The human neonatal gut microbiome: a brief review

Emily C Gritz, Vineet Bhandari, Emily C Gritz, Vineet Bhandari

Abstract

The field of genomics has expanded into subspecialties such as metagenomics over the course of the last decade and a half. The development of massively parallel sequencing capabilities has allowed for increasingly detailed study of the genome of the human microbiome, the microbial super organ that resides symbiotically within the mucosal tissues and integumentary system of the human host. The gut microbiome, and particularly the study of its origins in neonates, has become subtopics of great interest within the field of genomics. This brief review seeks to summarize recent literature regarding the origins and establishment of the neonatal gut microbiome, beginning in utero, and how it is affected by neonatal nutritional status (breastfed versus formula fed) and gestational age (term versus preterm). We also explore the role of dysbiosis, a perturbation within the fragile ecosystem of the microbiome, and its role in the origin of select pathologic states, specifically, obesity and necrotizing enterocolitis (NEC) in preterm infants. We discuss the evidence supporting enteral pre- and pro-biotic supplementation of commensal organisms such as Bifidobacterium and Lactobacillus in the neonatal period, and their role in the prevention and amelioration of NEC in premature infants. Finally, we review directions to consider for further research to promote human health within this field.

Keywords: dysbiosis; microbiota; newborn; preterm; probiotics.

Figures

Figure 1
Figure 1
Classification of common bacteria found in neonatal intestinal microbiome.

References

    1. Chen K, Pachter L. Bioinformatics for whole-genome shotgun sequencing of microbial communities. PLoS Comput Biol (2005) 1:106–12.10.1371/journal.pcbi.0010024
    1. Fricke WF. The more the merrier? Reduced fecal microbiota diversity in preterm infants treated with antibiotics. J Pediatr (2014) 165:8–1010.1016/j.jpeds.2014.03.022
    1. Berrington JE, Stewart CJ, Cummings SP, Embleton ND. The neonatal bowel microbiome in health and infection. Curr Opin Infect Dis (2014) 27:236–43.10.1097/QCO.0000000000000061
    1. Putignani L, Del Chierico F, Petrucca A, Vernocchi P, Dallapiccola B. The human gut microbiota: a dynamic interplay with the host from birth to senescence settled during childhood. Pediatr Res (2014) 76:2–10.10.1038/pr.2014.49
    1. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med (2014) 6:237ra65.10.1126/scitranslmed.3008599
    1. Adlerberth I, Wold AE. Establishment of the gut microbiota in Western infants. Acta Paediatr (2009) 98:229–38.10.1111/j.1651-2227.2008.01060.x
    1. Sood R, Zehnder JL, Druzin ML, Brown PO. Gene expression patterns in human placenta. Proc Natl Acad Sci U S A (2006) 103:5478–83.10.1073/pnas.0508035103
    1. Stout MJ, Conlon B, Landeau M, Lee I, Bower C, Zhao Q, et al. Identification of intracellular bacteria in the basal plate of the human placenta in term and preterm gestations. Am J Obstet Gynecol (2013) 208:.e1–7.10.1016/j.ajog.2013.01.018
    1. Madan JC, Salari RC, Saxena D, Davidson L, O’Toole GA, Moore JH, et al. Gut microbial colonisation in premature neonates predicts neonatal sepsis. Arch Dis child Fetal Neonatal Ed (2012) 97:F456–62.10.1136/fetalneonatal-2011-301373
    1. Ardissone AN, de la Cruz DM, Davis-Richardson AG, Rechcigl KT, Li N, Drew JC, et al. Meconium microbiome analysis identifies bacteria correlated with premature birth. PLoS One (2014) 9:e90784.10.1371/journal.pone.0090784
    1. Chassard C, de Wouters T, Lacroix C. Probiotics tailored to the infant: a window of opportunity. Curr Opin Biotechnol (2014) 26:141–7.10.1016/j.copbio.2013.12.012
    1. Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature (2012) 489:231–41.10.1038/nature11551
    1. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science (2005) 308:1635–8.10.1126/science.1110591
    1. Madan JC, Farzan SF, Hibberd PL, Karagas MR. Normal neonatal microbiome variation in relation to environmental factors, infection and allergy. Curr Opin Pediatr (2012) 24:753–9.10.1097/MOP.0b013e32835a1ac8
    1. Di Mauro A, Neu J, Riezzo G, Raimondi F, Martinelli D, Francavilla R, et al. Gastrointestinal function development and microbiota. Ital J Pediatr (2013) 39:15.10.1186/1824-7288-39-15
    1. Torrazza RM, Neu J. The altered gut microbiome and necrotizing enterocolitis. Clin Perinatol (2013) 40:93–108.10.1016/j.clp.2012.12.009
    1. Scholtens PA, Oozeer R, Martin R, Amor KB, Knol J. The early settlers: intestinal microbiology in early life. Annu Rev Food Sci Technol (2012) 3:425–47.10.1146/annurev-food-022811-101120
    1. Biasucci G, Rubini M, Riboni S, Morelli L, Bessi E, Retetangos C. Mode of delivery affects the bacterial community in the newborn gut. Early Hum Dev (2010) 86(Suppl 1):13–5.10.1016/j.earlhumdev.2010.01.004
    1. Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C, et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut (2014) 63:559–66.10.1136/gutjnl-2012-303249
    1. Salminen S, Gibson GR, McCartney AL, Isolauri E. Influence of mode of delivery on gut microbiota composition in seven year old children. Gut (2004) 53:1388–910.1136/gut.2004.041640
    1. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol (2007) 5:e177.10.1371/journal.pbio.0050177
    1. Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, et al. Diversity of bifidobacteria within the infant gut microbiota. PLoS One (2012) 7:e36957.10.1371/journal.pone.0036957
    1. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics (2006) 118:511–21.10.1542/peds.2005-2824
    1. Eggesbo M, Moen B, Peddada S, Baird D, Rugtveit J, Midtvedt T, et al. Development of gut microbiota in infants not exposed to medical interventions. APMIS (2011) 119:17–35.10.1111/j.1600-0463.2010.02688.x
    1. Groer MW, Luciano AA, Dishaw LJ, Ashmeade TL, Miller E, Gilbert JA. Development of the preterm infant gut microbiome: a research priority. Microbiome (2014) 2:38.10.1186/2049-2618-2-38
    1. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature (2012) 486:222–7.10.1038/nature11053
    1. Jain N, Walker WA. Diet and host-microbial crosstalk in postnatal intestinal immune homeostasis. Nat Rev Gastroenterol Hepatol (2014) 12(1):14–25.10.1038/nrgastro.2014.153
    1. Di Gioia D, Aloisio I, Mazzola G, Biavati B. Bifidobacteria: their impact on gut microbiota composition and their applications as probiotics in infants. Appl Microbiol Biotechnol (2014) 98:563–77.10.1007/s00253-013-5405-9
    1. Berrington JE, Stewart CJ, Embleton ND, Cummings SP. Gut microbiota in preterm infants: assessment and relevance to health and disease. Arch Dis Child Fetal Neonatal Ed (2013) 98:F286–9010.1136/archdischild-2012-302134
    1. Dai D, Walker WA. Protective nutrients and bacterial colonization in the immature human gut. Adv Pediatr (1999) 46:353–82.
    1. Oozeer R, van Limpt K, Ludwig T, Ben Amor K, Martin R, Wind RD, et al. Intestinal microbiology in early life: specific prebiotics can have similar functionalities as human-milk oligosaccharides. Am J Clin Nutr (2013) 98:561s–71s.10.3945/ajcn.112.038893
    1. Musilova S, Rada V, Vlkova E, Bunesova V. Beneficial effects of human milk oligosaccharides on gut microbiota. Benef Microbes (2014) 5:273–83.10.3920/BM2013.0080
    1. Solís G, de los Reyes-Gavilan CG, Fernández N, Margolles A, Gueimonde M. Establishment and development of lactic acid bacteria and bifidobacteria microbiota in breast-milk and the infant gut. Anaerobe (2010) 16:307–10.10.1016/j.anaerobe.2010.02.004
    1. Civardi E, Garofoli F, Tzialla C, Paolillo P, Bollani L, Stronati M. Microorganisms in human milk: lights and shadows. J Matern Fetal Neonatal Med (2013) 26(Suppl 2):30–4.10.3109/14767058.2013.829693
    1. Latuga MS, Stuebe A, Seed PC. A review of the source and function of microbiota in breast milk. Semin Reprod Med (2014) 32:68–73.10.1055/s-0033-1361824
    1. Donnet-Hughes A, Perez PF, Dore J, Leclerc M, Levenez F, Benyacoub J, et al. Potential role of the intestinal microbiota of the mother in neonatal immune education. Proc Nutr Soc (2010) 69:407–15.10.1017/S0029665110001898
    1. Power SE, O’Toole PW, Stanton C, Ross RP, Fitzgerald GF. Intestinal microbiota, diet and health. Br J Nutr (2014) 111:387–40210.1017/S0007114513002560
    1. Gomez-Llorente C, Plaza-Diaz J, Aguilera M, Munoz-Quezada S, Bermudez-Brito M, Peso-Echarri P, et al. Three main factors define changes in fecal microbiota associated with feeding modality in infants. J Pediatr Gastroenterol Nutr (2013) 57:461–6.10.1097/MPG.0b013e31829d519a
    1. Jost T, Lacroix C, Braegger CP, Chassard C. New insights in gut microbiota establishment in healthy breast fed neonates. PLoS One (2012) 7:e44595.10.1371/journal.pone.0044595
    1. Piacentini G, Peroni D, Bessi E, Morelli L. Molecular characterization of intestinal microbiota in infants fed with soymilk. J Pediatr Gastroenterol Nutr (2010) 51:71–6.10.1097/MPG.0b013e3181dc8b02
    1. Guaraldi F, Salvatori G. Effect of breast and formula feeding on gut microbiota shaping in newborns. Front Cell Infect Microbiol (2012) 2:94.10.3389/fcimb.2012.00094
    1. Mackie RI, Sghir A, Gaskins HR. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr (1999) 69:1035s–45s.
    1. Hascoet JM, Hubert C, Rochat F, Legagneur H, Gaga S, Emady-Azar S, et al. Effect of formula composition on the development of infant gut microbiota. J Pediatr Gastroenterol Nutr (2011) 52:756–62.10.1097/MPG.0b013e3182105850
    1. Manco M. Gut microbiota and developmental programming of the brain: from evidence in behavioral endophenotypes to novel perspective in obesity. Front Cell Infect Microbiol (2012) 2:109.10.3389/fcimb.2012.00109
    1. Hochberg Z, Feil R, Constancia M, Fraga M, Junien C, Carel JC, et al. Child health, developmental plasticity, and epigenetic programming. Endocr Rev (2011) 32:159–224.10.1210/er.2009-0039
    1. Kalliomaki M, Collado MC, Salminen S, Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr (2008) 87:534–8.
    1. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A (2005) 102:11070–5.10.1073/pnas.0504978102
    1. Mischke M, Plosch T. More than just a gut instinct-the potential interplay between a baby’s nutrition, its gut microbiome, and the epigenome. Am J Physiol (2013) 304:R1065–9.10.1152/ajpregu.00551.2012
    1. Luoto R, Kalliomaki M, Laitinen K, Delzenne NM, Cani PD, Salminen S, et al. Initial dietary and microbiological environments deviate in normal-weight compared to overweight children at 10 years of age. J Pediatr Gastroenterol Nutr (2011) 52:90–5.10.1097/MPG.0b013e3181f3457f
    1. Gupta RW, Tran L, Norori J, Ferris MJ, Eren AM, Taylor CM, et al. Histamine-2 receptor blockers alter the fecal microbiota in premature infants. J Pediatr Gastroenterol Nutr (2013) 56:397–400.10.1097/MPG.0b013e318282a8c2
    1. Stewart CJ, Marrs EC, Nelson A, Lanyon C, Perry JD, Embleton ND, et al. Development of the preterm gut microbiome in twins at risk of necrotising enterocolitis and sepsis. PLoS One (2013) 8:e73465.10.1371/journal.pone.0073465
    1. Arboleya S, Binetti A, Salazar N, Fernandez N, Solis G, Hernandez-Barranco A, et al. Establishment and development of intestinal microbiota in preterm neonates. FEMS Microbiol Ecol (2012) 79:763–72.10.1111/j.1574-6941.2011.01261.x
    1. Butel MJ, Suau A, Campeotto F, Magne F, Aires J, Ferraris L, et al. Conditions of bifidobacterial colonization in preterm infants: a prospective analysis. J Pediatr Gastroenterol Nutr (2007) 44:577–82.10.1097/MPG.0b013e3180406b20
    1. La Rosa PS, Warner BB, Zhou Y, Weinstock GM, Sodergren E, Hall-Moore CM, et al. Patterned progression of bacterial populations in the premature infant gut. Proc Natl Acad Sci U S A (2014) 111:12522–7.10.1073/pnas.1409497111
    1. Panigrahi P. Probiotics and prebiotics in neonatal necrotizing enterocolitis: new opportunities for translational research. Pathophysiology (2014) 21:35–46.10.1016/j.pathophys.2013.11.016
    1. Fanaroff AA, Korones SB, Wright LL, Verter J, Poland RL, Bauer CR, et al. Incidence, presenting features, risk factors and significance of late onset septicemia in very low birth weight infants. The National Institute of Child Health and Human Development Neonatal Research Network. Pediatr Infect Dis J (1998) 17:593–810.1097/00006454-199807000-00004
    1. Mai V, Torrazza RM, Ukhanova M, Wang X, Sun Y, Li N, et al. Distortions in development of intestinal microbiota associated with late onset sepsis in preterm infants. PLoS One (2013) 8:e52876.10.1371/journal.pone.0052876
    1. Neu J. The microbiome and its impact on disease in the preterm patient. Curr Pediatr Rep (2013) 1:215–2110.1007/s40124-013-0031-7
    1. Carlisle EM, Morowitz MJ. The intestinal microbiome and necrotizing enterocolitis. Curr Opin Pediatr (2013) 25:382–7.10.1097/MOP.0b013e3283600e91
    1. Grishin A, Papillon S, Bell B, Wang J, Ford HR. The role of the intestinal microbiota in the pathogenesis of necrotizing enterocolitis. Semin Pediatr Surg (2013) 22:69–75.10.1053/j.sempedsurg.2013.01.002
    1. Mai V, Young CM, Ukhanova M, Wang X, Sun Y, Casella G, et al. Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS One (2011) 6:e20647.10.1371/journal.pone.0020647
    1. Morrow AL, Lagomarcino AJ, Schibler KR, Taft DH, Yu Z, Wang B, et al. Early microbial and metabolomic signatures predict later onset of necrotizing enterocolitis in preterm infants. Microbiome (2013) 1:13.10.1186/2049-2618-1-13
    1. Smith B, Bode S, Skov TH, Mirsepasi H, Greisen G, Krogfelt KA. Investigation of the early intestinal microflora in premature infants with/without necrotizing enterocolitis using two different methods. Pediatr Res (2012) 71:115–20.10.1038/pr.2011.1
    1. Patel RM, Denning PW. Therapeutic use of prebiotics, probiotics, and postbiotics to prevent necrotizing enterocolitis: what is the current evidence? Clin Perinatol (2013) 40:11–25.10.1016/j.clp.2012.12.002
    1. Indrio F, Riezzo G, Raimondi F, Bisceglia M, Cavallo L, Francavilla R. Effects of probiotic and prebiotic on gastrointestinal motility in newborns. J Physiol Pharmacol (2009) 60(Suppl 6):27–31.
    1. Indrio F, Riezzo G, Raimondi F, Francavilla R, Montagna O, Valenzano ML, et al. Prebiotics improve gastric motility and gastric electrical activity in preterm newborns. J Pediatr Gastroenterol Nutr (2009) 49:258–61.10.1097/MPG.0b013e3181926aec
    1. Mastromarino P, Capobianco D, Campagna G, Laforgia N, Drimaco P, Dileone A, et al. Correlation between lactoferrin and beneficial microbiota in breast milk and infant’s feces. Biometals (2014) 27:1077–86.10.1007/s10534-014-9762-3
    1. Ofek Shlomai N, Deshpande G, Rao S, Patole S. Probiotics for preterm neonates: what will it take to change clinical practice? Neonatology (2014) 105:64–7010.1159/000354891
    1. Mihatsch WA, Braegger CP, Decsi T, Kolacek S, Lanzinger H, Mayer B, et al. Critical systematic review of the level of evidence for routine use of probiotics for reduction of mortality and prevention of necrotizing enterocolitis and sepsis in preterm infants. Clin Nutr (2012) 31:6–15.10.1016/j.clnu.2011.09.004
    1. Wang Q, Dong J, Zhu Y. Probiotic supplement reduces risk of necrotizing enterocolitis and mortality in preterm very low-birth-weight infants: an updated meta-analysis of 20 randomized, controlled trials. J Pediatr Surg (2012) 47:241–8.10.1016/j.jpedsurg.2011.09.064
    1. Deshpande G, Rao S, Patole S, Bulsara M. Updated meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Pediatrics (2010) 125:921–30.10.1542/peds.2009-1301
    1. AlFaleh K, Anabrees J. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst Rev (2014) 4:CD005496.10.1002/14651858.CD005496.pub4
    1. Janvier A, Malo J, Barrington KJ. Cohort study of probiotics in a North American neonatal intensive care unit. J Pediatr (2014) 164:980–5.10.1016/j.jpeds.2013.11.025
    1. Deshpande GC, Rao SC, Keil AD, Patole SK. Evidence-based guidelines for use of probiotics in preterm neonates. BMC Med (2011) 9:92.10.1186/1741-7015-9-92
    1. Oncel MY, Sari FN, Arayici S, Guzoglu N, Erdeve O, Uras N, et al. Lactobacillus reuteri for the prevention of necrotising enterocolitis in very low birthweight infants: a randomised controlled trial. Arch Dis Child Fetal Neonatal Ed (2014) 99:F110–5.10.1136/archdischild-2013-304745
    1. Jacobs SE, Tobin JM, Opie GF, Donath S, Tabrizi SN, Pirotta M, et al. Probiotic effects on late-onset sepsis in very preterm infants: a randomized controlled trial. Pediatrics (2013) 132:1055–62.10.1542/peds.2013-1339
    1. Serce O, Benzer D, Gursoy T, Karatekin G, Ovali F. Efficacy of Saccharomyces boulardii on necrotizing enterocolitis or sepsis in very low birth weight infants: a randomised controlled trial. Early Hum Dev (2013) 89:1033–6.10.1016/j.earlhumdev.2013.08.013
    1. Fernandez-Carrocera LA, Solis-Herrera A, Cabanillas-Ayon M, Gallardo-Sarmiento RB, Garcia-Perez CS, Montano-Rodriguez R, et al. Double-blind, randomised clinical assay to evaluate the efficacy of probiotics in preterm newborns weighing less than 1500 g in the prevention of necrotising enterocolitis. Arch Dis Child Fetal Neonatal Ed (2013) 98:F5–9.10.1136/archdischild-2011-300435
    1. Rojas MA, Lozano JM, Rojas MX, Rodriguez VA, Rondon MA, Bastidas JA, et al. Prophylactic probiotics to prevent death and nosocomial infection in preterm infants. Pediatrics (2012) 130:e1113–2010.1542/peds.2011-3584
    1. Al-Hosni M, Duenas M, Hawk M, Stewart LA, Borghese RA, Cahoon M, et al. Probiotics-supplemented feeding in extremely low-birth-weight infants. J Perinatol (2012) 32:253–9.10.1038/jp.2011.51
    1. Braga TD, da Silva GA, de Lira PI, de Carvalho Lima M. 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 (2011) 93:81–6.10.3945/ajcn.2010.29799
    1. Samanta M, Sarkar M, Ghosh P, Ghosh J, Sinha M, Chatterjee S. Prophylactic probiotics for prevention of necrotizing enterocolitis in very low birth weight newborns. J Trop Pediatr (2009) 55:128–31.10.1093/tropej/fmn091
    1. Lin HC, Hsu CH, Chen HL, Chung MY, Hsu JF, Lien RI, et al. Oral probiotics prevent necrotizing enterocolitis in very low birth weight preterm infants: a multicenter, randomized, controlled trial. Pediatrics (2008) 122:693–700.10.1542/peds.2007-3007
    1. Lin HC, Su BH, Chen AC, Lin TW, Tsai CH, Yeh TF, et al. Oral probiotics reduce the incidence and severity of necrotizing enterocolitis in very low birth weight infants. Pediatrics (2005) 115:1–410.1542/peds.2004-1463
    1. Bin-Nun A, Bromiker R, Wilschanski M, Kaplan M, Rudensky B, Caplan M, et al. Oral probiotics prevent necrotizing enterocolitis in very low birth weight neonates. J Pediatr (2005) 147:192–6.10.1016/j.jpeds.2005.03.054
    1. de Champs C, Maroncle N, Balestrino D, Rich C, Forestier C. Persistence of colonization of intestinal mucosa by a probiotic strain, Lactobacillus casei subsp. rhamnosus Lcr35, after oral consumption. J Clin Microbiol (2003) 41:1270–3.10.1128/JCM.41.3.1270-1273.2003
    1. Costa GN, Marcelino-Guimaraes FC, Vilas-Boas GT, Matsuo T, Miglioranza LH. Potential fate of ingested Lactobacillus plantarum and its occurrence in human feces. Appl Environ Microbiol (2014) 80:1013–9.10.1128/AEM.02588-13
    1. Parks DH, Beiko RG. Identifying biologically relevant differences between metagenomic communities. Bioinformatics (2010) 26:715–21.10.1093/bioinformatics/btq041
    1. Panigrahi P, Parida S, Pradhan L, Mohapatra S, Misra P, Johnson J, et al. Long-term colonization of a Lactobacillus plantarum synbiotic preparation in the neonatal gut. J Pediatr Gastroenterol Nutr (2008) 47:45–53.10.1097/MPG.0b013e31815a5f2c
    1. Tobin JM, Garland SM, Jacobs SE, Pirotta M, Tabrizi SN. Rapid assay to assess colonization patterns following in-vivo probiotic ingestion. BMC Res Notes (2013) 6:252.10.1186/1756-0500-6-252
    1. Kitajima H, Sumida Y, Tanaka R, Yuki N, Takayama H, Fujimura M. Early administration of Bifidobacterium breve to preterm neonates: randomised control trial. Arch Dis Child (1997) 76:F101–7.10.1136/fn.76.2.F101
    1. Reuman PD, Duckworth DH, Smith KL, Kagan R, Bucciarelli RL, Ayoub EM. Lack of effect of Lactobacillus on gastrointestinal bacterial colonization in premature infants. Pediatr Infect Dis (1986) 5:663–8.10.1097/00006454-198611000-00013
    1. Agarwal R, Sharma N, Chaudhry R, Deorari A, Paul VK, Gewolb IH, et al. Effects of oral Lactobacillus GG on enteric microflora in low-birth-weight neonates. J Pediatr Gastroenterol Nutr (2003) 36:397–402.10.1097/00005176-200303000-00019
    1. Bennet R, Nord CE, Zetterstrom R. Transient colonization of the gut of newborn infants by orally administered bifidobacteria and lactobacilli. Acta Paediatrica (1992) 81:784–7.10.1111/j.1651-2227.1992.tb12103.x
    1. Collins MD, Gibson GR. Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut. Am J Clin Nutr (1999) 69:1052s–7s.
    1. Martin R, Nauta AJ, Ben Amor K, Knippels LM, Knol J, Garssen J. Early life: gut microbiota and immune development in infancy. Benef Microbes (2010) 1:367–82.10.3920/BM2010.0027
    1. Garcia-Lafuente A, Antolin M, Guarner F, Crespo E, Malagelada JR. Modulation of colonic barrier function by the composition of the commensal flora in the rat. Gut (2001) 48:503–7.10.1136/gut.48.4.503
    1. Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, et al. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology (2001) 121:580–91.10.1053/gast.2001.27224
    1. Parassol N, Freitas M, Thoreux K, Dalmasso G, Bourdet-Sicard R, Rampal P. Lactobacillus casei DN-114 001 inhibits the increase in paracellular permeability of enteropathogenic Escherichia coli-infected T84 cells. Res Microbiol (2005) 156:256–62.10.1016/j.resmic.2004.09.013
    1. Karczewski J, Troost FJ, Konings I, Dekker J, Kleerebezem M, Brummer RJ, et al. Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am J Physiol Gastrointest Liver Physiol (2010) 298:G851–9.10.1152/ajpgi.00327.2009
    1. Smelt MJ, de Haan BJ, Bron PA, van Swam I, Meijerink M, Wells JM, et al. L. plantarum, L. salivarius, and L. lactis attenuate Th2 responses and increase Treg frequencies in healthy mice in a strain dependent manner. PLoS One (2012) 7:e47244.10.1371/journal.pone.0047244
    1. Hempel S, Newberry S, Ruelaz A, Wang Z, Miles JN, Suttorp MJ, et al. Safety of probiotics used to reduce risk and prevent or treat disease. Evid Rep Technol Assess (2011) 1–645.
    1. Zbinden A, Zbinden R, Berger C, Arlettaz R. Case series of Bifidobacterium longum bacteremia in three preterm infants on probiotic therapy. Neonatology (2015) 107:56–9.10.1159/000367985
    1. Abrahamsson TR, Rautava S, Moore AM, Neu J, Sherman PM. The time for a confirmative necrotizing enterocolitis probiotics prevention trial in the extremely low birth weight infant in North America is now! J Pediatr (2014) 165:389–9410.1016/j.jpeds.2014.05.012
    1. Chan L-N, Soltani H, Hazlet TK. Probiotics for neonates: safety for prime time questioned without regulatory changes. J Pediatr (2015) 166(2):502.10.1016/j.jpeds.2014.10.041

Source: PubMed

3
Suscribir