Applied Microbiology and Biotechnology

, Volume 98, Issue 2, pp 563–577 | Cite as

Bifidobacteria: their impact on gut microbiota composition and their applications as probiotics in infants

  • Diana Di Gioia
  • Irene Aloisio
  • Giuseppe Mazzola
  • Bruno Biavati
Mini-Review

Abstract

This review is aimed at describing the most recent advances in the gut microbiota composition of newborns and infants with a particular emphasis on bifidobacteria. The newborn gut microbiota is quite unstable, whereas after weaning, it becomes more stable and gets closer to the typical adult microbiota. The newborn and infant gut microbiota composition is impaired in several enteric and non-enteric pathologies. The core of this review is the description of the most recent documented applications of bifidobacteria to newborns and infants for their prevention and treatment. Acute diarrhea is the most studied disease for which bifidobacteria are applied with great success, Bifidobacterium longum and Bifidobacterium breve being the most applied species. Moreover, the most recent updates in the use of bifidobacteria for the prevention and treatment of pathologies typical of newborns, such as necrotizing enterocolitis, colics, and streptococcal infections, are presented. In addition, a number of not strictly enteric pathologies have in recent years evidenced a strict correlation with an aberrant gut microbiota in infants, in particular showing a reduced level of bifidobacteria. These diseases represent new potential opportunities for probiotic applications. Among them, allergic diseases, celiac disease, obesity, and neurologic diseases are described in this review. The preliminary use of bifidobacteria in in vitro systems and animal models is summarized as well as preliminary in vivo studies. Only after validation of the results via human clinical trials will the potentiality of bifidobacteria in the prevention and cure of these pathologies be definitely assessed.

Keywords

Bifidobacteria Gut microbiota Infants Newborns Probiotics Therapeutic microbiology 

References

  1. Akobeng AK, Ramanan AV, Buchan I, Heller RF (2006) Effect of breast feeding on risk of coeliac disease: a systematic review and meta-analysis of observational studies. Arch Dis Child 91:39–43PubMedGoogle Scholar
  2. Aloisio I, Santini C, Biavati B, Dinelli G, Cencič A, Chingwaru W, Mogna L, Di Gioia D (2012) Characterization of Bifidobacterium spp. strains for the treatment of enteric disorders in newborns. Appl Microbiol Biotechnol 96:1561–1576PubMedGoogle Scholar
  3. Amisano G, Fornasero S, Migliaretti G, Caramello S, Tarasco V, Savino F (2011) Diarrheagenic Escherichia coli in acute gastroenteritis in infants in North-West Italy. New Microbiol 34:45–51PubMedGoogle Scholar
  4. An HM, Park SY, Lee do K, Kim JR, Cha MK, Lee SW, Lim HT, Kim KJ, Ha NJ (2011) Antiobesity and lipid-lowering effects of Bifidobacterium spp. in high fat diet-induced obese rats. Lipids Health Dis 10:116PubMedCentralPubMedGoogle Scholar
  5. Arboleya S, Ruas-Madiedo P, Margolles A, Solís G, Salminen S, de Los Reyes-Gavilán CG, Gueimonde M (2011) Characterization and in vitro properties of potentially probiotic Bifidobacterium strains isolated from breast-milk. Int J Food Microbiol 149:28–36PubMedGoogle Scholar
  6. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101:15718–15723PubMedCentralPubMedGoogle Scholar
  7. Barclay AR, Stenson B, Simpson JH, Weaver LT, Wilson DC (2007) Probiotics for necrotizing enterocolitis: a systematic review. J Pediatr Gastroenterol Nutr 45:569–576PubMedGoogle Scholar
  8. Barrett E, Guinane C, Ryan A, Dempsey E, Murphy B, O’Toole P, Fizgerarld G, Cotter P, Ross P, Stanton C (2013) Microbiota diversity and stability of the preterm neonatal ileum and colon of two infants. MicrobiolOpen 2:215–225Google Scholar
  9. Bercik P, Park AJ, Sinclair D, Khoshdel A, Lu J, Huang X, Deng Y, Blennerhassett P, Fahnestock M, Moine D, Berger B, Huizinga J, Kunze W, Mclean P, Bergonzelli G, Collins S, Verdu E (2011) The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut–brain communication. Neurogastroenterol Motil 23:1132–1139PubMedCentralPubMedGoogle Scholar
  10. Bezirtzoglou E, Tsiotsias A, Welling GW (2011) Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe 17:478–482PubMedGoogle Scholar
  11. Biasucci G, Rubini M, Riboni S, Morelli L, Bessi E, Retetangos C (2010) Mode of delivery affects the bacterial community in the newborn gut. Early Hum Dev 86:13–15PubMedGoogle Scholar
  12. Biavati B, Castagnoli P, Crociani F, Trovatelli LD (1984) Species of the Bifidobacterium in the feces of infants. Microbiologica 7:341–345PubMedGoogle Scholar
  13. Biavati B, Vescovo M, Torriani S, Bottazzi V (2000) Bifidobacteria: history, ecology, physiology and applications. Ann Microbiol 50:117–131Google Scholar
  14. Bingley PJ, Williams AJ, Norcross AJ, Unsworth DJ, Lock RJ, Ness AR, Jones RW (2004) Undiagnosed coeliac disease at age seven: population based prospective birth cohort study. BMJ 328:322–323PubMedGoogle Scholar
  15. Blaut M, Bischoff SC (2010) Probiotics and obesity. Ann Nutr Metab 57:20–23PubMedGoogle Scholar
  16. Boyle RJ, Tang ML (2006) The role of probiotics in the management of allergic diseases. Clin Exp Allergy 36:568–576PubMedGoogle Scholar
  17. Braga TD, da Silva GA, de Lira PI, de Carvalho Lima M (2011) Efficacy of Bifidobacterium breve and Lactobacillus casei oral supplementation on necrotizing enterocolitis in very-low-birth-weight preterm infants: a double-blind, randomized, controlled trial. Am J Clin Nutr 93:81–86PubMedGoogle Scholar
  18. Cabana MD, McKean M, Wong AR, Chao C, Caughey AB (2007) Examining the hygiene hypothesis: the trial of infant probiotic supplementation. Paediatr Perinat Epidemiol 21:23–28PubMedGoogle Scholar
  19. Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM, Gibson GR, Delzenne NM (2007) Selective increases of bifidobacteria in gut microflora improves high-fat diet induced diabetes in mice through a mechanism associated with endotoxemia. Diabetologia 50:2374–2383PubMedGoogle Scholar
  20. Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, Geurts L, Naslain D, Neyrinck A, Lambert DM, Muccioli GG, Delzenne NM (2009) Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2 driven improvement of gut permeability. Gut 58:1091–1103PubMedCentralPubMedGoogle Scholar
  21. Claud EC, Walker WA (2001) Hypothesis: inappropriate colonization of the premature intestine can cause neonatal necrotizing enterocolitis. FASEB J 15:1398–1403PubMedGoogle Scholar
  22. Collado MC, Calabuig M, Sanz Y (2007) Differences between the faecal microbiota of coeliac children and healthy controls. Curr Issues Intest Microbiol 8:9–14PubMedGoogle Scholar
  23. Collado MC, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y (2008) Imbalances in faecal and duodenal Bifidobacterium species composition in active and non-active celiac disease. BMC Microbiol 8:232PubMedCentralPubMedGoogle Scholar
  24. Collins SM, Bercik P (2009) The relationship between intestinal microbiota and the central nervous system in normal gastrointestinal function and disease. Gastroenterology 136:2003–2014PubMedGoogle Scholar
  25. Coppa G, Gabrielli O (2008) Human milk oligosaccharides as prebiotics. In: Versalovic J, Wilson M (eds) Therapeutic microbiology: probiotics and related strategies. American Society for Microbiology Press, Washington, pp 131–146Google Scholar
  26. Corvaglia L, Legnani E, Di Gioia D, Aloisio I, Martini S, Oss M, Biavati B, Faldella G (2012) Effects of intrapartum antibiotic prophylaxis on newborn microbiota. Arch Dis Child 97:A380. doi:10.1136/archdischild-2012-302724.1334, Abstract at the 4th Congress of the European Academy of Paediatric Societies (EAPS). Istanbul, Turkey, 5–9 October 2012Google Scholar
  27. Cryan JF, O'Mahony SM (2011) The microbiome–gut–brain axis: from bowel to behavior. Neurogastroenterol Motil 23:187–192PubMedGoogle Scholar
  28. De Angelis M, Rizzello CG, Fasano A, Clemente MG, De Simone C, Silano M, De Vincenzi M, Losito I, Gobbetti M (2006) Vsl#3 probiotic preparation has the capacity to hydrolyze gliadin polypeptides responsible for Celiac Sprue. Biochim Biophys Acta 1762:80–93PubMedGoogle Scholar
  29. de Weerth C, Fuentes S, Puylaert P, de Vos M (2013) Intestinal microbiota of infants with colic: development and specific signatures. Pediatrics 131:e550–e558PubMedGoogle Scholar
  30. Desbonnet L, Garrett L, Clarke G, Bienenstock J, Dinan T (2008) The probiotic Bifidobacterium infantis: an assessment of potential antidepressant properties in the rat. J Psychiatr Res 43:164–174PubMedGoogle Scholar
  31. Deshpande G, Rao S, Patole S (2007) Probiotics for prevention of necrotizing enterocolitis in preterm neonates with very low birthweight: a systematic review of randomized controlled trials. Lancet 369:1614–1620PubMedGoogle Scholar
  32. Deshpande G, Rao S, Patole S, Bulsara M (2010) Updated meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Pediatrics 125:921–930PubMedGoogle Scholar
  33. Deshpande GC, Rao SC, Keil AD, Patole SK (2011) Evidence-based guidelines for use of probiotics in preterm neonates. BMC Med 9:92PubMedCentralPubMedGoogle Scholar
  34. Di Felice G, Barletta B, Butteroni C, Corinti S, Tinghino R, Colombo P, Boirivant M (2008) Use of probiotic bacteria for prevention and therapy of allergic diseases: studies in mouse model of allergic sensitization. J Clin Gastroenterol 42:130–132Google Scholar
  35. Dotan I, Rachmilewitz D (2005) Probiotics in inflammatory bowel disease: possible mechanisms of action. Curr Opin Gastroenterol 21:426–430PubMedGoogle Scholar
  36. Dubois PC, van Heel DA (2008) Translational mini-review series on the immunogenetics of gut disease: immunogenetics of coeliac disease. Clin Exp Immunol 153:162–173PubMedCentralPubMedGoogle Scholar
  37. EFSA (2013) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011. EFSA J 11:3129, 250 ppGoogle Scholar
  38. Fallani M, Young D, Scott J, Norin E, Amarri S, Adam R, Aguilera M, Khanna S, Gil A, Edwards CA, Doré J, INFABIO team (2010) Intestinal microbiota of 6-week-old infants across Europe: geographic influence beyond delivery mode, breast-feeding, and antibiotics. J Pediatr Gastroenterol Nutr 51:77–84PubMedGoogle Scholar
  39. Fallani M, Amarri S, Uusijarvi A, Adam R, Khanna S, Aguilera M, Gil A, Vieites JM, Norin E, Young D, Scott JA, Doré J, Edwards CA, INFABIO team (2011) Determinants of the human infant intestinal microbiota after the introduction of first complementary foods in infant samples from five European centres. Microbiology 157:1385–1392PubMedGoogle Scholar
  40. Fasano A, Catassi C (2005) Coeliac disease in children. Best Pract Res Clin Gastroenterol 19:467–478PubMedGoogle Scholar
  41. Favier CF, Vaughan EE, De Vos WM, Akkermans AD (2002) Molecular monitoring of succession of bacterial communities in human neonates. Appl Environ Microbiol 68:219–226PubMedCentralPubMedGoogle Scholar
  42. Feleszko W, Jaworska J, Rha RD, Steinhausen S, Avagyan A, Jandzus A, Ahreus B, Gronenberg DA, Wahn V, Hamelmann E (2007) Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma. Clin Exp Allergy 37:498–505PubMedGoogle Scholar
  43. Ferrieri P, Wallen L (2012) Neonatal bacterial sepsis. In: Gleason CA, Devaskar SU (eds) Avery's disease of the newborn. Elsevier, Amsterdam, pp 538–550Google Scholar
  44. Forsythe P, Sudo N, Dinan T, Taylor V, Bienenstock J (2010) Mood and gut feelings. Brain Behav Immun 24:9–16PubMedGoogle Scholar
  45. Grandy G, Medina M, Soria R, Terán CG, Araya M (2010) Probiotics in the treatment of acute rotavirus diarrhoea. A randomized, double-blind, controlled trial using two different probiotic preparations in Bolivian children. BMC Infect Dis 10:253PubMedCentralPubMedGoogle Scholar
  46. Green PH, Cellier C (2007) Celiac disease. N Engl J Med 357:1731–1743PubMedGoogle Scholar
  47. Gueimonde M, Ouwehand A, Huhtinen H, Salminen E, Salminen S (2007) Qualitative and quantitative analyses of the bifidobacterial microbiota in the colonic mucosa of patients with colorectal cancer, diverticulitis and inflammatory bowel disease. World J Gastroenterol 13:3985–3989PubMedGoogle Scholar
  48. Hammerman C, Bin-Nun A, Kaplan M (2006) Safety of probiotics: comparison of two popular strains. BMJ 333:1006–1008PubMedGoogle Scholar
  49. Hansen CH, Nielsen DS, Kverka M, Zakostelska Z, Klimesova K, Hudcovic T, Tlaskalova-Hogenova H, Hansen AK (2012) Patterns of early gut colonization shape future immune responses of the host. PLoS One 7:e34043PubMedCentralPubMedGoogle Scholar
  50. Harder T, Bergmann R, Kallischnigg G, Plagemann A (2005) Duration of breastfeeding and risk of overweight: a meta-analysis. Am J Epidemiol 162:397–403PubMedGoogle Scholar
  51. Hunter CJ, Upperman JS, Ford HR, Camerini V (2008) Understanding the susceptibility of the premature infant to necrotizing enterocolitis (NEC). Pediatr Res 63:117–123PubMedGoogle Scholar
  52. Indrio F, Neu J (2011) The intestinal microbiome of infants and the use of probiotics. Curr Opin Pediatr 23:145–150PubMedCentralPubMedGoogle Scholar
  53. Isolauri E (2004) Dietary modification of atopic disease: use of probiotics in the prevention ofatopic dermatitis. Curr Allergy Asthma Rep 4:270–275PubMedGoogle Scholar
  54. Isolauri E, Salminen S (2008) Probiotics: use in allergic disorders: a Nutrition, Allergy, Mucosal Immunology, and Intestinal Microbiota (NAMI) Research Group Report. J Clin Gastroenterol 42:S91–S96PubMedGoogle Scholar
  55. Isolauri E, Arvola T, Sutas Y, Moilanen E, Salminen S (2000) Probiotics in the management of atopic eczema. Clin Exp Allergy 30:1604–1610PubMedGoogle Scholar
  56. Ivarsson A, Hernell O, Stenlund H, Persson LA (2002) Breast-feeding protects against celiac disease. Am J Clin Nutr 75:914–921PubMedGoogle Scholar
  57. Kailasapathy (2008) Formulation, administration, and delivery of probiotics. In: Versalovic J, Wilson M (eds) Therapeutic microbiology: probiotics and related strategies. American Society for Microbiology, Washington, pp 97–118Google Scholar
  58. Kalliomaki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E (2001) Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol 107:129–134PubMedGoogle Scholar
  59. Kalliomaki M, Collado MC, Salminen S, Isolauri E (2008) Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr 87:534–538PubMedGoogle Scholar
  60. Kaur IP, Chopra K, Saini A (2002) Probiotics: potential pharmaceutical applications. Eur J Pharm Sci 15:1–9PubMedGoogle Scholar
  61. Khailova L, Dvorak K, Arganbright KM, Halpern MD, Kinouchi T, Yajima M, Dvorak B (2009) Bifidobacterium bifidum improves intestinal integrity in a rat model of necrotizing enterocolitis. Am J Physiol Gastrointes Liver Physio 1297:940–949Google Scholar
  62. Klaassens ES, Boesten RJ, Haarman M, Knol J, Schuren FH, Vaughan EE, de Vos WM (2009) Mixed-species genomic microarray analysis of fecal samples reveals differential transcriptional responses of bifidobacteria in breast- and formula-fed infants. Appl Environ Microbiol 75:2668–2676PubMedCentralPubMedGoogle Scholar
  63. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT, Ley RE (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A 108:4578–4585PubMedCentralPubMedGoogle Scholar
  64. Kuitunen M, Kukkonen K, Juntunen-Backman K, Korpela R, Poussae T, Tuure T, Haahtela T, Savilahti E (2009) Probiotics prevent IgE-associated allergy until age 5 years in caesarean delivered children but not in the total cohort. J Allergy Clin Immunol 123:335–341PubMedGoogle Scholar
  65. Lawlor DA, Smith GD, O'Callaghan M, Alati R, Mamun AA, Williams GM, Najman JM (2007) Epidemiologic evidence for the fetal over-nutrition hypothesis: findings from the Mater-University study of pregnancy and its outcomes. Am J Epidemiol 165:418–424PubMedGoogle Scholar
  66. Li Y, Shimizu T, Hosaka A, Kaneko N, Ohtsuka Y, Yamashiro Y (2004) Effects of Bifidobacterium breve supplementation on intestinal flora of low birth weight infants. Pediatr Int 46:509–515PubMedGoogle Scholar
  67. Lin HC, Hsu CH, Chen HL, Chung MY, Hsu JF, Lien RI, Tsao LY, Chen CH, Su BH (2008) Oral probiotics prevent necrotizing enterocolitis in very low birth weight preterm infants: a multicenter, randomized, controlled trial. Pediatrics 122:693–700PubMedGoogle Scholar
  68. Lindfors K, Blomqvist T, Juuti-Uusitalo K, Stenman S, Venäläinen J, Mäki M, Kaukinen K (2008) Live probiotic Bifidobacterium lactis bacteria inhibit the toxic effects induced by wheat gliadin in epithelial cell culture. Clin Exp Immunol 152:552–558PubMedCentralPubMedGoogle Scholar
  69. Londei M, Ciacci C, Ricciardelli I, Vacca L, Quaratino S, Maiuri L (2005) Gliadin as a stimulator of innate responses in celiac disease. Mol Immunol 42:913–918PubMedGoogle Scholar
  70. Lowenthal A, Livni G, Amir J, Samra Z, Ashkenazi S (2006) Secondary bacteremia after rotavirus gastroenteritis in infancy. Pediatrics 117:224–226PubMedGoogle Scholar
  71. Ma X, Hua J, Li Z (2008) Probiotics improve high fat diet-induced hepatic steatosis and insulin resistance by increasing hepatic NKT cells. J Hepatol 49:821–830PubMedCentralPubMedGoogle Scholar
  72. Magne F, Hachelaf W, Suau A, Boudraa G, Mangin I, Touhami M, Bouziane-Nedjadi K, Pochart P (2006) A longitudinal study of infant faecal microbiota during weaning. FEMS Microbiol Ecol 58:563–571PubMedGoogle Scholar
  73. Mai V, Young CM, Ukhanova M, Wang X, Sun Y, Casella G, Theriaque D, Li N, Sharma R, Hudak M, Neu J (2011) Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS One 6:e20647PubMedCentralPubMedGoogle Scholar
  74. Meresse B, Ripoche J, Heyman M, Cerf-Bensussan N (2009) Celiac disease: from oral tolerance to intestinal inflammation, autoimmunity and lymphomagenesis. Mucosal Immunol 2:8–23PubMedGoogle Scholar
  75. Messaoudi M, Lalonde R, Violle N, Javelot H, Desor D, Nejedi A, Bisson J, Roujeot C, PichelIn M, Cazaubiel M, Cazaubiel J (2010) Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr 26:1–9Google Scholar
  76. Million M, Maraninchi M, Henry F, Armougom F, Richet Carrieri H, Valero R, Raccah D, Viallettes B, Raoult D (2012) Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int J Obes 36:817–825Google Scholar
  77. Million M, Angelakis E, Maraninchi M, Henry M, Giorgi R, Valero R, Vialettes B, Raoult D (2013) Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli. Int J Obes 37(11):1460–1467Google Scholar
  78. Mohan R, Koebnick C, Schildt J, Schmidt S, Mueller M, Possner M, Radke M, Blaut M (2006) Effects of Bifidobacterium lactis Bb12 supplementation on intestinal microbiota of preterm infants: a double-blind, placebo-controlled, randomized study. J Clin Microbiol 44:4025–4031PubMedCentralPubMedGoogle Scholar
  79. Mulder CJ, Bartelsman JF (2005) Case-finding in coeliac disease should be intensified. Best Pract Res Clin Gastroenterol 19:479–486PubMedGoogle Scholar
  80. Muñoz JA, Chenoll E, Casinos B, Bataller E, Ramón D, Genovés S, Montava R, Ribes JM, Buesa J, Fàbrega J, Rivero M (2011) Novel probiotic Bifidobacterium longum subsp. infantis CECT 7210 strain active against rotavirus infections. Appl Environ Microbiol 77:8775–8783PubMedGoogle Scholar
  81. Nadal I, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y (2007) Imbalance in the composition of the duodenal microbiota of children with coeliac disease. J Med Microbiol 56:1669–1674PubMedGoogle Scholar
  82. Neu J, Walker WA (2011) Necrotizing enterocolitis. N Engl J Med 364:255–264PubMedCentralPubMedGoogle Scholar
  83. Ouwehand AC, Isolauri E, He F, Hashimoto H, Benno Y, Salminen S (2001) Differences in Bifidobacterium flora composition in allergic and healthy infants. J Allergy Clin Immunol 108:144–145PubMedGoogle Scholar
  84. Owen CG, Martin RM, Whincup PH, Smith GD, Cook DG (2005) The effect of infant feeding on the risk of obesity across the life course: a quantitative review of published evidence. Pediatrics 115:1367–1377PubMedGoogle Scholar
  85. Özdemir Ö (2009) Gut flora development in infancy and its effect on immune system. Çocuk Enf Derg J Pediatr Inf 3:202–203Google Scholar
  86. Özdemir Ö (2010) Variuos effects of different probiotic starins in allergic disorders: an update from laboratory and clinical data. Clin Exp Immunol 160:295–304PubMedCentralPubMedGoogle Scholar
  87. Palma GD, Capilla A, Nova E, Castillejo G, Varea V, Pozo T, Garrote JA, Polanco I, López A, Ribes-Koninckx C, Marcos A, García-Novo MD, Calvo C, Ortigosa L, Peña-Quintana L, Palau F, Sanz Y (2012) Influence of milk-feeding type and genetic risk of developing coeliac disease on intestinal microbiota of infants: the PROFICEL study. PLoS One 7:e30791PubMedCentralPubMedGoogle Scholar
  88. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5:e177PubMedCentralPubMedGoogle Scholar
  89. Penders J, Thijs C, van den Brandt PA, Kummeling I, Snijders B, Stelma F, Adams H, van Ree R, Stobberingh EE (2006) Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut 56:661–667PubMedGoogle Scholar
  90. Puopolo KM, Madoff LC, Eichenwald EC (2005) Early-onset group B streptococcal disease in the era of maternal screening. Pediatrics 115:1240–1246PubMedGoogle Scholar
  91. Rhee SH, Pothoulakis C, Mayer EA (2009) Principles and clinical implications of the brain–gut–enteric microbiota axis. Nat Rev Gastroenterol Hepatol 6:306–314PubMedGoogle Scholar
  92. Ruddick J, Evans A, Nutt D, Lightman S, Rook G, Lowry C (2006) Tryptophan metabolism in the central nervous system: medical implications. Expert Rev Mol Med 8:1–27PubMedGoogle Scholar
  93. Saavedra JM, Tschernia A (2002) Human studies with probiotics and prebiotics: clinical implications. Br J Nutr 87:241–246Google Scholar
  94. Sanders ME, Akkermans LM, Haller D, Hammerman C, Heimbach J, Hörmannsperger G, Huys G, Levy DD, Lutgendorff F, Mack D, Phothirath P, Solano-Aguilar G, Vaughan E (2010) Safety assessment of probiotics for human use. Gut Microbes 1:164–185PubMedGoogle Scholar
  95. Sanz Y, Sánchez E, Marzotto M, Calabuig M, Torriani S, Dellaglio F (2007) Differences in faecal bacterial communities in coeliac and healthy children as detected by PCR and denaturing gradient gel electrophoresis. FEMS Immunol Med Microbiol 51:562–568PubMedGoogle Scholar
  96. Sartor BR (2004) Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 126:1620–1633PubMedGoogle Scholar
  97. Savino F, Pelle E, Palumeri E, Oggero R, Miniero R (2007) Lactobacillus reuteri (American Type Culture Collection Strain 55730) versus simethicone in the treatment of infantile colic: a prospective randomized study. Pediatrics 119:124–130Google Scholar
  98. Savino F, Cordisco L, Tarasco V, Calabrese R, Palumeri E, Matteuzzi D (2009) Molecular identification of coliform bacteria from colicky breastfed infants. Acta Paediatr 98:1582–1588PubMedGoogle Scholar
  99. Savino F, Cordisco L, Tarasco V, Palumeri E, Calabrese R, Oggero R, Roos S, Matteuzzi D (2010) Lactobacillus reuteri DSM 17939 in infantile colic: a randomized, double-blind, placebo-controlled trial. Pediatrics 126:526–533Google Scholar
  100. Savino F, Cordisco L, Tarasco V, Locatelli E, Di Gioia D, Oggero R, Matteuzzi D (2011) Antagonistic effect of Lactobacillus strains against gas-producing coliforms isolated from colicky infants. BMC Microbial 11:157Google Scholar
  101. Schwiertz A, Taras D, Schäfer K, Beijer S, Bos NA, Donus C, Hardt PD (2010) Microbiota and SCFA in lean and overweight healthy subjects. Obesity 18:190–195PubMedGoogle Scholar
  102. Sisk PM, Lovelady CA, Dillard RG, Gruber KJ, O'Shea TM (2007) Early human milk feeding is associated with a lower risk of necrotizing enterocolitis in very low birth weight infants. J Perinatol 27:428–433PubMedGoogle Scholar
  103. Soh SE, Aw M, Gerez I, Chong YS, Rauff M, Ng YPM, Wong HB, Pai N, Lee BW, Shek LPC (2009) Probiotic supplementation in the first 6 months of life in at risk Asian infants—effects on eczema and atopic sensitization at the age of 1 year. Clin Exp Allergy 39:571–578PubMedGoogle Scholar
  104. Solís G, de Los Reyes-Gavilan CG, Fernández N, Margolles A, Gueimonde M (2010) Establishment and development of lactic acid bacteria and bifidobacteria microbiota in breast-milk and the infant gut. Anaerobe 16:307–310PubMedGoogle Scholar
  105. Stockman JA (2009) Newborn: probiotics for prevention of necrotising enterocolitis in preterm neonates with very low birthweight: a systematic review of randomised controlled trials. In: Deshpande G, Rao S, Patole S (eds) Yearbook of pediatrics. Elsevier, Philadelphia, pp 441–443Google Scholar
  106. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu X, Kubo C, Koga Y (2004) Postnatal microbial colonization programs the hypothalamic–pituitary–adrenal system for stress response in mice. J Physiol 558:263–275PubMedGoogle Scholar
  107. Sullivan S, Schanler RJ, Kim JH, Patel AL, Trawöger R, Kiechl-Kohlendorfer U, Chan GM, Blanco CL, Abrams S, Cotten CM, Laroia N, Ehrenkranz RA, Dudell G, Cristofalo EA, Meier P, Lee ML, Rechtman DJ, Lucas A (2010) An exclusively human milk-based diet is associated with a lower rate of necrotizing enterocolitis than a diet of human milk and bovine milk-based products. J Pediatr 156:562–567PubMedGoogle Scholar
  108. Symonds EL, O'Mahony C, Lapthorne S, O'Mahony D, Sharry JM, O'Mahony L, Shanahan F (2012) Bifidobacterium infantis 35624 protects against salmonella-induced reductions in digestive enzyme activity in mice by attenuation of the host inflammatory response. Clin Transl Gastroenterol 3:e15PubMedCentralPubMedGoogle Scholar
  109. Szajewska H, Ruszczyński M, Radzikowski A (2006) Probiotics in the prevention of antibiotic-associated diarrhea in the children: a meta-analysis of randomized controlled trials. J Pedriatr 149:367–372Google Scholar
  110. Tennyson CA, Friedman G (2008) Microecology, obesity, and probiotics. Curr Opin Endocrinol Diabetes Obes 15:422–427PubMedGoogle Scholar
  111. Tham CSC, Peh KK, Bhat R, Liong MT (2011) Probiotic properties of bifidobacteria and lactobacilli isolated from local dairy products. Ann Microbiol 62:1079–1087Google Scholar
  112. Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, Kerr C, Hourihane J, Murray D, Fuligni F, Gueimonde M, Margolles A, De Bellis G, O'Toole PW, van Sinderen D, Marchesi JR, Ventura M (2012) Diversity of bifidobacteria within the infant gut microbiota. PLoS One 7:e36957PubMedCentralPubMedGoogle Scholar
  113. Underwood MA, Kananurak A, Coursodon CF, Adkins-Reick CK, Chu H, Bennett SH, Wehkamp J, Castillo PA, Leonard BC, Tancredi DJ, Sherman MP, Dvorak B, Bevins CL (2012) Bifidobacterium bifidum in a rat model of necrotizing enterocolitis: antimicrobial peptide and protein responses. 71:546–551Google Scholar
  114. van Heel DA, West J (2006) Recent advances in coeliac disease. Gut 55:1037–1046PubMedGoogle Scholar
  115. Vandenplas Y, De Hert SG (2011) Randomised clinical trial: the synbiotic food supplement probiotical vs. placebo for acute gastroenteritis in children. Aliment Pharmacol Ther 34:862–867PubMedGoogle Scholar
  116. Verdu EF (2009) Probiotics effects on gastrointestinal function: beyond the gut? Neurogastroenterol Motil 21:477–480PubMedGoogle Scholar
  117. Viljanen M, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, Tuure T, Kuitunen M (2005) Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo-controlled trial. Allergy 60:494–500PubMedGoogle Scholar
  118. Wada M, Nagata S, Saito M, Shimizu T, Yamashiro Y, Matsuki T, Asahara T, Nomoto K (2010) Effects of the enteral administration of Bifidobacterium breve on patients undergoing chemotherapy for pediatric malignancies. Supp Care Cancer 18:751–759Google Scholar
  119. Wang C, Shoji H, Sato H, Nagata S, Ohtsuka Y, Shimizu T, Yamashiro Y (2007) Effects of oral administration of Bifidobacterium breve on fecal lactic acid and short-chain fatty acids in low birth weight infants. J Pediatr Gastroenterol Nutr 44:252–257PubMedGoogle Scholar
  120. Wassenaar TM, Klein G (2008) Safety aspects and implications of regulation of probiotic bacteria in food and food supplements. J Food Protect 71:1734–1741Google Scholar
  121. Weizman Z, Asli G, Alsheikh A (2005) Effect of a probiotic infant formula on infections in child care centers: comparison of two probiotic agents. Pediatrics 115:5–9PubMedGoogle Scholar
  122. Wiegering V, Kaiser J, Tappe D, Weissbrich B, Morbach H, Girschick HJ (2011) Gastroenteritis in childhood: a retrospective study of 650 hospitalized pediatric patients. Int J Infect Dis 15:401–407Google Scholar
  123. Xiao JZ, Kondo S, Takahashi N, Miyaji K, Oshida K, Hiramatsu A, Iwatsuki K, Kokubo S, Hosono A (2003) Effects of milk products fermented by Bifidobacterium longum on blood lipids in rats and healthy adult male volunteers. J Dairy Sci 86:2452–2461PubMedGoogle Scholar
  124. Xiao JZ, Kondo S, Yanagisawa N, Takahashi N, Odamaki T, Iwabuchi N, Miyaji K, Iwatsuki K, Togashi H, Enomoto K, Enomoto T (2006) Probiotics in the treatment of Japanese cedar pollinosis: a double-blind placebo-controlled trial. Clin Exp Allergy 36:1425–1435PubMedGoogle Scholar
  125. Yin YN, Yu QF, Fu N, Liu XW, Lu FG (2010) Effects of four Bifidobacteria on obesity in high-fat diet induced rats. World J Gastroenterol 16:3394–3401PubMedGoogle Scholar
  126. Young SL, Simon MA, Baird MA, Tannock GW, Bibiloni R, Spencely K, Lane JM, Fitzharris P, Crane J, Town I, Addo-Yobo E, Murray CS, Woodcock A (2004) Bifidobacterial species differentially affect expression of cell surface markers and cytokines of dendritic cells harvested from cord blood. Clin Diagn Lab Immunol 11:686–690PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Diana Di Gioia
    • 1
  • Irene Aloisio
    • 1
  • Giuseppe Mazzola
    • 1
  • Bruno Biavati
    • 1
  1. 1.Department of Agricultural ScienceUniversity of BolognaBolognaItaly

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