Skip to main content

Advertisement

SpringerLink
Log in

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

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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 91:39–43

    CAS  PubMed  Google Scholar 

  • 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 96:1561–1576

    CAS  PubMed  Google Scholar 

  • 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 34:45–51

    CAS  PubMed  Google Scholar 

  • 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 10:116

    PubMed Central  PubMed  Google Scholar 

  • 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 149:28–36

    CAS  PubMed  Google Scholar 

  • 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 101:15718–15723

    PubMed Central  PubMed  Google Scholar 

  • Barclay AR, Stenson B, Simpson JH, Weaver LT, Wilson DC (2007) Probiotics for necrotizing enterocolitis: a systematic review. J Pediatr Gastroenterol Nutr 45:569–576

    PubMed  Google Scholar 

  • 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 2:215–225

    Google Scholar 

  • 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 23:1132–1139

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 17:478–482

    PubMed  Google Scholar 

  • 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 86:13–15

    PubMed  Google Scholar 

  • Biavati B, Castagnoli P, Crociani F, Trovatelli LD (1984) Species of the Bifidobacterium in the feces of infants. Microbiologica 7:341–345

    CAS  PubMed  Google Scholar 

  • Biavati B, Vescovo M, Torriani S, Bottazzi V (2000) Bifidobacteria: history, ecology, physiology and applications. Ann Microbiol 50:117–131

    Google Scholar 

  • 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 328:322–323

    PubMed  Google Scholar 

  • Blaut M, Bischoff SC (2010) Probiotics and obesity. Ann Nutr Metab 57:20–23

    CAS  PubMed  Google Scholar 

  • Boyle RJ, Tang ML (2006) The role of probiotics in the management of allergic diseases. Clin Exp Allergy 36:568–576

    CAS  PubMed  Google Scholar 

  • 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 93:81–86

    CAS  PubMed  Google Scholar 

  • Cabana MD, McKean M, Wong AR, Chao C, Caughey AB (2007) Examining the hygiene hypothesis: the trial of infant probiotic supplementation. Paediatr Perinat Epidemiol 21:23–28

    PubMed  Google Scholar 

  • 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 50:2374–2383

    CAS  PubMed  Google Scholar 

  • 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 58:1091–1103

    CAS  PubMed Central  PubMed  Google Scholar 

  • Claud EC, Walker WA (2001) Hypothesis: inappropriate colonization of the premature intestine can cause neonatal necrotizing enterocolitis. FASEB J 15:1398–1403

    CAS  PubMed  Google Scholar 

  • Collado MC, Calabuig M, Sanz Y (2007) Differences between the faecal microbiota of coeliac children and healthy controls. Curr Issues Intest Microbiol 8:9–14

    CAS  PubMed  Google Scholar 

  • 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 8:232

    PubMed Central  PubMed  Google Scholar 

  • Collins SM, Bercik P (2009) The relationship between intestinal microbiota and the central nervous system in normal gastrointestinal function and disease. Gastroenterology 136:2003–2014

    PubMed  Google Scholar 

  • 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 131–146

    Google Scholar 

  • 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 2012

    Google Scholar 

  • Cryan JF, O'Mahony SM (2011) The microbiome–gut–brain axis: from bowel to behavior. Neurogastroenterol Motil 23:187–192

    CAS  PubMed  Google Scholar 

  • 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 1762:80–93

    PubMed  Google Scholar 

  • de Weerth C, Fuentes S, Puylaert P, de Vos M (2013) Intestinal microbiota of infants with colic: development and specific signatures. Pediatrics 131:e550–e558

    PubMed  Google Scholar 

  • 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 43:164–174

    PubMed  Google Scholar 

  • 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 369:1614–1620

    PubMed  Google Scholar 

  • Deshpande G, Rao S, Patole S, Bulsara M (2010) Updated meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Pediatrics 125:921–930

    PubMed  Google Scholar 

  • Deshpande GC, Rao SC, Keil AD, Patole SK (2011) Evidence-based guidelines for use of probiotics in preterm neonates. BMC Med 9:92

    PubMed Central  PubMed  Google Scholar 

  • 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 42:130–132

    Google Scholar 

  • Dotan I, Rachmilewitz D (2005) Probiotics in inflammatory bowel disease: possible mechanisms of action. Curr Opin Gastroenterol 21:426–430

    PubMed  Google Scholar 

  • Dubois PC, van Heel DA (2008) Translational mini-review series on the immunogenetics of gut disease: immunogenetics of coeliac disease. Clin Exp Immunol 153:162–173

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 pp

    Google Scholar 

  • 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 51:77–84

    PubMed  Google Scholar 

  • 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 157:1385–1392

    CAS  PubMed  Google Scholar 

  • Fasano A, Catassi C (2005) Coeliac disease in children. Best Pract Res Clin Gastroenterol 19:467–478

    PubMed  Google Scholar 

  • Favier CF, Vaughan EE, De Vos WM, Akkermans AD (2002) Molecular monitoring of succession of bacterial communities in human neonates. Appl Environ Microbiol 68:219–226

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 37:498–505

    CAS  PubMed  Google Scholar 

  • Ferrieri P, Wallen L (2012) Neonatal bacterial sepsis. In: Gleason CA, Devaskar SU (eds) Avery's disease of the newborn. Elsevier, Amsterdam, pp 538–550

    Google Scholar 

  • Forsythe P, Sudo N, Dinan T, Taylor V, Bienenstock J (2010) Mood and gut feelings. Brain Behav Immun 24:9–16

    PubMed  Google Scholar 

  • 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 10:253

    PubMed Central  PubMed  Google Scholar 

  • Green PH, Cellier C (2007) Celiac disease. N Engl J Med 357:1731–1743

    CAS  PubMed  Google Scholar 

  • 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 13:3985–3989

    PubMed  Google Scholar 

  • Hammerman C, Bin-Nun A, Kaplan M (2006) Safety of probiotics: comparison of two popular strains. BMJ 333:1006–1008

    PubMed  Google Scholar 

  • 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:e34043

    CAS  PubMed Central  PubMed  Google Scholar 

  • Harder T, Bergmann R, Kallischnigg G, Plagemann A (2005) Duration of breastfeeding and risk of overweight: a meta-analysis. Am J Epidemiol 162:397–403

    PubMed  Google Scholar 

  • Hunter CJ, Upperman JS, Ford HR, Camerini V (2008) Understanding the susceptibility of the premature infant to necrotizing enterocolitis (NEC). Pediatr Res 63:117–123

    PubMed  Google Scholar 

  • Indrio F, Neu J (2011) The intestinal microbiome of infants and the use of probiotics. Curr Opin Pediatr 23:145–150

    PubMed Central  PubMed  Google Scholar 

  • Isolauri E (2004) Dietary modification of atopic disease: use of probiotics in the prevention ofatopic dermatitis. Curr Allergy Asthma Rep 4:270–275

    PubMed  Google Scholar 

  • 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–S96

    PubMed  Google Scholar 

  • Isolauri E, Arvola T, Sutas Y, Moilanen E, Salminen S (2000) Probiotics in the management of atopic eczema. Clin Exp Allergy 30:1604–1610

    CAS  PubMed  Google Scholar 

  • Ivarsson A, Hernell O, Stenlund H, Persson LA (2002) Breast-feeding protects against celiac disease. Am J Clin Nutr 75:914–921

    CAS  PubMed  Google Scholar 

  • 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 97–118

    Google Scholar 

  • 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 107:129–134

    CAS  PubMed  Google Scholar 

  • Kalliomaki M, Collado MC, Salminen S, Isolauri E (2008) Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr 87:534–538

    CAS  PubMed  Google Scholar 

  • Kaur IP, Chopra K, Saini A (2002) Probiotics: potential pharmaceutical applications. Eur J Pharm Sci 15:1–9

    CAS  PubMed  Google Scholar 

  • 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 1297:940–949

    Google Scholar 

  • 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 75:2668–2676

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 108:4578–4585

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 123:335–341

    PubMed  Google Scholar 

  • 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 165:418–424

    PubMed  Google Scholar 

  • 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 46:509–515

    PubMed  Google Scholar 

  • 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 122:693–700

    PubMed  Google Scholar 

  • 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 152:552–558

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 42:913–918

    CAS  PubMed  Google Scholar 

  • Lowenthal A, Livni G, Amir J, Samra Z, Ashkenazi S (2006) Secondary bacteremia after rotavirus gastroenteritis in infancy. Pediatrics 117:224–226

    PubMed  Google Scholar 

  • 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 49:821–830

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 58:563–571

    CAS  PubMed  Google Scholar 

  • 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:e20647

    CAS  PubMed Central  PubMed  Google Scholar 

  • Meresse B, Ripoche J, Heyman M, Cerf-Bensussan N (2009) Celiac disease: from oral tolerance to intestinal inflammation, autoimmunity and lymphomagenesis. Mucosal Immunol 2:8–23

    CAS  PubMed  Google Scholar 

  • 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 26:1–9

    Google Scholar 

  • 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 36:817–825

    CAS  Google Scholar 

  • 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):1460–1467

    CAS  Google Scholar 

  • 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 44:4025–4031

    PubMed Central  PubMed  Google Scholar 

  • Mulder CJ, Bartelsman JF (2005) Case-finding in coeliac disease should be intensified. Best Pract Res Clin Gastroenterol 19:479–486

    PubMed  Google Scholar 

  • 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 77:8775–8783

    PubMed  Google Scholar 

  • 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 56:1669–1674

    CAS  PubMed  Google Scholar 

  • Neu J, Walker WA (2011) Necrotizing enterocolitis. N Engl J Med 364:255–264

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 108:144–145

    CAS  PubMed  Google Scholar 

  • 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 115:1367–1377

    PubMed  Google Scholar 

  • Özdemir Ö (2009) Gut flora development in infancy and its effect on immune system. Çocuk Enf Derg J Pediatr Inf 3:202–203

    Google Scholar 

  • Özdemir Ö (2010) Variuos effects of different probiotic starins in allergic disorders: an update from laboratory and clinical data. Clin Exp Immunol 160:295–304

    PubMed Central  PubMed  Google Scholar 

  • 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:e30791

    PubMed Central  PubMed  Google Scholar 

  • Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5:e177

    PubMed Central  PubMed  Google Scholar 

  • 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 56:661–667

    PubMed  Google Scholar 

  • Puopolo KM, Madoff LC, Eichenwald EC (2005) Early-onset group B streptococcal disease in the era of maternal screening. Pediatrics 115:1240–1246

    PubMed  Google Scholar 

  • Rhee SH, Pothoulakis C, Mayer EA (2009) Principles and clinical implications of the brain–gut–enteric microbiota axis. Nat Rev Gastroenterol Hepatol 6:306–314

    CAS  PubMed  Google Scholar 

  • 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 8:1–27

    PubMed  Google Scholar 

  • Saavedra JM, Tschernia A (2002) Human studies with probiotics and prebiotics: clinical implications. Br J Nutr 87:241–246

    Google Scholar 

  • 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 1:164–185

    PubMed  Google Scholar 

  • 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 51:562–568

    CAS  PubMed  Google Scholar 

  • Sartor BR (2004) Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 126:1620–1633

    PubMed  Google Scholar 

  • 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 119:124–130

    Google Scholar 

  • Savino F, Cordisco L, Tarasco V, Calabrese R, Palumeri E, Matteuzzi D (2009) Molecular identification of coliform bacteria from colicky breastfed infants. Acta Paediatr 98:1582–1588

    CAS  PubMed  Google Scholar 

  • 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 126:526–533

    Google Scholar 

  • 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 11:157

    Google Scholar 

  • 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 18:190–195

    PubMed  Google Scholar 

  • 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 27:428–433

    CAS  PubMed  Google Scholar 

  • 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 39:571–578

    CAS  PubMed  Google Scholar 

  • 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 16:307–310

    PubMed  Google Scholar 

  • 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 441–443

    Google Scholar 

  • 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 558:263–275

    CAS  PubMed  Google Scholar 

  • 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 156:562–567

    CAS  PubMed  Google Scholar 

  • 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:e15

    PubMed Central  PubMed  Google Scholar 

  • 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 149:367–372

    Google Scholar 

  • Tennyson CA, Friedman G (2008) Microecology, obesity, and probiotics. Curr Opin Endocrinol Diabetes Obes 15:422–427

    PubMed  Google Scholar 

  • Tham CSC, Peh KK, Bhat R, Liong MT (2011) Probiotic properties of bifidobacteria and lactobacilli isolated from local dairy products. Ann Microbiol 62:1079–1087

    Google Scholar 

  • 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:e36957

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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. 71:546–551

  • van Heel DA, West J (2006) Recent advances in coeliac disease. Gut 55:1037–1046

    PubMed  Google Scholar 

  • Vandenplas Y, De Hert SG (2011) Randomised clinical trial: the synbiotic food supplement probiotical vs. placebo for acute gastroenteritis in children. Aliment Pharmacol Ther 34:862–867

    CAS  PubMed  Google Scholar 

  • Verdu EF (2009) Probiotics effects on gastrointestinal function: beyond the gut? Neurogastroenterol Motil 21:477–480

    CAS  PubMed  Google Scholar 

  • 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 60:494–500

    CAS  PubMed  Google Scholar 

  • 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 18:751–759

    Google Scholar 

  • 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 44:252–257

    CAS  PubMed  Google Scholar 

  • Wassenaar TM, Klein G (2008) Safety aspects and implications of regulation of probiotic bacteria in food and food supplements. J Food Protect 71:1734–1741

    Google Scholar 

  • 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 115:5–9

    PubMed  Google Scholar 

  • 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 15:401–407

    Google Scholar 

  • 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 86:2452–2461

    CAS  PubMed  Google Scholar 

  • 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 36:1425–1435

    CAS  PubMed  Google Scholar 

  • 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 16:3394–3401

    CAS  PubMed  Google Scholar 

  • 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 11:686–690

    PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Agricultural Science, University of Bologna, viale Fanin 44, 40127, Bologna, Italy

    Diana Di Gioia, Irene Aloisio, Giuseppe Mazzola & Bruno Biavati

Authors
  1. Diana Di Gioia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Irene Aloisio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giuseppe Mazzola
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bruno Biavati
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Diana Di Gioia.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Di Gioia, D., Aloisio, I., Mazzola, G. et al. Bifidobacteria: their impact on gut microbiota composition and their applications as probiotics in infants. Appl Microbiol Biotechnol 98, 563–577 (2014). https://doi.org/10.1007/s00253-013-5405-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-013-5405-9

Keywords

Search

Navigation