Early Microbe Contact in Defining Child Metabolic Health and Obesity Risk

  • Erika Isolauri
  • Samuli Rautava
  • Maria Carmen Collado
  • Seppo Salminen
Chapter
Part of the Physiology in Health and Disease book series (PIHD)

Abstract

The background to the increase in nutrition-related chronic conditions such as overweight and obesity is more complex than is generally anticipated. Recent scientific data suggest that metabolic disturbances can arise from aberrant gut microbiota, with or without alterations in dietary composition. In particular, early-life dysbiosis induces lasting alterations in the immune and metabolic phenotype. The compositional development of the indigenous intestinal microbiota, co-evolving with the key regulatory systems of the body, is highly sensitive to the mode of delivery and early feeding, antibiotic use and maternal immune and nutritional state during pregnancy. All these elements interact with the microbiota. Consequently, considerable research interest is currently focusing on the microbial inoculum provided by the feto-maternal interface, along with microbe contact during delivery and through lactation. The early colonisers provide a framework conceptualising the way early-life (pre-, peri- and postnatal) exposures are linked to disease processes and even the pathogenesis of disease. To quote Hippocrates: “All disease begins in the gut”. This holds especially true for nutrition-related diseases, polarised in the detrimental consequences of undernutrition or overnutrition. The impact of the gut microbiota culminates in early infancy, when the immune responsiveness and metabolic phenotype are consolidated. The gut microbiota contributes to nutrition, immunity and metabolism by processing nutrients and regulating their access to and storage in the body, producing chemicals of hormonal nature and controlling the secretion of pro-inflammatory mediators locally and systemically. Another quotation from Hippocrates states that “Natural forces within us are the true healers of disease”. Recent experimental and clinical studies have attracted scientific interest in reprogramming deviations in the gut microbiota. Promoting the predominance of specific non-pathogenic microbes and thereby modifying the intestinal milieu may be taken as an alternative means of attaining prophylactic or therapeutic effects in metabolic and inflammatory conditions. As the critical time window for these to exert their programming effects falls around birth, early initiation of preventive measures is of the essence; influencing the feto-maternal microbe contact may promote the health of the next generation.

Keywords

Allergic disease Atopy Child Growth Gut microbiota Microbiome Mode of delivery Obesity Overweight Pregnancy Probiotics 

References

  1. 1.
    Liem ET, van Buuren S, Sauer PJJ, Jaspers M, Stolk RP, Reijneveld SA (2013) Growth during infancy and childhood, and adiposity at age 16 years: ages 2 to 7 are pivotal. J Pediatr 162:287–292CrossRefPubMedGoogle Scholar
  2. 2.
    Ovesen P, Jensen DM, Damm P, Rasmussen, Kesmodel US (2014) Maternal and neonatal outcomes in pregnancies complicated by gestational diabetes. A nation-wide study. J Matern Fetal Neonatal Med. doi: 10.3109/14767058.2014.966677
  3. 3.
    Monasta L, Batty GD, Cattaneo A, Lutje V, Ronfani L, Van Lenthe FJ et al (2010) Early life determinants of overweight and obesity. Obes Rev 11:695–708CrossRefPubMedGoogle Scholar
  4. 4.
    Suez J, Korem T, Zeevi D, Zilberman-Schapira G, Thaiss CA, Maza O et al (2014) Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature 514:181–186PubMedGoogle Scholar
  5. 5.
    Hall WL, Millward DJ, Long SJ, Morgan LM (2003) Casein and whey exert different effects on plasma amino acid profiles, gastrointestinal hormone secretion and appetite. Br J Nutr 89:239–248CrossRefPubMedGoogle Scholar
  6. 6.
    Hoffmann I (2003) Transcending reductionism in nutrition research. Am J Clin Nutr 78:514S–516SPubMedGoogle Scholar
  7. 7.
    Isolauri E, Kalliomäki M, Laitinen K, Salminen S (2008) Modulation of the maturing gut barrier and microbiota: a novel target in allergic disease. Curr Pharm Des 14:1368–1375CrossRefPubMedGoogle Scholar
  8. 8.
    Luoto R, Collado MC, Salminen S, Isolauri E (2013) Reshaping the gut microbiota at an early age-functional impact on obesity risk? Ann Nutr Metab 63(Suppl 2):17–26CrossRefPubMedGoogle Scholar
  9. 9.
    Greer RL, Morgum A, Shulzhenko N (2013) Bridging immunity and lipid metabolism by gut microbiota. J Allergy Clin Immunol 132:253–262CrossRefPubMedGoogle Scholar
  10. 10.
    Kalliomäki 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
  11. 11.
    Le Chatelier E, Nielsen T, Qin J, Prifiti E, Hildebrand F, Falony G et al (2013) Richness of human gut microbiome correlates with metabolic markers. Nature 500:541–546CrossRefPubMedGoogle Scholar
  12. 12.
    Kasubuchi M, Hasegawa S, Hiramatsu T, Ichimura A, Kimura I (2015) Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation. Nutrients 7:2839–2849CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Canfora EE, Jocken JW, Blaak EE (2015) Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol. doi: 10.1038/nrendo.2015.128
  14. 14.
    Barker DJ (2007) The origins of the developmental origins theory. J Intern Med 261:412–417CrossRefPubMedGoogle Scholar
  15. 15.
    Ravelli AC, van Der Meulen JH, Osmond C, Barker DJ, Bleker OP (1999) Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr 70:811–816PubMedGoogle Scholar
  16. 16.
    Ong KK, Ahmed ML, Emmett PM, Preece MA, Dunger DB (2000) Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ 320:967–971CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Gluckman PD, Hanson MA, Cooper C, Thornburg KL (2008) Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359:61–73CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Fall CH (2011) Evidence for intra-uterine programming of adiposity in later life. Ann Hum Biol 38:410–428CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A et al (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101:15718–15723CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D et al (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56:1761–1772CrossRefPubMedGoogle Scholar
  22. 22.
    Clarke G, Stilling RM, Kennedy PJ, Stanton C, Cryan JF, Dinan TG (2014) Gut microbiota: the neglected endocrine organ. Mol Endocrinol 28:1221–1238CrossRefPubMedGoogle Scholar
  23. 23.
    Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J (2014) The placenta harbors a unique microbiome. Sci Transl Med 6:237ra65CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Isolauri E, Rautava S, Collado MC, Salminen S (2015) Probiotics in reducing the risk of gestational diabetes. Diabetes Obes Metab 17:713–719CrossRefPubMedGoogle Scholar
  25. 25.
    Mändar R, Punab M, Borovkova N, Lapp E, Kiiker R, Korrovits P et al (2015) Complementary seminovaginal microbiome in couples. Res Microbiol 166:440–447CrossRefPubMedGoogle Scholar
  26. 26.
    Rautava S, Collado MC, Salminen S, Isolauri E (2012) Probiotics modulate host-microbe interaction in the placenta and fetal gut: a randomized, double-blind, placebo-controlled trial. Neonatology 102:178–184CrossRefPubMedGoogle Scholar
  27. 27.
    Satokari R, Grönroos T, Laitinen K, Salminen S, Isolauri E (2009) Bifidobacterium and Lactobacillus DNA in the human placenta. Lett Appl Microbiol 48:8–12CrossRefPubMedGoogle Scholar
  28. 28.
    Wassenaar TM, Panigrahi P (2014) Is a foetus developing in a sterile environment? Lett Appl Microbiol 59:572–579CrossRefPubMedGoogle Scholar
  29. 29.
    DiGiulio DB (2012) Diversity of microbes in amniotic fluid. Semin Fetal Neonatal Med 17:2–11CrossRefPubMedGoogle Scholar
  30. 30.
    Zheng J, Xiao X, Zhang Q, Mao L, Yu M, Xu J (2015) The placental microbiome varies in association with low birth weight in full-term neonates. Nutrients 7:6924–6937CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Ardissone AN, de la Cruz DM, Davis-Richardson AG, Rechcigl KT, Li N, Drew JC et al (2014) Meconium microbiome analysis identifies bacteria correlated with premature birth. PLoS One 9(3):e90784CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Gosalbes MJ, Llop S, Vallès Y, Moya A, Ballester F, Francino MP (2013) Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin Exp Allergy 43:198–211CrossRefPubMedGoogle Scholar
  33. 33.
    Hansen R, Scott KP, Khan S, Martin JC, Berry SH, Stevenson M et al (2015) First-pass meconium samples from healthy term vaginally-delivered neonates: an analysis of the microbiota. PLoS One 10(7):e0133320. doi: 10.1371/journal.pone.0133320 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P et al (2015) Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17:690–703CrossRefPubMedGoogle Scholar
  35. 35.
    Salminen S, Endo A, Isolauri E, Scalabrin D (2016) Early gut colonization with Lactobacilli and Staphylococcus in infants: the hygiene hypothesis extended. J Pediatr Gastroenterol Nutr 62(1):80–86Google Scholar
  36. 36.
    Gueimonde M, Laitinen K, Salminen S, Isolauri E (2007) Breast milk: a source of bifidobacteria for infant gut development and maturation? Neonatology 92:64–66CrossRefPubMedGoogle Scholar
  37. 37.
    Cabrera-Rubio R, Collado MC, Laitinen K, Salminen S, Isolauri E, Mira A (2012) The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr 96:544–551CrossRefPubMedGoogle Scholar
  38. 38.
    Hunt KM, Foster JA, Forney LJ, Schütte UM, Beck DL, Abdo Z et al (2011) Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS One 6:e21313CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Jost T, Lacroix C, Braegger C, Chassard C (2015) Impact of human milk bacteria and oligosaccharides on neonatal gut microbiota establishment and gut health. Nutr Rev 73:426–437CrossRefPubMedGoogle Scholar
  40. 40.
    Urbaniak C, Cummins J, Brackstone M, Macklaim JM, Gloor GB, Baban CK et al (2014) Microbiota of human breast tissue. Appl Environ Microbiol 80:3007–3014CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Grześkowiak Ł, Sales Teixeira TF, Bigonha SM, Lobo G, Salminen S, Ferreira CL (2015) Gut Bifidobacterium microbiota in one-month-old Brazilian newborns. Anaerobe 35:54–58CrossRefPubMedGoogle Scholar
  42. 42.
    Grześkowiak Ł, Collado MC, Mangani C, Maleta K, Laitinen K, Ashorn P et al (2012) Distinct gut microbiota in southeastern African and northern European infants. J Pediatr Gastroenterol Nutr 54:812–816CrossRefPubMedGoogle Scholar
  43. 43.
    Rodríguez JM, Murphy K, Stanton C, Ross RP, Kober OI, Juge N et al (2015) The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis 26. doi: 10.3402/mehd.v26.26050
  44. 44.
    Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R et al (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA 108(Suppl 1):4578–4585CrossRefPubMedGoogle Scholar
  45. 45.
    Subramanian S, Blanton LV, Frese SA, Charbonneau M, Mills DA, Gordon JI (2015) Cultivating healthy growth and nutrition through the gut microbiota. Cell 161:36–48CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Endo A, Pӓrtty A, Kalliomӓki M, Isolauri E, Salminen S (2014) Long-term monitoring of the human intestinal microbiota from the 2nd week to 13 years of age. Anaerobe 28:149–156CrossRefPubMedGoogle Scholar
  47. 47.
    Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA et al (2014) Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 510:417–421PubMedPubMedCentralGoogle Scholar
  48. 48.
    Lang JM, Eisen JA, Zivkovic AM (2014) The microbes we eat: abundance and taxonomy of microbes consumed in a day’s worth of meals for three diet types. Peer J 2:e659. doi: 10.7717/peerj.659 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Dogra S, Sakwinska O, Soh SE, Ngom-Bru C, Brück WM, Berger B et al (2015) GUSTO study group. Dynamics of infant gut microbiota are influenced by delivery mode and gestational duration and are associated with subsequent adiposity. MBio 6, pii:e02419-14Google Scholar
  50. 50.
    Scheepers LE, Penders J, Mbakwa CA, Thijs C, Mommers M, Arts IC (2015) The intestinal microbiota composition and weight development in children: the KOALA Birth Cohort Study. Int J Obes (Lond) 39:16–25CrossRefGoogle Scholar
  51. 51.
    Vael C, Verhulst SL, Nelen V, Goossens H, Desager KN (2011) Intestinal microflora and body mass index during the first three years of life: an observational study. Gut Pathog 3:8. doi: 10.1186/1757-4749-3-8 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Kozyrskyj AL, Kalu R, Koleva PT, Bridgman SL (2016) Fetal programming of overweight through the microbiome: boys are disproportionately affected. J Dev Orig Health Dis 7(1):25–34Google Scholar
  53. 53.
    Galley JD, Bailey M, Kamp Dush C, Schoppe-Sullivan S et al (2014) Maternal obesity is associated with alterations in the gut microbiome in toddlers. PLoS One 9:e113026CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Karlsson CL, Onnerfält J, Xu J, Molin G, Ahrné S, Thorngren-Jerneck K (2012) The microbiota of the gut in preschool children with normal and excessive body weight. Obesity 20:2257–2261CrossRefPubMedGoogle Scholar
  55. 55.
    Cox LM, Yamanishi S, Sohn J, Alekseyenko AV, Leung JM, Cho I et al (2014) Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 158:705–721CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI (2011) Human nutrition, the gut microbiome and the immune system. Nature 474:327–336CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Belkaid Y, Hand TW (2014) Role of the microbiota in immunity and inflammation. Cell 157:121–141CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Vrieze A, Holleman F, Zoetendal EG, de Vos WM, Hoekstra JB, Nieuwdorp M (2010) The environment within: how gut microbiota may influence metabolism and body composition. Diabetologia 53:606–613CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Bäckhed HK et al (2012) Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150:470–480CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    MacIntyre DA, Chandiramani M, Lee YS, Kindinger L, Smith A, Angelopoulos N et al (2015) The vaginal microbiome during pregnancy and the postpartum period in a European population. Sci Rep 5:8988CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Adriaens LM, Alessandri R, Spörri S, Lang NP, Persson GR (2009) Does pregnancy have an impact on the subgingival microbiota? J Periodontol 80:72–81CrossRefPubMedGoogle Scholar
  62. 62.
    Borgo PV, Rodrigues VA, Feitosa AC, Xavier KC, Avila-Campos MJ (2014) Association between periodontal condition and subgingival microbiota in women during pregnancy: a longitudinal study. J Appl Oral Sci 22:528–533CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Antony KM, Ma J, Mitchell KB, Racusin DA, Versalovic J, Aagaard K (2015) The preterm placental microbiome varies in association with excess maternal gestational weight gain. Am J Obstet Gynecol 212:653.e1–653.e16CrossRefGoogle Scholar
  64. 64.
    Santacruz A, Collado MC, García-Valdés L, Segura MT, Martín-Lagos JA, Anjos T et al (2010) Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr 104:83–92CrossRefPubMedGoogle Scholar
  65. 65.
    Collado MC, Isolauri E, Laitinen K, Salminen S (2008) Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr 88:894–899PubMedGoogle Scholar
  66. 66.
    Collado MC, Laitinen K, Salminen S, Isolauri E (2012) Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatr Res 72:77–85CrossRefPubMedGoogle Scholar
  67. 67.
    Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo GFiere N, Knight R (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA 107:11971–11975CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C et al (2014) Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut 63:559–566CrossRefPubMedGoogle Scholar
  69. 69.
    Salminen S, Gibson GR, McCartney AL, Isolauri E (2004) Influence of mode of delivery on gut microbiota composition in seven year old children. Gut 53:1388–1389CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Kero J, Gissler M, Grönlund MM, Kero P, Koskinen P, Hemminki E, Isolauri E (2002) Mode of delivery and asthma—is there a connection? Pediatr Res 52:6–11PubMedGoogle Scholar
  71. 71.
    Huurre A, Kalliomäki M, Rautava S, Rinne M, Salminen S, Isolauri E (2008) Mode of delivery—effects on gut microbiota and humoral immunity. Neonatology 93:236–240CrossRefPubMedGoogle Scholar
  72. 72.
    Miettinen R, Hermansson H, Merkikukka M, Gissler M, Isolauri E (2015) Mode of delivery—impact on risk of non-communicable diseases. J Allergy Clin Immunol pii: S0091–6749(15):00782-4. doi: 10.1016/j.jaci.2015.05.032
  73. 73.
    Kuhle S, Tong OS, Woolcott CG (2015) Association between caesarean section and childhood obesity: a systematic review and meta-analysis. Obes Rev 16:295–303CrossRefPubMedGoogle Scholar
  74. 74.
    Mueller NT, Whyatt R, Hoepner L, Oberfield S, Dominguez-Bello MG, Widen EM et al (2015) Prenatal exposure to antibiotics, cesarean section and risk of childhood obesity. Int J Obes (Lond) 39:665–670CrossRefGoogle Scholar
  75. 75.
    Blustein J, Attina T, Liu M, Ryan AM, Cox LM, Blaser MJ et al (2013) Association of caesarean delivery with child adiposity from age 6 weeks to 15 years. Int J Obes (Lond) 37:900–906CrossRefGoogle Scholar
  76. 76.
    Dethlefsen L, Huse S, Sogin ML, Relman DA (2008) The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 6:e280CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Fouhy F, Guinane CM, Hussey S, Wall R, Ryan CA, Dempsey EM et al (2012) High-throughput sequencing reveals the incomplete, short-term recovery of infant gut microbiota following parenteral antibiotic treatment with ampicillin and gentamicin. Antimicrob Agents Chemother 56:5811–5820CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Tanaka S, Kobayashi T, Songjinda P, Tateyama A, Tsubouchi M, Kiyohara T et al (2009) Influence of antibiotic exposure in the early postnatal period on the development of intestinal microbiota. FEMS Immunol Med Microbiol 56:80–87CrossRefPubMedGoogle Scholar
  79. 79.
    Arboleya S, Sánchez B, Milani C, Duranti S, Solís G, Fernández N et al (2015) Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics. J Pediatr 166:538–544CrossRefPubMedGoogle Scholar
  80. 80.
    Cani PC, Delzenne NM (2009) The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des 15:1546–1558CrossRefPubMedGoogle Scholar
  81. 81.
    Nobel YR, Cox LM, Kirigin FF, Bokulich NA, Yamanishi S, Teitler I et al (2015) Metabolic and metagenomic outcomes from early-life pulsed antibiotic treatment. Nat Commun 6:7486. doi: 10.1038/ncomms8486 CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Persaud RR, Azad MB, Chari RS, Sears MR, Becker AB, Kozyrskyj AL et al (2014) Perinatal antibiotic exposure of neonates in Canada and associated risk factors: a population-based study. Matern Fetal Neonatal Med 14:1–6Google Scholar
  83. 83.
    Saari A, Virta LJ, Sankilampi U, Dunkel L, Saxén H (2015) Antibiotic exposure in infancy and risk of being overweight in the first 24 months of life. Pediatrics 135:617–626CrossRefPubMedGoogle Scholar
  84. 84.
    Bailey LC, Forrest CB, Zhang P, Richards TM, Livshits A, DeRusso PA (2014) Association of antibiotics in infancy with early childhood obesity. JAMA Pediatr 168:1063–1069CrossRefPubMedGoogle Scholar
  85. 85.
    Makino H, Kushiro A, Ishikawa E, Kubota H, Gawad A, Sakai T et al (2013) Mother-to-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant’s microbiota. PLoS One 8:e78331CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Jost T, Lacroix C, Braegger CP, Rochat F, Chassard C (2014) Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ Microbiol 16:2891–2904CrossRefPubMedGoogle Scholar
  87. 87.
    Pacheco AR, Barile D, Underwood MA, Mills DA (2015) The impact of the milk glycobiome on the neonate gut microbiota. Annu Rev Anim Biosci 3:419–445CrossRefPubMedGoogle Scholar
  88. 88.
    Jost T, Lacroix C, Braegger C, Chassard C (2013) Assessment of bacterial diversity in breast milk using culture-dependent and culture-independent approaches. Br J Nutr 110:1253–1262CrossRefPubMedGoogle Scholar
  89. 89.
    Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS et al (2013) Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ 185:385–394CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Biesbroek G, Bosch AA, Wang X, Keijser BJ, Veenhoven RH, Sanders EA et al (2014) The impact of breastfeeding on nasopharyngeal microbial communities in infants. Am J Respir Crit Care Med 190:298–308CrossRefPubMedGoogle Scholar
  91. 91.
    Albenberg LG, Wu GD (2014) Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology 146:1564–1572CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM et al (2007) Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50:2374–2383CrossRefPubMedGoogle Scholar
  93. 93.
    Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B et al (2014) Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11:506–514CrossRefPubMedGoogle Scholar
  94. 94.
    Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis EL, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031CrossRefPubMedGoogle Scholar
  95. 95.
    Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE et al (2009) A core gut microbiome in obese and lean twins. Nature 457:480–484CrossRefPubMedGoogle Scholar
  96. 96.
    Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3:213–223CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023CrossRefPubMedGoogle Scholar
  98. 98.
    Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL et al (2013) Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341:1241214. doi: 10.1126/science.1241214 CrossRefPubMedGoogle Scholar
  99. 99.
    Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489:242–249CrossRefPubMedGoogle Scholar
  100. 100.
    Osborn O, Olefsky JM (2012) The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med 18:363–374CrossRefPubMedGoogle Scholar
  101. 101.
    Tremaroli V, Karlsson F, Werling M, Ståhlman M, Kovatcheva-Datchary P, Olbers T et al (2015) Roux-en-Y gastric bypass and vertical banded gastroplasty induce long-term changes on the human gut microbiome contributing to fat mass regulation. Cell Metab 22:228–238CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The American Physiological Society 2016

Authors and Affiliations

  • Erika Isolauri
    • 1
    • 2
  • Samuli Rautava
    • 1
    • 2
  • Maria Carmen Collado
    • 3
  • Seppo Salminen
    • 4
  1. 1.Department of Paediatrics and Adolescent MedicineTurku University HospitalTurkuFinland
  2. 2.Department of Clinical Sciences, Faculty of MedicineUniversity of TurkuTurkuFinland
  3. 3.Institute of Agrochemistry and Food Technology-National Research Council (IATA-CSIC)BurjassotSpain
  4. 4.Functional Foods Forum, Faculty of MedicineUniversity of TurkuTurkuFinland

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