Probiotic bacteria in infant formula and follow-up formula: Microencapsulation using milk and pea proteins to improve microbiological quality

Food Research International

Volumn 64, Issue , 2014, Pages 567-576

  Kent, Robert M ^a   Doherty, Sinéad B ^a  

^a R and D Centre of Excellence and Production   (Ireland)

Author keywords

Follow up formula; Infant formula; Microencapsulation; Probiotic; Protein

Indexed keywords

CELLS; FOOD PROCESSING; MICROENCAPSULATION; PROTEINS;

FOLLOW-UP FORMULA; GASTROINTESTINAL TRACT; INFANT FORMULA; MICROBIOLOGICAL QUALITY; MICROENCAPSULATION TECHNOLOGY; POWDERED INFANT FORMULAE; PROBIOTICS; PROCESSING TECHNIQUE; PEA PROTEINS; PROBIOTIC BACTERIA;

CYTOLOGY; MICROENCAPSULATION;

EID: 84907347840     PISSN: 09639969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodres.2014.07.029     Document Type: Review

References (101)

1. Adams C.A. The probiotic paradox: Live and dead cells are biological response modifiers. Nutrition Research Reviews 2010, 23(1):37-46.
2. Altermann E., Russell W.M., Azcarate-Peril M.A., Barrangou R., Buck B.L., McAuliffe O., et al. Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(11):3906-3912.
3. 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.
4. Axelsson L., Chung T., Dobrogosz W., Lindgren S. Production of a broad spectrum antimicrobial substance by Lactobacillus reuteri. Microbial Ecology in Health and Disease 1989, 2(2):131-136.
5. +-induced gelation of pre-heated whey protein isolate. Journal of Food Science 1993, 58(4):867-871.
6. Björkstén B., Naaber P., Sepp E., Mikelsaar M. The intestinal microflora in allergic Estonian and Swedish 2-year-old children. Clinical and Experimental Allergy 1999, 29:342-346.
7. Boehm G., Stahl B., Jelinek J., Knol J., Miniello V., Moro G.E. Prebiotic carbohydrates in human milk and formulas. Acta Paediatrica 2005, 94(s449):18-21.
8. Braegger C., Chmielewska A., Decsi T., Kolacek S., Mihatsch W., Moreno L., et al. ESPGHAN Committee on Nutrition. Supplementation of infant formula with probiotics and/or prebiotics: A systematic review and comment by the ESPGHAN committee on nutrition. Journal of Pediatric Gastroenterology and Nutrition 2011, 52(2):238-251.
9. Burgain J., Gaiani C., Cailliez-Grimal C., Jeandel C., Scher J. Encapsulation of Lactobacillus rhamnosus GG in microparticles: Influence of casein to whey proteins ratio on bacterial survival during digestion. Innovative Food Science & Emerging Technologies 2013, 19:233-242.
10. Burgain J., Gaiani C., Linder M., Scher J. Encapsulation of probiotic living cells: From laboratory scale to industrial applications. Journal of Food Engineering 2011, 104(4):467-483.
11. CAC Codex standard for infant formula (revision 2007, amended 2011) 1976, 72-1981. Codex Stan.
12. CAC Codex standard follow-up formula CODEX STAN 156-1987 (amended 1989, 2011): Joint FAO/WHO Food Standards Programme, Codex Alimentarius Commission 1987.
13. CAC Proposal to review the Codex standard for follow-up formula 2011.
14. CDRF Products with probiotics 2011.
15. Champagne C.P., Lacroix C., Sodini-Gallot I. Immobilized cell technologies for the dairy industry. Critical Reviews in Biotechnology 1994, 14(2):109-134.
16. Charteris W., Kelly P., Morelli L., Collins J. 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. Journal of Applied Microbiology 1998, 84(5):759-768.
17. 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.
18. Coppa G.V., Gabrielli O., Pierani P., Catassi C., Carlucci A., Giorgi P.L. Changes in carbohydrate composition in human milk over 4 months of lactation. Pediatrics 1993, 91(3):637-641.
19. Corthésy B., Gaskins H.R., Mercenier A. Cross-talk between probiotic bacteria and the host immune system. The Journal of Nutrition 2007, 137(3):781S-790S.
20. Cummings J.H., Antoine J.-M., Azpiroz F., Bourdet-Sicard R., Brandtzaeg P., Calder P.C., et al. PASSCLAIM1-gut health and immunity. European Journal of Nutrition 2004, 43(2):ii118-ii173.
21. de Vos P., Faas M.M., Spasojevic M., Sikkema J. Encapsulation for preservation of functionality and targeted delivery of bioactive food components. International Dairy Journal 2010, 20(4):292-302.
22. Derbyshire E., Wright D., Boulter D. Legumin and vicilin, storage proteins of legume seeds. Phytochemistry 1976, 15:3-24.
23. Di Giacinto C., Marinaro M., Sanchez M., Strober W., Boirivant M. Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-β-bearing regulatory cells. The Journal of Immunology 2005, 174(6):3237-3246.
24. Ding W., Shah N. Acid, bile, and heat tolerance of free and microencapsulated probiotic bacteria. Journal of Food Science 2007, 72(9):M446-M450.
25. Doherty S., Auty M., Stanton C., Ross R., Fitzgerald G., Brodkorb A. Survival of entrapped Lactobacillus rhamnosus GG in whey protein micro-beads during simulated ex vivo gastro-intestinal transit. International Dairy Journal 2012, 22(1):31-43.
26. Doherty S., Gee V., Ross R., Stanton C., Fitzgerald G., Brodkorb A. Development and characterisation of whey protein micro-beads as potential matrices for probiotic protection. Food Hydrocolloids 2011, 25(6):1604-1617.
27. Donsi F., Senatore B., Huang Q., Ferrari G. Development of novel pea protein-based nanoemulsions for delivery of nutraceuticals. Journal of Agricultural and Food Chemistry 2010, 58(19):10653-10660.
28. Ducel V., Richard J., Saulnier P., Popineau Y., Boury F. Evidence and characterization of complex coacervates containing plant proteins: Application to the microencapsulation of oil droplets. Colloids and Surfaces A: Physicochemical and Engineering Aspects 2004, 232(2):239-247.
29. EFSA EFSA. Guidance on the scientific. 462 requirements for health claims related to gut and immune function. EFSA Journal 2011, 9. (1984).
30. Fanaro S., Boehm G., Garssen J., Knol J., Mosca F., Stahl B., et al. Galacto-oligosaccharides and long-chain fructo-oligosaccharides as prebiotics in infant formulas: A review. Acta Paediatrica 2005, 94(s449):22-26.
31. FAO/WHO Report of a joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria 2001, World Health Organization and Food and Agriculture Organization of the United Nations, London, Ontario, Canada.
32. Fox P.F. Advanced dairy chemistry. Bd. 1. Proteins 2003, Vol. 1. Springer.
33. Francavilla R., Lionetti E., Castellaneta S., Ciruzzi F., Indrio F., Masciale A., et al. Randomised clinical trial: Lactobacillus reuteri DSM 17938 vs. placebo in children with acute diarrhoea-a double-blind study. Alimentary Pharmacology & Therapeutics 2012, 36(4):363-369.
34. Fuller R. Probiotics in man and animals. Journal of Applied Microbiology 1989, 66(5):365-378.
35. Gardiner G., O'sullivan E., Kelly J., Auty M., Fitzgerald G., Collins J., et al. Comparative survival rates of human-derived probiotic Lactobacillus paracasei and L. salivarius strains during heat treatment and spray drying. Applied and Environmental Microbiology 2000, 66(6):2605-2612.
36. Garrigues C., Johansen E., Pedersen M.B. Complete genome sequence of Bifidobacterium animalis subsp. lactis BB-12, a widely consumed probiotic strain. Journal of Bacteriology 2010, 192(9):2467-2468.
37. Gharsallaoui A., Saurel R., Chambin O., Voilley A. Pea (Pisum sativum, L.) protein isolate stabilized emulsions: A novel system for microencapsulation of lipophilic ingredients by spray drying. Food and Bioprocess Technology 2012, 5(6):2211-2221.
38. Gouin S. Microencapsulation: Industrial appraisal of existing technologies and trends. Trends in Food Science & Technology 2004, 15(7):330-347.
39. Granato D., Branco G.F., Nazzaro F., Cruz A.G., Faria J.A. Functional foods and nondairy probiotic food development: Trends, concepts, and products. Comprehensive Reviews in Food Science and Food Safety 2010, 9(3):292-302.
40. Guerrero M., Dohnalek M., Newton P., Kuznetsova O., Ruiz-Palacios G., Murphy T., et al. Effect of probiotic-containing beverages on incidence of diarrhoea. Paper presented at the 1st World Congress of Pediatric Infectious Diseases 1996.
41. Gunasekaran S., Ko S., Xiao L. Use of whey proteins for encapsulation and controlled delivery applications. Journal of Food Engineering 2007, 83(1):31-40.
42. Harmsen H.J., Wildeboer-Veloo A.C., Raangs G.C., Wagendorp A.A., Klijn N., Bindels J.G., et al. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. Journal of Pediatric Gastroenterology and Nutrition 2000, 30(1):61-67.
43. He F., Ouwehand A.C., Isolauri E., Hashimoto H., Benno Y., Salminen S. Comparison of mucosal adhesion and species identification of bifidobacteria isolated from healthy and allergic infants. FEMS Immunology & Medical Microbiology 2001, 30(1):43-47.
44. He F., Ouwehand A.C., Isolauri E., Hosoda M., Benno Y., Salminen S. Differences in composition and mucosal adhesion of bifidobacteria isolated from healthy adults and healthy seniors. Current Microbiology 2001, 43(5):351-354.
45. Heidebach T., Först P., Kulozik U. Microencapsulation of probiotic cells by means of rennet-gelation of milk proteins. Food Hydrocolloids 2009, 23(7):1670-1677.
46. Heidebach T., Först P., Kulozik U. Transglutaminase-induced caseinate gelation for the microencapsulation of probiotic cells. International Dairy Journal 2009, 19(2):77-84.
47. Heidebach T., Först P., Kulozik U. Influence of casein-based microencapsulation on freeze-drying and storage of probiotic cells. Journal of Food Engineering 2010, 98(3):309-316.
48. Holscher H.D., Czerkies L.A., Cekola P., Litov R., Benbow M., Santema S., et al. Bifidobacterium lactis Bb12 enhances intestinal antibody response in formula-fed infants a randomized, double-blind, controlled trial. Journal of Parenteral and Enteral Nutrition 2012, 36(1 Suppl.):106S-117S.
49. Indrio F., Riezzo G., Raimondi F., Bisceglia M., Filannino A., Cavallo L., et al. Lactobacillus reuteri accelerates gastric emptying and improves regurgitation in infants. European Journal of Clinical Investigation 2011, 41(4):417-422.
50. Jankovic I., Sybesma W., Phothirath P., Ananta E., Mercenier A. Application of probiotics in food products-challenges and new approaches. Current Opinion in Biotechnology 2010, 21(2):175-181.
51. Jantzen M., Göpel A., Beermann C. Direct spray drying and microencapsulation of probiotic Lactobacillus reuteri from slurry fermentation with whey. Journal of Applied Microbiology 2013, 115(4):1029-1036.
52. Kailasapathy Microencapsulation of probiotic bacteria: Technology and potential applications. Current Issues in Intestinal Microbiology 2002, 3(2):39-48.
53. Kailasapathy Encapsulation technologies for functional foods and nutraceutical product development. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2009, 4(033):1-19.
54. Khan N.H., Korber D.R., Low N.H., Nickerson M.T. Development of extrusion-based legume protein isolate-alginate capsules for the protection and delivery of the acid sensitive probiotic, Bifidobacterium adolescentis. Food Research International 2013, 54(1):730-737.
55. Klemmer K.J., Korber D.R., Low N.H., Nickerson M.T. Pea protein-based capsules for probiotic and prebiotic delivery. International Journal of Food Science & Technology 2011, 46(11):2248-2256.
56. Koletzko B., Ashwell M., Beck B., Bronner A., e, e, Mathioudakis B. Characterisation of infant food modifications in the European Union. Annals of Nutrition and Metabolism 2002, 46(6):231-242.
57. Koyoro H., Powers J. Functional properties of pea globulin fractions. Cereal Chemistry 1987, 64(2):97.
58. Krasaekoopt W., Bhandari B., Deeth H. Evaluation of encapsulation techniques of probiotics for yoghurt. International Dairy Journal 2003, 13(1):3-13.
59. Lakkis J.M. Encapsulation and controlled release technologies in food systems 2008, Wiley, (com).
60. Lammers K.M., Brigidi P., Vitali B., Gionchetti P., Rizzello F., Caramelli E., et al. Immunomodulatory effects of probiotic bacteria DNA: IL-1 and IL-10 response in human peripheral blood mononuclear cells. FEMS Immunology & Medical Microbiology 2003, 38(2):165-172.
61. Larsen N., Vogensen F.K., Gøbel R., Michaelsen K.F., Al-Soud W.A., Sørensen S.J., et al. Predominant genera of fecal microbiota in children with atopic dermatitis are not altered by intake of probiotic bacteria Lactobacillus acidophilus NCFM and Bifidobacterium animalis subsp. lactis Bi-07. FEMS Microbiology Ecology 2011, 75(3):482-496.
62. Livney Y.D. Milk proteins as vehicles for bioactives. Current Opinion in Colloid & Interface Science 2010, 15(1):73-83.
63. Manzoni P., Lista G., Gallo E., Marangione P., Priolo C., Fontana P., et al. Routine Lactobacillus rhamnosus GG administration in VLBW infants: A retrospective, 6-year cohort study. Early Human Development 2011, 87:S35-S38.
64. Mitropoulou G., Nedovic V., Goyal A., Kourkoutas Y. Immobilization technologies in probiotic food production. Journal of nutrition and metabolism 2013, 2013.
65. Mohan R., Koebnick C., Schildt J., Schmidt S., Mueller M., Possner M., et al. Effects of Bifidobacterium lactis Bb12 supplementation on intestinal microbiota of preterm infants: A double-blind, placebo-controlled, randomized study. Journal of Clinical Microbiology 2006, 44(11):4025-4031.
66. Mortazavian A., Azizi A., Ehsani M., Razavi S., Mousavi S., Sohrabvandi S., et al. Survival of encapsulated probiotic bacteria in Iranian yogurt drink (Doogh) after the product exposure to simulated gastrointestinal conditions. Milchwissenschaft 2008, 63(4):427-429.
67. Mugambi M.N., Musekiwa A., Lombard M., Young T., Blaauw R. Synbiotics, probiotics or prebiotics in infant formula for full term infants: A systematic review. Nutrition Journal 2012, 11:81.
68. Nesterenko A., Alric I., Silvestre F., Durrieu V. Vegetable proteins in microencapsulation: A review of recent interventions and their effectiveness. Industrial Crops and Products 2013, 42:469-479.
69. Ouwehand A.C. Antiallergic effects of probiotics. The Journal of Nutrition 2007, 137(3):794S-797S.
70. Pärtty A., Luoto R., Kalliomäki M., Salminen S., Isolauri E. Effects of early prebiotic and probiotic supplementation on development of gut microbiota and fussing and crying in preterm infants: A randomized, double-blind, placebo-controlled trial. The Journal of Pediatrics 2013, 163(5):1272-1277. (e1272).
71. Patel A.K., Singhania R.R., Pandey A., Chincholkar S.B. Probiotic bile salt hydrolase: Current developments and perspectives. Applied Biochemistry and Biotechnology 2010, 162(1):166-180.
72. Phillips G.O., Williams P.A. Handbook of food proteins 2011, Elsevier.
73. 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.
74. Roos S., Dicksved J., Tarasco V., Locatelli E., Ricceri F., Grandin U., et al. 454 Pyrosequencing analysis on faecal samples from a randomized DBPC trial of colicky infants treated with Lactobacillus reuteri DSM 17938. PloS One 2013, 8(2):e56710.
75. Rosander A., Connolly E., Roos S. Removal of antibiotic resistance gene-carrying plasmids from Lactobacillus reuteri ATCC 55730 and characterization of the resulting daughter strain, L. reuteri DSM 17938. Applied and Environmental Microbiology 2008, 74(19):6032-6040.
76. Roy F., Boye J., Simpson B. Bioactive proteins and peptides in pulse crops: Pea, chickpea and lentil. Food Research International 2010, 43(2):432-442.
77. Ruiz-Palacios G., Tuz F., Arteaga F., Guerrero M.L., Dohnalek M., Hilty M. Tolerance and fecal colonization with Lactobacillus reuteri in children fed a beverage with a mixture of Lactobacillus spp. 1090. Pediatric Research 1996, 39:184.
78. Saavedra J.M., Abi-Hanna A., Moore N., Yolken R.H. Long-term consumption of infant formulas containing live probiotic bacteria: tolerance and safety. The American Journal of Clinical Nutrition 2004, 79(2):261-267.
79. Saier M.H., Mansour N.M. Probiotics and prebiotics in human health. Journal of Molecular Microbiology and Biotechnology 2006, 10(1):22-25.
80. Sanders M., Klaenhammer T. Invited review: The scientific basis of Lactobacillus acidophilus NCFM functionality as a probiotic. Journal of Dairy Science 2001, 84(2):319-331.
81. Savino F., Pelle E., Palumeri E., Oggero R., Miniero R. Lactobacillus reuteri (American type culture collection strain 55730) versus simethicone in the treatment of infantile colic: A prospective randomized study. Pediatrics 2007, 119(1):e124-e130.
82. Schmidt C. The startup bugs. Nature Biotechnology 2013, 31(4):279-281.
83. Semyonov D., Ramon O., Kaplun Z., Levin-Brener L., Gurevich N., Shimoni E. Microencapsulation of Lactobacillus paracasei by spray freeze drying. Food Research International 2010, 43(1):193-202.
84. Shah N.P. Functional cultures and health benefits. International Dairy Journal 2007, 17(11):1262-1277.
85. Sirtori E., Isak I., Resta D., Boschin G., Arnoldi A. Mechanical and thermal processing effects on protein integrity and peptide fingerprint of pea protein isolate. Food Chemistry 2012, 134(1):113-121.
86. Soh S., Aw M., Gerez I., Chong Y., Rauff M., Ng Y., et al. Probiotic supplementation in the first 6months of life in at risk Asian infants-effects on eczema and atopic sensitization at the age of 1year. Clinical & Experimental Allergy 2009, 39(4):571-578.
87. Solis G., de Los Reyes-Gavilan C., Fernandez N., Margolles A., Gueimonde M. Establishment and development of lactic acid bacteria and bifidobacteria microbiota in breast-milk and the infant gut. Anaerobe 2010, 16(3):307-310.
88. Sullivan F. Strategic analysis of the European pea market 2010.
89. Sung V., Hiscock H., Tang M.L., Mensah F.K., Nation M.L., Satzke C., et al. Treating infant colic with the probiotic Lactobacillus reuteri: Double blind, placebo controlled randomised trial. BMJ [British Medical Journal] 2014, 348.
90. Szajewska H., Gyrczuk E., Horvath A. Lactobacillus reuteri DSM 17938 for the management of infantile colic in breastfed infants: A randomized, double-blind, placebo-controlled trial. The Journal of Pediatrics 2013, 162(2):257-262.
91. Taipale T., Pienihäkkinen K., Isolauri E., Larsen C., Brockmann E., Alanen P., et al. Bifidobacterium animalis subsp. lactis BB-12 in reducing the risk of infections in infancy. British Journal of Nutrition 2011, 105(03):409-416.
92. Talarico T., Casas I., Chung T.C., Dobrogosz W. Production and isolation of reuterin, a growth inhibitor produced by Lactobacillus reuteri. Antimicrobial Agents and Chemotherapy 1988, 32(12):1854-1858.
93. Thomas D.W., Greer F.R. Probiotics and prebiotics in pediatrics. Pediatrics 2010, 126(6):1217-1231.
94. Van Baarlen P., Troost F.J., van Hemert S., van der Meer C., de Vos W.M., de Groot P.J., et al. Differential NF-κB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proceedings of the National Academy of Sciences 2009, 106(7):2371-2376.
95. van den Nieuwboer M., Claassen E., Morelli L., Guarner F., Brummer R. Probiotic and synbiotic safety in infants under two years of age. Beneficial Microbes 2014, 1-16.
96. Vandenplas Y. Oligosaccharides in infant formula. British Journal of Nutrition 2002, 87(2):293-296.
97. Vendt N., Grünberg H., Tuure T., Malminiemi O., Wuolijoki E., Tillmann V., et al. Growth during the first 6months of life in infants using formula enriched with Lactobacillus rhamnosus GG: Double-blind, randomized trial. Journal of Human Nutrition and Dietetics 2006, 19(1):51-58.
98. Vlieger A.M., Robroch A., van Buuren S., Kiers J., Rijkers G., Benninga M.A., et al. Tolerance and safety of Lactobacillus paracasei ssp. paracasei in combination with Bifidobacterium animalis ssp. lactis in a prebiotic-containing infant formula: a randomised controlled trial. British Journal of Nutrition 2009, 102(6):869.
99. Weinbreck F., Bodnár I., Marco M. Can encapsulation lengthen the shelf-life of probiotic bacteria in dry products?. International Journal of Food Microbiology 2010, 136(3):364-367.
100. Whelehan M., Marison I.W. Microencapsulation using vibrating technology. Journal of Microencapsulation 2011, 28(8):669-688.
101. Yoshioka H., Iseki K.-i, Fujita K. Development and differences of intestinal flora in the neonatal period in breast-fed and bottle-fed infants. Pediatrics 1983, 72(3):317-321.