. Leyland, and C.J. Connon Enhanced viability of corneal epithelial cells for efficient transport/storage using a structurally modified calcium alginate hydrogel Regen. Med. 7 2012 295 307
67. K.I. Draget, G.S. Braek, and O. Smidsrod Alginic acid gels - the effect of alginate chemical-composition and molecular-weight Carbohydr. Polym. 25 1994 31 38
68. B. Albertini, B. Vitali, N. Passerini, F. Cruciani, M. Di Sabatino, L. Rodriguez, and P. Brigidi Development of microparticulate systems for intestinal delivery of Lactobacillus acidophilus and Bifidobacterium lactis Eur. J. Pharm. Sci. 40 2010 359 366
69. L. Sabikhi, R. Babu, D.K. Thompkinson, and S. Kapila Resistance of microencapsulated Lactobacillus acidophilus LA1 to processing treatments and simulated gut conditions Food Bioprocess Technol. 3 2010 586 593
70. L.T. Hansen, P.M. Allan-Wojtas, Y.L. Jin, and A.T. Paulson Survival of Ca-alginate microencapsulated Bifidobacterium spp. in milk and simulated gastrointestinal conditions Food Microbiol. 19 2002 35 45
71. K. Sultana, G. Godward, N. Reynolds, R. Arumugaswamy, P. Peiris, and K. Kailasapathy Encapsulation of probiotic bacteria with alginate-starch and evaluation of survival in simulated gastrointestinal conditions and in yoghurt Int. J. Food Microbiol. 62 2000 47 55
72. W.K. Ding, and N.P. Shah Effect of various encapsulating materials on the stability of probiotic bacteria J. Food Sci. 74 2009 M100 M107
73. M. Papagianni, and S. Anastasiadou Encapsulation of Pediococcus acidilactici cells in corn and olive oil microcapsules emulsified by peptides and stabilized with xanthan in oil-in-water emulsions: studies on cell viability under gastro-intestinal simulating conditions Enzym. Microb. Technol. 45 2009 514 522
74. P. Muthukumarasamy, P. Allan-Wojtas, and R.A. Holley Stability of Lactobacillus reuteri in different types of microcapsules J. Food Sci. 71 2006 M20 M24
75. X.Y. Li, X.G. Chen, D.S. Cha, H.J. Park, and C.S. Liu Microencapsulation of a probiotic bacteria with alginate-gelatin and its properties J. Microencapsul. 26 2009 315 324
76. S.-J. Kim, S.Y. Cho, S.H. Kim, O.-J. Song, I.I.S. Shin, D.S. Cha, and H.J. Park Effect of microencapsulation on viability and other characteristics in Lactobacillus acidophilus ATCC 43121 LWT - Food Sci. Technol. 41 2008 493 500
77. W. Krasaekoopt, B. Bhandari, and H. Deeth The influence of coating materials on some properties of alginate beads and survivability of microencapsulated probiotic bacteria Int. Dairy J. 14 2004 737 743
78. G.K. Gbassi, T. Vandamme, S. Ennahar, and E. Marchioni Microencapsulation of Lactobacillus plantarum spp in an alginate matrix coated with whey proteins Int. J. Food Microbiol. 129 2009 103 105
79. A.M. Liserre, M.I. Re, and B. Franco Microencapsulation of Bifidobacterium animalis subsp lactis in modified alginate-chitosan beads and evaluation of survival in simulated gastrointestinal conditions Food Biotechnol. 21 2007 1 16
80. M. Kumar A review of chitin and chitosan applications React. Funct. Polym. 46 2000 1 27
81. M.F.A. Goosen Applications of Chitin and Chitosan 2006 CRC Press 336
82. I.A. Sogias, V.V. Khutoryanskiy, and A.C. Williams Exploring the factors affecting the solubility of chitosan in water Macromol. Chem. Phys. 211 2010 426 433
83. K.V.H. Prashanth, and R.N. Tharanathan Chitin/chitosan: modifications and their unlimited application potential - an overview Trends Food Sci. Technol. 18 2007 117 131
84. A.C.M. Wu, W.A. Bough, E.C. Conrad, and K.E. Alden Determination of molecular-weight distribution of chitosan by high-performance liquid-chromatography J. Chromatogr. 128 1976 87 99
85. M. Rinaudo Chitin and chitosan: properties and applications Prog. Polym. Sci. 31 2006 603 632
86. J.Z. Lin, W.T. Yu, X.D. Liu, H.G. Xie, W. Wang, and X.J. Ma In vitro and in vivo characterization of alginate-chitosan-alginate artificial microcapsules for therapeutic oral delivery of live bacterial cells J. Biosci. Bioeng. 105 2008 660 665
87. E.-S. Chan, S.-L. Wong, P.-P. Lee, J.-S. Lee, T.B. Ti, Z. Zhang, D. Poncelet, P. Ravindra, S.-H. Phan, and Z.-H. Yim Effects of starch filler on the physical properties of lyophilized calcium-alginate beads and the viability of encapsulated cells Carbohydr. Polym. 83 2011 225 232
88. F. Garcia-Ochoa, V.E. Santos, J.A. Casas, and E. Gomez Xanthan gum: production, recovery, and properties Biotechnol. Adv. 18 2000 549 579
89. L.D. McMaster, S.A. Kokott, S.J. Reid, and V. Abratt Use of traditional African fermented beverages as delivery vehicles for Bifidobacterium lactis DSM 10140 Int. J. Food Microbiol. 102 2005 231 237
90. L.D. McMaster, S.A. Kokott, and P. Slatter Micro-encapsulation of Bifidobacterium lactis for incorporation into soft foods World J. Microbiol. Biotechnol. 21 2005 723 728
91. C. Desmond, R.P. Ross, E. O'Callaghan, G. Fitzgerald, and C. Stanton Improved survival of Lactobacillus paracasei NFBC 338 in spray-dried powders containing gum acacia J. Appl. Microbiol. 93 2002 1003 1011
92. Y. Dror, Y. Cohen, and R. Yerushalmi-Rozen Structure of gum arabic in aqueous solution J. Polym. Sci. Part B: Polym. Phys. 44 2006 3265 3271
93. W.-C. Lian, H.-C. Hsiao, and C.-C. Chou Viability of microencapsulated bifidobacteria in simulated gastric juice and bile solution Int. J. Food Microbiol. 86 2003 293 301
94. A.D. Borza, N.T. Annan, D.L. Moreau, P.M. Allan-Wojtas, A. Ghanem, D. Rousseau, A.T. Paulson, and L.T. Hansen Microencapsulation in genipin cross-linked gelatine-maltodextrin improves survival of Bifidobacterium adolescentis during exposure to in vitro gastrointestinal conditions J. Microencapsul. 27 2010 387 399
95. F.L. Mi, Y.C. Tan, H.F. Liang, and H.W. Sung In vivo biocompatibility and degradability of a novel injectable-chitosan-based implant Biomaterials 23 2002 181 191
96. T. Heidebach, P. Forst, and U. Kulozik Transglutaminase-induced caseinate gelation for the microencapsulation of probiotic cells Int. Dairy J. 19 2009 77 84
97. A. Picot, and C. Lacroix Encapsulation of bifidobacteria in whey protein-based microcapsules and survival in simulated gastrointestinal conditions and in yoghurt Int. Dairy J. 14 2004 505 515
98. D. Ying, J. Sun, L. Sanguansri, R. Weerakkody, and M.A. Augustin Enhanced survival of spray-dried microencapsulated Lactobacillus rhamnosus GG in the presence of glucose J. Food Eng. 109 2011 597 602
99. S.B. Doherty, M.A. Auty, C. Stanton, R.P. Ross, G.F. Fitzgerald, and A. Brodkorb Survival of entrapped Lactobacillus rhamnosus GG in whey protein micro-beads during simulated ex vivo gastro-intestinal transit Int. Dairy J. 22 2012 31 43
100. A. López-Rubio, E. Sanchez, S. Wilkanowicz, Y. Sanz, and J.M. Lagaron Electrospinning as a useful technique for the encapsulation of living bifidobacteria in food hydrocolloids Food Hydrocolloids 28 2011 159 167
101. C.L. Gerez, G. Font de Valdez, M.L. Gigante, and C.R.F. Grosso Whey protein coating bead improves the survival of the probiotic Lactobacillus rhamnosus CRL 1505 to low pH Lett. Appl. Microbiol. 54 2012 552 556
102. M. George, and T.E. Abraham Polyionic hydrocolloids for the intestinal delivery of protein drugs: alginate and chitosan - a review J. Control. Release 114 2006 1 14
103. R. Bibiloni, R.N. Fedorak, G.W. Tannock, K.L. Madsen, P. Gionchetti, M. Campieri, C. De Simone, and R.B. Sartor VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis Am. J. Gastroenterol. 100 2005 1539 1546
104. Y. Zhou, E. Martins, A. Groboillot, C.P. Champagne, and P.C. Neufeld Spectrophotometric quantification of lactic bacteria in alginate and control of cell release with chitosan coating J. Appl. Microbiol. 84 1998 342 348
105. J.F. Brandts The thermodynamics of protein denaturation. I. The denaturation of chymotrypsinogen J. Am. Chem. Soc. 86 1964 4291 4301
106. E. Lindh Increased resistance of immunoglobulin a dimers to proteolytic degradation after binding of secretory component J. Immunol. 114 1975 284 286
107. S.B. Doherty, V.L. Gee, R.P. Ross, C. Stanton, G.F. Fitzgerald, and A. Brodkorb Development and characterisation of whey protein micro-beads as potential matrices for probiotic protection Food Hydrocolloids 25 2011 1604 1617
108. S.A. Hamad, S.D. Stoyanov, and V.N. Paunov Triggered cell release from shellac-cell composite microcapsules Soft Matter 8 2012 5069 5077
109. W. Sun, and M.W. Griffiths Survival of bifidobacteria in yogurt and simulated gastric juice following immobilization in gellanâxanthan beads Int. J. Food Microbiol. 61 2000 17 25
110. K.-Y. Lee, and T.-R. Heo Survival of Bifidobacterium longum immobilized in calcium alginate beads in simulated gastric juices and bile salt solution Appl. Environ. Microbiol. 66 2000 869 873
111. C.I. And, and K. Kailasapathy Effect of co-encapsulation of probiotics with prebiotics on increasing the viability of encapsulated bacteria under in vitro acidic and bile salt conditions and in yogurt J. Food Sci. 70 2005 M18 M23
112. P. Marteau, M. Minekus, R. Havenaar, and J.H. Huis in't Veld Survival of lactic acid bacteria in a dynamic model of the stomach and small intestine: validation and the effects of bile J. Dairy Sci. 80 1997 1031 1037
113. P. Marteau, P. Pochart, Y. Bouhnik, S. Zidi, I. Goderel, and J.C. Rambaud Survival of Lactobacillus-acidophilus and Bifidobacterium sp ingested in a fermented milk in the small-intestine - a rational basis for the use of probiotics in man Gastroenterol. Clin. Biol. 16 1992 25 28
114. K. Molly, I. DeSmet, L. Nollet, M. VandeWoestyne, and W. Verstraete Effect of lactobacilli on the ecology of the gastro-intestinal microbiota cultured in the SHIME reactor Microb. Ecol. Heal. Dis. 9 1996 79 89
115. K. Molly, M. Vandewoestyne, I. Desmet, and W. Verstraete Validation of the simulator of the human intestinal microbial ecosystem (SHIME) reactor using microorganism-associated activities Microb. Ecol. Heal. Dis. 7 1994 191 200
116. P. De Boever, B. Deplancke, and W. Verstraete Fermentation by gut microbiota cultured in a simulator of the human intestinal microbial ecosystem Is improved by supplementing a soygerm powder J. Nutr. 130 2000 2599 2606
117. T.T. Kararli Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals Biopharm. Drug Dispos. 16 1995 351 380
118. A.L. McCartney Application of molecular biological methods for studying probiotics and the gut flora Br. J. Nutr. 88 Suppl. 1 2002 S29 S37
119. L. Mare, G.M. Wolfaardt, and L.M. Dicks Adhesion of Lactobacillus plantarum 423 and Lactobacillus salivarius 241 to the intestinal tract of piglets, as recorded with fluorescent in situ hybridization (FISH), and production of plantaricin 423 by cells colonized to the ileum J. Appl. Microbiol. 100 2006 838 845
120. L. Masco, T. Vanhoutte, R. Temmerman, J. Swings, and G. Huys Evaluation of real-time PCR targeting the 16S rRNA and recA genes for the enumeration of bifidobacteria in probiotic products Int. J. Food Microbiol. 113 2007 351 357
121. R. Kushal, S.K. Anand, and H. Chander In vivo demonstration of enhanced probiotic effect of co-immobilized Lactobacillus acidophilus and Bifidobacterium bifidum Int. J. Dairy Technol. 59 2006 265 271
122. A. Lan, A. Bruneau, C. Philippe, V. Rochet, A. Rouault, C. Herve, N. Roland, S. Rabot, and G. Jan Survival and metabolic activity of selected strains of Propionibacterium freudenreichii in the gastrointestinal tract of human microbiota-associated rats Br. J. Nutr. 97 2007 714 724
123. G. Tzortzis, A.K. Goulas, J.M. Gee, and G.R. Gibson A novel galactooligosaccharide mixture increases the bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo J. Nutr. 135 2005 1726 1731
124. L.R. Fitzpatrick, J. Small, R.A. Hoerr, E.F. Bostwick, L. Maines, and W.A. Koltun In vitro and in vivo effects of the probiotic Escherichia coli strain M-17: immunomodulation and attenuation of murine colitis Br. J. Nutr. 100 2008 530 541
125. J.L. Zani, F.W. da Cruz, A.F. dos Santos, and C. Gil-Turnes Effect of probiotic CenBiot on the control of diarrhoea and feed efficiency in pigs J. Appl. Microbiol. 84 1998 68 71